Phylogenetic relationships among extant brachiopods

cludi.stics(1995) 11:131-197

PHYLOGENETIC RELATIONSHIPS EXTANT BRACHIOPODS

AMONG

Sandra J. Carlson Dqbartment of Geology, Universig of California, Davis, iXij&mia 956168605, U.S.A. l&wivedfar public&m 22 September1993; amped 22 June 1994 Abstract-The monophyletic status of the Brachiopoda and phylogenetic relationships within the phylum have long been contentious issues for brachiopod systematists. The relationship of brachiopods to other lophophorebearing taxa is also uncertain; results from recent morph* logical and molecular studies are in conflict To test current hypotheses of relationship, a phylogenetic analysis was completed (using PAUP X1.1) with 112 morphological and embryological characters that vary among extant representatives of seven brachiopod superfamilies. using bryozoans, phoronids, pterobranchs and sipunculids as outgroups. In the range of analyses performed, brachiopod monophyly is well suppormd, particularly by characters of soft anatomy. Arguments concerning single or multiple origins of a bivalved shell are not relevant to recognizing brachiopods as a clade. Articulate monophyly is very strongly supported, but inarticulate monophyly receives relatively weak support Unlike previous studies, the nature of uncertainties about the clade status of Inarticulata are detailed explicitly here, making them easier to test in the future. Calcareous inarticulates appear to share derived characters with the other inarticulates, while sharing many primitive characters with other calcareous brachiopods (the articulates). Experimental manipulation of the data matrix reveals potential sources of bias in previous hypotheses of bmchiopod phylogeny. Although not tested explicitly, lophophomte monophyly is very tentatively supported. Molecular systematic studies of a diverse group of brachiopods and other lophophorates will be particularly welcome in providing a test of the conclusions presented here. 0 1995 The Wti

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Brachiopods were the most abundant and diverse skeletonized marine invertebrates throughout most of the Paleozoic era -a period of over 300 Myr of evolutionary history. Because they are well-preserved and easily collected as fossils, and occur in many different paleoenvironmental settings, brachiopods play an extremely important role in biostratigraphy, paleobiogeography, paleoecology, functional morphology and evolutionary paleobiology. Although they occur at substantially lower diversity today, they remain a significant and locally abundant faunal element in temperate and high latitude environments (e.g. Foster, 1974; Noble et al., 1976; Logan, 1979; Curry, 1982; Lee, 1991). Despite the paleontological significance of brachiopods, classifications of their morphological diversity, and the phylogenetic relationships they imply, have been contentious for well over a century (e.g. Ring, 1846; Waagen, 1882-1885; Beecher, 1892; Schuchert, 1893; Walcott, 1912; Thomson, 1927; Williams, 1956; Williams and Rowell, 1965; Rudwick, 1970). The history of brachiopod classification (MuirWood, 1955; Williams and Rowell, 1965) chronicles a series of organizational schemes based largely on single “key” characters: the disposition of the lophophore between the valves (Gray, 1848), the presence and orientation of the pedicle relative to the valves (Beecher, 1892; Schuchert, 1897) and the nature of articulation (or lack thereof) between the valves (Huxley, 1869). Brachiopod systematists, to 07483007/95/0?0131+67$12.00/0

0 1995 The Wdti Hennig

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their credit, have consistently attempted to establish brachiopod higher taxa on some defensible phylogenetic basis. Existing classifications were abolished, and new ones adopted, with the explicitjustification that classification must be founded on “the facts of evolution” (Schuchert, 1893) and must reflect (to every extent possible) hypothesized phylogenetic relationships. Despite these good intentions, numerous problems with brachiopod systematics remain at several levels of analysis. Results from recent studies in paleontology, embryology and molecular systematits have brought some of the problems into clear focus. Valentine (1975) and Wright (1979) argued that the brachiopods are polyphyletic, having evolved a bivalved shell several times independently from different infaunal, lophophorebearing organisms lacking mineralized skeletons (Fig. 1A; see also Willmer, 1990). In a morphological cladistic analysis of the extant brachiopods, Rowe11 (1981a,b, 1982) presented evidence to support the monophyly of the phylum Brachiopoda, and the classes Inarticulata and Articulata (Fig. 1B). This is consistent with the current classification of the phylum, which recognizes two classes based on the nature of articulation between the valves (Table 1; Williams and Rowe& 1965; Williams and Hurst, 1977). Corjansky and Popov (1985, 1986) and Popov (1992) disputed Rowell’s results and claimed that brachiopods (and the inarticulates) are diphyletic, and that the classification should be revised to reflect similarity in shell mineralogy rather than valve articulation (Fig. 1C). Following further analysis, this proposal was modified (Holmer, 1991; Popov et al., 1993) to suggest that

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Fig. 1. Hypotheses of phylogenetic relationships among the major taxa of extant brachiopods. (A) Brachiopod (and inarticulate) polyphyly. (B) Brachiopod (and inarticulate) monophyly. (C) Brachiopod (and inarticulate) diphyly. (D) Brachiopod monophyly, inarticulate paraphyly. Filled circles indicate inarticulate brachiopods; open circles indicate extinct taxa.

BRACHIOPOD

PHYLOGENY

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Table 1 Current classification of all named extant brachiopod genera, following Williams and Rowe11 (1965) and R Doescher (pers. comm., 1993). Italicized species listed after superfamily name indicate the species most frequently representing the superfamily in these analyses. Brachiopoda Inarticulata Craniacea: Crania anomoln Ancislrocmnia, Crania, Craniscus, Neoancistnxrania, Neocrania, Valdiviathyris Discinacea: D&in&u lamellosa Dtkina, Did&a [ P&gvdiscus] , Discradisca Lingulacea: LinguIa anatinq GhtidiaPyramiahkz GIoUidia, Lingulu Articulata Rhynchonellacea: Hemithirispsittacea, Notosatia nigkans Abyssorhynchia, Amnthabadioh, Aetheia, Auiites, Basiliola, BasilioL&, Gnnpsoth~, C+opora, Eohemithiris, Frieleia, Grammetatia, Hemithiric, Hispanirhynchia, Manithyris, Neorhynchia, Notosaria, Pemphixina, Rhytirhynchia, Striarina, Teguhhynchia Terebratellacea: Terebmtalia transversa, Wdtonia inconspk-ua Aerothyris, Akiingiu, Amphithyris, Anahineticn, Anebowncha, Anndopkatidia, Avtheca, Bouchardia, Campages, Compsoria, Coptothyris, Dallinu, DaUineUa, Diestathyks, Dysc&zia, Economiosa, Fallax, Fosleria, Fnmulina, Gkuiarcukz, Gupia, GyWhyris, Jaffaia, Japanithyris, Jobmica, Kkssina, Lqueus, LeptothyreUa, MacandreGa, Magodinu, MagaseUa, Magella, Magellania, Megathiris, Me&& Megerlina, Neothyris, Nipponithyris, Nototygmia, Pacifilyris, Pant&k, Parokineticn, Phaneropora, Pictothyris, Piroth*, Platidia, l%milus, septiwllatina, Simplitithyris, Stethothyk, Syntomak, Terebrakalia, Tetzbratella, Thaumatosia, Tisimania, Tythothyris, Waltonia Terebratulacea: Terebratulinu retusa, T. unguiculo, T. s+enhwnalis Abyssothyris, Acmbeksia, Acrobrochus, A&ha&a, Arc&a, Bathynanus, Gsncellothyks, Chlidunophora, Cnismatocentvum, Dallithyris, Dolickygus, Dyswlia, Dysedrosia, Epacrosina, Etymnia, Eucalathis, Eurysinu, Goniobrochus, c;lyphus, Liothyrellu, Murravia, Stenobrochus, Stenosarina, Sunqathyris, Terebratulina, Tichosina, Xenobrochw, Zygtmaria Thecideacea: Thecio!eUina b.Wzmanni, Lauwdla diterranea LacazeUu, Pajaudina, Th&okUina

brachiopods are monophyletic, but that the inarticulates are paraphyletic (Fig. lD), a hypothesis proposed earlier by both Hennig (1966) and Forey (1982). This view recently received indirect corroboration from Nielsen (1991)) who suggested on the basis of new embryological data that the calcareous inarticulates share more recent common ancestry with the calcareous articulates than with the other (phosphatic) inarticulates. The results of these studies of intraphylum relationships are compelling in their own right, but each has typically considered only a relatively small number of characters, many for which homology and polarity are questionable. The purpose of this study is to analyze phylogenetic relationships among all extant brachiopods in order to investigate the phylogenetic status of currently recognized higher taxa and, in the process, test the results of previous studies. In a preliminary study of the phylogenetic relationships among brachiopod higher taxa, I assembled and analyzed a large body of comparative morphological and embryological information (Carlson, 1989, 1991a,b). The results obtained were generally consistent with Rowell’s conclusions; brachiopod monophyly was supported by fairly robust apomorphies and inarticulate monophyly was tentatively supported by relatively weak apomorphies. Since then, the initial data matrix has been thoroughly revised to eliminate redundant characters, and add other informative characters as they became known. A complete description of all the characters used and the results obtained form the basis of this study.

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Focusing exclusively on the extant brachiopods only has several advantages. Information on a wider range of characters (including soft anatomy and embryology) can be used with extant taxa than extinct taxa. The results can be tested by molecular studies on living taxa. The primary disadvantage, a significant one from a paleontological point of view, is that only a very narrow range of (and presumably genotype) is being sampled. As a brachiopod “morphospace” rough comparison of taxonomic diversity (which approximates morphological diversity), only seven (possibly eight, see Cooper, 1973) brachiopod superfamilies currently recognized are extant; 41 are extinct (Williams and Rowell, 1965). Preliminary results that included both fossil and Recent taxa (Carlson, 1991a,b) are being reanalyzed currently. First, obtaining a hypothesis of relationship among the extant taxa only will allow me to test whether, in brachiopod phylogenetic

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Fig. 2. Hypotheses of phylogenetic relationships among the lophophorates (filled circles) and their relationship to the protostomes and deuterostomes. (A) Lophophorate monophyly. (B) Lophophorate paraphyly. (C) Lophophorate polyphyly. (D) Metazoan phylogeny based on 18s rRNA sequence data. Note position of brachiopods (Lingula rcev) with molluscs.

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inference, fossils can and will overturn results obtained using extant taxa only (Patterson, 1981; Gauthier et al., 1988; Donoghue et al., 1989). Not only are phylogenetic relationships within the phylum contentious, but from the broader perspective of metazoan phylogeny, the relationship of brachiopods to other metazoans is also controversial (Fig. 2). Do brachiopods share most recent common ancestry with the other lophophorates (Emig, 1977, 1984)? Are they more closely related to the protostomes or the deuterostomes? Using the data and methods of molecular systematics, Field et al. (1988; see also Ghiselin, 1988; Patterson, 1989; Lake, 1990) investigated metazoan phylogeny by analyzing 18s rRNA sequences in a range of species, including LinguZu reevi (an inarticulate brachiopod). Their results suggest that brachiopods are most closely related to the (paraphyletic) molluscs, a conclusion quickly adopted by a number of paleontologists (Runnegar, 1992; Valentine, 1992; Conway Morris, 1993). This runs surprisingly contrary to a large amount of morphological and embryological data, which indicate strongly that brachiopods share more recent common ancestry with the hemichordates and other deuterostomes, than the protostomes (Brusca and Brusca, 1990; Willmer, 1990; Schram, 1991; Meglitsch and Schram, 1991; Eemisse et al., 1992). This seemingly irreconcilable conflict underscores the importance of a reanalysis of the full body of available morphological and embryological data bearing on the phylogenetic relationships of the extant brachiopods.

Methods

One hundred and twenty-two genera of extant brachiopods are classified in seven superfamilies and two classes (Table 1; Williams and Rowe& 1965). Forty-three genera have been named since 1965; not all may be valid. An eighth extant superfamily was named by’cooper (1973); because I was unable to examine specimens of the two genera initially included within, I chose not to include the Cancellothyridacea in this analysis. As a compromise between feasibility and taxonomic detail, brachiopod superfamilies were chosen as the terminal taxa in this study. This choice may prove to be problematic because the monophyly of named superfamilies has ‘not been tested rigorously. Superfamilies are widely recognized to be “good” taxonomic groups, and most have remained recognizable and defensible (at some rank) through several previous higher level classifications, but it is possible that at least some are not clades. To proceed with the investigation, however, the (testable) assumption that named taxa are monophyletic must be accepted, at least provisionally. Phylogenetic analyses of genera and species within named superfamilies are currently being conducted in preparation for the revision of the Treatise on Invertebrate Pakwntolo~ (expected publication, 1995; Williams and Rowell, 1965). Results from these ongoing studies have the potential to affect the results presented here. When possible, a single species was selected to represent the superfamily as the terminal taxon (Table 1). Relatively little comparative phylogenetic work within superfamilies exists, and intrasuperfamily (extant) diversity is often low, so this was seldom a problem. This strategy has the advantage that within-taxon character

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polymorphisms will not obscure the analysis. In the higher-diversity articulate super-families, however, I combined any information I could extract from the literature and coded character states per superfamily as a composite. In other words, information on embryology may have come from a study of one species, and information on the blood vascular system from another species. Because within-taxon relationships are not well characterized for all superfamilies, it is not yet possible to distinguish unambiguously primitive from derived states, within taxa. Ideally, only those character states known to be “basal” for the superfamily would be included, as features derived later in the evolution of the group have the potential to obscure the phylogenetic pattern. This strategy therefore runs the risk of coding a taxon as a combination of primitive and derived characters. Future intrasuperfamily analyses are necessary to test this possibly weak assumption. The seven superfamilies with extant representatives are easily distinguished from one another. All inarticulates lack a tooth-and-socket hinge mechanism allowing the articulation of the two valves; all have spirolophous lophophores. Lingulaceans are free-living, phosphatic inarticulates with long pedicles, that burrow into soft substrates using a “scissoring” action of the two valves (see Savazzi, 1991). Discinaceans are phosphatic inarticulates attached to hard substrates with short pedicles. Craniaceans are calcareous inarticulates cemented to hard substrata by their ventral valves. All articulates have calcareous shells. Thecideaceans are tiny articulates with a ptycholophe lophophore and a punctate shell structure; they live cemented to hard substrates by their ventral valves. Rhynchonellaceans are impunctate pediculate articulates with spirolophe lophophores. Terebratulides are punctate pediculate articulates with a calcareous loop supporting a plectolophe lophophore; terebratulaceans have a short loop, while terebratellaceans have a long loop. Throughout, I use informal taxon designations (e.g. inarticulates for Inarticulata, terebratulides for Terebratulida, rhynchonellaceans for Rhynchonellacea) that refer to groups of brachiopods currently classified in various higher taxa. The phylogenetic status, relative taxonomic rank and lower-level classification of these named taxa are all in the process of being evaluated for the Treatise revision. Thus, the informal name is used to convey some sense of the brachiopods in question, without placing undue emphasis on the rank of the taxon name itself. The main purpose of this study is to investigate phylogenetic relationships among brachiopod superfamilies. Formally revising brachiopod higher-level classification is a separate, subsequent endeavor, and is beyond the scope of the present paper. CHARACTERS Information was compiled primarily from the literature on 112 characters of embryology, reproductive and larval biology, soft anatomy (coelom, mantles, setae, pedicle, lophophore, and digestive, excretory, circulatory, respiratory, nervous and muscular systems), mode of life, and skeletal anatomy (shell structure and mineralization, valve form and ornament, articulation and the hinge region, and dorsal and ventral valve interiors, including the pedicle opening, calcareous lophophore supports, and mantle canal markings; see Appendix 2). Because character data from any single body region or life history stage may be prone to

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certain kinds of homoplasy, using all character data together will, ideally, ensure the most comprehensive results. No attempt was made to eliminate characters thought to be homoplastic prior to performing the analyses, under the assump tion that homoplasy would be revealed in the analysis itself by phylogenetic congruence with other putative homologues (Patterson, 1982). Additional positional or developmental information was considered, as relevant, in evaluating character homology (see descriptions of characters in Appendix 2 for specific examples). Both binary and multistate characters were recognized. All characters were unordered. All characters were weighted equally in the main analysis; all were reweighted according to their resealed consistency indices in a subsequent analysis. Selective weighting of character suites was performed in a series of experiments described after the main analysis. No characters were constrained to be irreversible. Despite the fact that all taxa are extant, many characters were coded as missing (Appendix l), for one of three different reasons. Either the character is not applicable to the taxon (e.g. pedicle type in a taxon lacking a pedicle), is simply not known for the taxon, or the states are variable among species in a superfamily (polymorphic). The cladogram topology is structured largely on the basis of coded characters. However, missing characters are increasingly viewed as playing a potentially significant role in cladogram construction (see Platnick et al., 1991; Nixon and Davis, 1991; Novacek, 1992; Maddison, 1993), particularly when the missing information is not distributed evenly across the data matrix (i.e. when a few taxa are very poorly known, while others are mostly complete). This can be a difficult problem to resolve operationally (Maddison, 1993; see Experiments section), even though the theoretical basis of the problem is readily acknowledged. POLARITYDETERMINATION Outgroup criteria were used to determine the direction of character transformation (Watrous and Wheeler, 1981). Four taxa were chosen as outgroups, each assumed to be monophyletic: Ectoprocta (= Bryozoa), Phoronida, Pterobranchia and Sipunculida. To polarize character change among the brachio-pods, the other two lophophorate phyla, Bryozoa and Phoronida, are logical choices, since many consider the lophophorates to be a clade (Emig, 1977, 1984; Brusca and Brusca, 1990; Willmer, 1990). However, the lophophorates are notorious for exhibiting a curious mixture of both protostome and deuterostome characters, which explains why they are commonly located somewhere between protostomes and deuterostomes in metazoan phylogenetic trees (e.g. Hadzi, 1953; Hyman, 1959; Jagersten, 1972; Willmer, 1990). For this reason, a protostome taxon (Sipunculida) and a deuterostome taxon (Pterobranchia) were added to the two lophophorate outgroups in order to include at least minimal representation of other metazoans. Pterobranchs (Brusca and Brusca, 1990; Willmer, 1990; Schram, 1991; Meglitsch and Schram, 1991) and sipunculids (Nichols, 1971; Field et al., 1988; Eernisse et al., 1992) were chosen because they have figured prominently in previous phylogenetic discussions featuring the lophophorates. Each of these taxa is problematic as a brachiopod outgroup, however. Only brachiopods have a bivalved shell (although see characters 62 and 63 in Appendix

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2); many aspects of their anatomy and development are fundamentally related to this bivalved Bauplan. Neither phoronids nor pterobranchs have mineralized skeletons or trustworthy body-fossil records (see Valentine, 1987). Some bryozoans have a mineralized skeleton, but are miniaturized and colonial and so different from brachiopods that they share very few hard-part characters with them. Some sipunculids mineralize small calcareous plates in their shields, but are morphologically very different from brachiopods. The fewer characters the outgroup taxa share with the ingroup, the less power they will have in shaping the polarity of character transformation within the ingroup. This is one of the unavoidable difficulties with morphological analyses, particularly among higher taxa with such ancient divergence times. When investigating patterns of relationship that were established over 500 Myr ago, it makes evolutionary sense to expect fairly high levels of convergence, parallelism and reversals in morphology. Even though this difficulty highlights the value of a test using molecular systematics (which can suffer from other types of methodological difficulties; see Wheeler, 1992)) morphology is still the most immediately accessible of all sources of information on phylogenetic relationships and will always play a significant role in phylogenetic inference. PHYLOGENETK

METHODS

A phylogenetic systematic methodology was employed to analyze genealogical relationships among the brachiopods (see Hennig 1966; Eldridge and Cracraft 1980; Wiley 1981). All analyses were conducted using the microcomputer program PAUP 3.1.1 (Phylogenetic Analysis Using Parsimony; Swofford, 1993). The results of three analyses form the basis of this study. I first performed a branch-and-bound search (identifies all optimal cladograms; see Swofford, 1993), and then an exhaustive search, guaranteed to find all the most parsimonious cladograms, and obtained a single most parsimonious cladogram. Three different optimization criteria were used and results compared (character transformations discussed in Appendix 2 following ACCTRAN optimization, unless otherwise noted). To obtain a rough measure of the stability of the cladogram, I compared the topologies of the 15 cladograms that were just one and two steps longer than the most parsimonious cladogram. Next, a bootstrap analysis of 1000 replicates using RANDOM CLADISTICS 2.1.1 (Siddall, 1995) with commands mh* bb* for Hennig86 (Farris, 1988) was calculated’. Any phylogenetic analysis is only as robust as the assumptions implicit in its methods. Particularly, given the ease with which microcomputer programs designed to reconstruct phylogenetic patterns can be used, it is important to experiment extensively with the data matrix and the program itself, to avoid accepting uncritically the first result obtained (e.g. Cann et al., 1987; Maddison et al., 1992). To this end, I experimented with removing individual taxa and suites of characters one by one, imposing character irreversibility, reweighting each of the characters based on their resealed consistency index in the first analysis, and weighting suites of characters arbitrarily, to explore the contribution of each to restructuring cladogram topology. ’ This

was performed

by D. Lipscomb.

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Results %-RET

PARSMONY

The branch-and-bound search and exhaustive search each yielded the same most parsimonious cladogram (hereafter abbreviated MPC) of length 224, with a consistency index (excluding uninformative characters) of 0.742 (Fig. 3). The brachiopods, inarticulates and articulates are each monophyletic. Craniaceans are the most primitive inarticulates, while thecideaceans are the most primitive articulates. Rooting the tree along the branch leading to either the pterobranchs or sipunculids instead of at the base of the ingroup, the lophophorates are also mono phyletic, with bryozoans and brachiopods as sister taxa and phoronids sharing more distant common ancestry with them. Different character state optimization criteria were compared in order to evaluate competing hypotheses of character transformation among these taxa (Fig. 4). Different optimizations of missing data or characters where outgroup states are equivocal will result in differences in branch length and number of apomorphies supporting each node, but usually not in cladogram topology. Branch lengths are best viewed conservatively as indicating the strength of character support per node rather than the rate of evolution between nodes. ACCTRAN (accelerated transformation) favors character reversals over parallelisms, and was used in the

Fig. 3. Topology of the single most parsimonious cladogram obtained under assumption of strict parsimony. Bryozoans, phoronids, pterobranchs and sipunculids as outgroups; cladogram rooted at base of ingroup (does not imply that pterobranchs and sipunculids are sister groups). Characters unweighted, unordered and fully reversible. Consistency index = 0.812 (minus uninformative characters = 0.742); retention index = 0.706, resealed consistency index = 0.574. Numbers beside nodes indicate the number of analyses supporting each node, out of 1000 branch-and-bound analyses in a bootstrap analysis. Apomorphies at nodes-k 4(0-l), 6(01), 13(0-l), 14(0-l), 16(0-2), 24(0-l), 36(0-l), 37(01), 39(0-l), 43(0-l), 44(0-l), 48(01), 49(0-2),51(0-l), 56(0-l). B: 2(1-2), 16(2-3), 25(0-l), 38(&l), 39(1-2), 40(@1), 43(1-2), lOO(l-2), 108(0-l), 112(2-3). C: 5(0-2). 7(10), 10(1-O), 11(1-O), 13(H), 14(10), 15(1-2), 19(2-O), 28(0-l), 29(01), 30(0-l), 37(1-2), 44(1-2), 58(2-o), 61(1-2), 62(2-O), 72(W), 79(1-O), 92(0-l), 94(0-l), 108(1-2). D: 5(0-l), 8(1-O), 120%2), 18(1-2),21(1-2),23(0-l), 28(02), 30(0-2), 31(01), 32(&l), 42(0-l), 44(1-3), 52(01), 54(0-l), 55(0-l), 65(0-l), 67(0-l), 68(0-2). 69(02), 70(01), 74(0-2), 77(0-l), 78(W), 80(02),82(0-l), 86(0-l), 87(W), 88(0-l), 89(02), 92(02), 96(@1), 102(01), 103(02), 105(01), lll(l-3). E: 9(1-2), 29(01), 57(0-l), 58(2-O), 64(1-2), 66(10), 73(0-l), 76(W), 88(13), 91(01), 98(0-l), 104(0-l). F: 12(2-l), 35(1-2), 36(1-O), 75(1-2), 84(0-l), 85(0-l), 106(1-2), 108(0-l), 110(1-2), ill(%).

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unguTheddeecee Rhynchonell ~Terebmtell I Terebmhd

I

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Fig. 4. Comparison of branch lengths of phylograms obtained using different character optimization options.(A) AC-, character transformations are accelerated, favoring reversals over parallelisms. (B) DELTRAN, character transformations are delayed, favoring parallelisms over reversals.(C) MINF; character transformations minimize the@aJue of Fan-is (1972).

analysis just described (26 parallelisms and 9 reversals). Character change is shifted to internode branches, away from terminal branches. DELTRAN delays character transformation and favors parallelisms over reversals (33 parallelisms and 1 reversal); terminal branches are often longer than in ACCTRAN optimization. MINF minimizes the fvalue of Far-r-is (1972) and substantially lengthens terminal branches, which can be especially problematic if ingroup relationships are close relative to the chosen outgroups. Using ACCTRAN, character states that are coded as missing in certain taxa are “predicted” by character congruence based on the topological distribution of known, coded states of other characters (see Swofford, 1993). For example, the origin of the coelomic spaces (character 19) is known to be schizocoelous only in lingulaceans (among the OTUs in this study), but its state in discinaceans is not yet known. ACCI’RAN resolves schizocoely as a synapomorphy of (Lingulacea t Discinacea) , but DELTRAN and MINF resolve schizocoely as an autapomorphy of Lingulacea.

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Character consistency necessarily deviates from 1.00 in characters that are universally (or locally) homoplastic in this analysis (Appendix 2). Of the 112 characters coded, 78 have consistency indices (CI) of 1.00, indicating that derived states evolved only once. Thirty-four characters have CI values between 0 and 1.00, which indicates that the states have evolved more than once independently (are globally homoplastic) but may be homologous at a lower level of universality (sensu Wiley, 1981). Forty-two are essentially uninformative because of missing (unknown) data that render one or more states autapomorphous. Even though uninformative, these characters have been retained in the analysis because at least some have the potential to become informative as additional information is made available. Consistency indices noted for cladograms exclude uninformative characters. RELAXED

PARSIMONY

To investigate the relative robustness of the topology obtained using strict parsimony, cladograms one and two steps longer than the shortest were examined. Five cladograms of length 225 and 10 cladograms of length 226 were obtained from the exhaustive search. Two additional ingroup topologies resulted (Fig. 5). Although the single MPC resolves inarticulate monophyly, one cladogram just one step longer (and 6 of the cladograms two steps longer) render the inarticulates BfyOZOa

A

Phoronlda Pterobranch Sipuncula Craniacea

FE

B

Rhynchonell Brebratell hbmtlll

Bry Bryozoa PhorOnida Pterobranch Sipuncula Craniacea DiedIMea Ungulacea

Phoronlda pterobmch Sipuncula DiaciMcea Ungulacea cmiawa Theddeacea Mvnchonell izzf Fig. 5. Topologies obtained monophyletic. (B) Brachiopods to all other brachiopods.(C) articulates as sister groups.

under a relaxed parsimony monophyletic, inarticulates Bmchiopods monophyletic,

model. (A) Brachiopods paraphyletic; craniaceans inarticulates paraphyletic;

and inarticulates as sister group craniaceans and

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paraphyletic, in one of two different configurations. These results indicate some critical nodes of the cladogram are not strongly supported.

that

Because of the instability detected above, a bootstrap analysis was performed (Fig. 3). Bootstrapping provides confidence limits (of sorts) on each node (see Felsenstein, 1985; Sanderson, 1989), and indicates which portions of the cladogram are more consistently supported by the data than others. This method is not without its detractors, in part because the bootstrap analysis produces a consensus cladogram, and consensus diagrams may not be topologically congruent with any of the MPCs in the initial analysis (see Miyamoto, 1985; Carpenter, 1988) (not a problem in this analysis). In addition, bootstrap results appear to be very poor estimates of repeatability and very conservative underestimates of phylogenetic accuracy (Hillis and Bull, 1993; see also Felsenstein and Rishino, 1993). However, unless rates of change are highly unequal, are high enough to randomize characters over time, or a systematic bias, such as lack of character independence, exists in the data, bootstrapping has value as a method for assessing confidence in phylogenetic analyses (Hillis and Bull, 1993). In this analysis, brachiopod (94%), inarticulate (75%), and articulate (98%) monophyly are variously supported. While inarticulate monophyly is supported in 75% of the 1000 bootstrap analyses, craniaceans are the sister group to the rest of the brachiopods in 19% of the analyses, and to the articulates in 19% of the analyses. EXPERIMENTS Reweighting the characters by the value of their resealed consistency indices yields a single MPC (length = 150994, CI = 0.917), with a topology identical to that in Figure 3. Not surprisingly, a bootstrap analysis of the reweighted characters provides stronger support for brachiopod (98%) and inarticulate (82%) monophyly, but slightly less support for articulate monophyly, than the unweighted bootstrap analysis. Craniaceans are the sister group to the articulates in 12 of 100 analyses, and to the rest of the brachiopods in 4 of 100 analyses. Weighting suites of characters by an arbitrary value generated interesting results. Weighting embryological characters (l-23) by two resulted in two MPCs, one comparable in topology to Figure 5A and one to Figure 5C. Weighting these same characters by three resulted in three MPCs, one comparable to Figure 5C and two in which brachiopods are nonmonophyletic (but articulates and inarticulates are each monophyletic) . Previous studies emphasizing the importance of embryological characters may have overly exaggerated the differences between the articulates and inarticulates. Weighting characters of soft anatomy (24-57), mode of life (58-60)) mineralization (61-71)) and skeletal anatomy (72-112) by three had no effect on ingroup (brachiopod) topology. Constraining all characters to be irreversible (but unordered) resulted in a single MPC with a much lower consistency index (length = 315, CI = 0.568) in which craniaceans and articulates are sister taxa (as in Fig. 5C). The shortest cladogram resolving inarticulate monophyly is seven steps longer (length = 323). Of all the characters used in this study, the evolutionary probability of reversal has been

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discussed in the literature for only a few. For example, planktotrophic larval ecology is widely considered to be primitive, while nonplanktotrophy is derived (character 14). Once nonplanktotrophy has evolved in a lineage, reversal to the planktotrophic condition is considered to be very unlikely (Strathmann, 1978, 1985) because so many anatomical features are lost or highly transformed in the process. When all characters are allowed to be fully reversible, nonplanktotrophy appears to evolve at least three times independently in pterobranchs, some sipunculid species, and brachiopods (Fig. 3). Planktotrophy does appear as a reversal once in (Lingulacea + Discinacea), in apparent conflict with the irreversibility “rule.” It is only slightly less parsimonious, however, to interpret this pattern in a manner consistent with Strathmann’s rule (using DELTRAN character state optimization). Rather than originating once in brachiopods, nonplanktotrophy may have originated twice independently in the craniaceans and the articulates, while (Lingulacea + Discinacea) retain the primitive planktotrophic condition. As an experiment, I specified that only character 14 be irreversible; 13 MPC (length = 224, CI = 0.742) resulted, primarily affecting relationships among the outgroups. Inarticulates are monophyletic in nine cladograms. In six of the 13, brachiopods are nonmonophyletic; in four of these six, inarticulates are also nonmonophyletic. Craniaceans are not the sister group to the articulates in any of the 13 cladograms. Character suites were removed by character type (Appendix 2), one by one, to evaluate their effect on cladogram topology. Removing all characters of soft anatomy (2457) simultaneously resulted in four MPCs, none of which support brachiopod monophyly. Of these soft anatomical characters, only characters of the lophophore (33-41) affected the original topology when removed. Specifically, removing either character 38 or 40 resulted in two MPCs comparable to Figures 5A and C. Removing taxa one by one also had an effect on cladogram topology. Among the ingroup, only thecideaceans, when removed, resolved craniaceans as the sister group to the articulate brachiopods in one of four MPCs (Fig. 5C); the other three MPCs resolved craniaceans as sister group to the rest of the brachiopods (Fig. 5B). Removing any other single ingroup taxon had no effect on cladogram topology. Among the outgroup, only sipunculids, when removed, resolved craniaceans as the sister group to the articulate brachiopods in one of two MPCs (Fig. 5C) and to the other inarticulates in the other MPC (Fig. 5A). Analyzing relationships among the ingroup taxa using each of the four outgroups individually (and deleting the other three outgroup taxa) does not affect ingroup relationships as resolved in Figure 5A. However, pairing the outgroups does have an effect. Three of the six pairs of outgroups alter topology in one of the two MPCs resulting from each analysis: phoronids and pterobranchs as outgroups result in topologies 5A and 5B; bryozoans and sipunculids, and bryozoans and pterobranchs result in topologies 5A and 5C. To investigate the effects of missing data, I performed three experiments. First, I coded polymorphic states in the 13 characters in which they occur (see Appendix 2) as polymorphisms rather than as “missing” (Nixon and Davis, 1991) and analyzed the new data set using MacClade 3.0 (PAUP 3.1.1 does not yet allow differentiation between polymorphisms and real uncertainties in a single data set). Cladogram length increased, as expected, but the topology of the shortest cladogram (length = 245) remained the same as in the original analysis (Fig. 3). Resolving craniaceans as the sister group to the articulates (Fig. 5C) generated a

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cladogram one step longer; resolving craniaceans as the sister group to all other brachiopods (Fig. 5B) generated a cladogram two steps longer. The small number and particular distribution of polymorphisms in this data set does not appear to have a major effect on cladogram topology. Next, I coded all inapplicable characters as a separate state indicating “not present” rather than “missing” (Maddison and Maddison, 1992; Maddison, 1993), and left the polymorphisms coded as polymorphisms (as above). MacClade 3.0 resolved this data set most parsimoniously with craniaceans either as the sister group to all other brachiopods or to the articulates alone (length = 309). Inarticulate monophyly was resolved in a cladogram one step longer. Finally, I recoded the polymorphisms as “missing” once again, but left the inapplicable characters as “not present” and analyzed the data set using PAUP 3.1.1 (branch-and-bound search). Five MPCs resulted (length = 288, CI = 0.821); four resolved craniaceans as the sister group to all other brachiopods (Fig. 5B) and one as the sister group to the articulates (Fig. 5C). Ten cladograms one step longer presented a range of topologies: craniaceans are the sister group to the other inarticulates in four cladograms, to the articulates in three cladograms, and to all other brachiopods in three cladograms. Reweighting the characters by their resealed consistency indices generated a single MPC (length = 229882, CI = 0.899) with craniaceans as the most primitive brachiopods (Fig. 5B). A bootstrap analysis of the unweighted characters resulted in a consensus diagram of the same topology (Fig. 5B): brachiopod and articulate monophyly were supported in 100% of the analyses, all brachiopods except for craniaceans in 53%, craniaceans with the articulates in 38%, and craniaceanswith the other inarticulates in 13%. The practical difficulties with coding inapplicable characters are discussed clearly in Maddison (1993). Because of the very large number of characters of skeletal anatomy (related to the bivalved shell; characters 72-112) that differentiate sub clades within the brachiopods, but do not apply to any of the outgroups that all lack two valves, it is not practical to use a very large step matrix (Maddison, 1993) to accommodate these ingroup distinctions. Leaving the inapplicable characters coded as a separate state “not present” in such a large fraction of this data set inappropriately overemphasizes and overweights the (apparently independent) gain of each one of these skeletal characters (thus, the 100% support for both brachiopod and articulate monophyly in the bootstrap results). Nevertheless, it is interesting that inarticulate monophyly is not the most parsimonious result (by length measures alone) in this experiment. This underscores the inherently weak morphological character support for inarticulate monophyly, particularly the ambiguity in the polarity of craniacean character states, and again suggests the need for additional outgroups and/or sources of phylogenetically informative character variation (e.g. molecular data). SUMMARY The results bear out the general dissatisfaction that brachiopod systematists have had with determining phylogenetic relationships among these taxa. Articulate monophyly is rarely questioned, brachiopod monophyly is occasionally contentious, while inarticulate relationships are in almost continual turmoil. Depending on the level of consensus one is willing to accept, all or perhaps none of these taxa

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145

are supported strongly enough to be considered monophyletic. Homoplasy is abundant and pervasive among brachiopods. Based on the excellent fossil record of these animals, it is clear that divergence among clades represented by extant species is very ancient (> 500 .Myr). Given the fossil evidence and the extensive character conflicts observed among Recent species, homoplasy is to be anticipated and evaluated, not ignored. Much of the previous disagreement among brachiopod systematists has resulted from exclusive focus on one or a few characters of questionable polarity to diagnose major groups. The purpose of this study is to make explicit all the characters that support the clades recognized here, and to provide more substantive evaluation of all the available data, rather than continuing to argue about only a small and possibly biased sample. Brachiopoda Brachiopod monophyly is supported in this study by 14 apomorphies (Table 2)) nine of which do not later reverse or reappear convergently at a higher level in the topology. The hypothesis of brachiopod monophyly has the strongest support in this analysis. It is necessarily in conflict with two hypotheses of brachiopod polyphyly that have been proposed previously. Wright (1979; see also Valentine, 1975) suggested that bivalved shells evolved seven times independently within the Brachiopoda from ancestors lacking mineralized skeletons (Fig. 1A). This apparently occurred sometime near the Precambrian-Cambrian boundary (at approximately 540 Myr) , when mineralized hard parts first appear abundantly in the fossil record. Because of the advantages mineralized skeletons confer in structural support, deterring predators, etc. (see Vermeij, 1989), Wright’s argument suggests that there were strong selection pressures to mineralize hard skeletons at this time. Thus, according to this scenario, mineralized skeletons evolved in parallel in many different groups of marine invertebrates more or less simultaneously, as soon as ancient ocean chemistry and paleophysiology permitted. Among the brachiopods, the multiple evolution of two valves (of either calcareous or phosphatic composition) produced only valves lacking in articulation. The articulate brachiopods were thought to be monophyletic (Wright, 1979), having evolved from the lingulacean brachiopods sometime in the Cambrian, after the multiple origin of the inarticulates (and thus the brachiopods). It is not possible to reject this particular argument of polyphyly outright, in part because the unmineralized fossil remains of these brachiopod ancestors are unlikely to be found. A paleontological test of the hypothesis is difficult to envision, given the difficulty of preserving soft anatomical structures. However, the results presented here suggest that monophyly is a significantly more parsimonious hypothesis that accounts for the existing data, particularly in the absence of tangible evidence to support brachiopod polyphyly. Although the possession of two valves is widely agreed to be a shared derived character of brachiopods, it is not the only character that supports their monophyly. Recall that characters of soft anatomy (24-57), not skeletal anatomy, provide the strongest support for monophyly in the analysis presented here (see Experiments, above). Even if mineralized shells did evolve several times independently among the organisms we call brachiopods (see Valentine and Erwin, 1987), a clade defined on the basis of soft anatomy alone encompasses all of these bivalved organisms.

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Comparison of brachiopod column refer to characters refer to (consistency index,

Table 4 apomorphies from among several listed in Appendix 2. For the results retention index, resealed consistency

recent studies. Numbers from this study, numbers index).

Character Hyman (1959) Bilaterally symmetrical bivalve shell Attached directly or by way of pedicle Valve dorsal and ventral and lined by mantle lobes Lophophore Open circulatory system Dorsal contractile vessel One or two pairs of mixonephridia Williams and Hurst (1977) Triple segmented coelomate Poorly developed protosome (undergoing atrophy) A pair of metanephridia Recurved gut, anus outside feeding apparatus (lophophore) Lophophore w/single row of filaments in ring around mouth Muscular pedicle as extension of ventral body wall Pedicle can secrete a cementing mucopolysaccharide Valves present and lacking articulation Valves secreted by epithelial folds (mantles) Valves initially organic, then chitinous, then phosphatic Rowell(l981,1982) Filaments in a single palisade about lophophore axiS

Double row of filaments on adult lophophore Brachial lip bounding food groove Two mesocoelic cavities in lophophore Mantle canals Forey (1982) Dorsal and ventral valves secreted by a mantle Carle and Ruppert (1983) Cuticle present as dorsal and ventral valves Mantles Pedicle Brusca and Brusca (1990) Trimeric (modified), coelomate lophophorates Dorsal and ventral valves Usually attached by pedicle Valves lined (and produced) by mantle lobes Epistome present, with or without coelomic lumen Lophophore circular or coiled, w/ or w/out internal skeletal support U-shaped gut, anus present or absent One or two pairs of metanephridia Circulatory systems reduced and open Most gonochoristic undergo indirect lie histories Solitary, benthic, marine Nielsen (1991) Longitudinal main axis U-shaped with short ventral side Pair of mantle folds present Attachment to substrate by a pedicle or direct cementation

in “Character” in parentheses

Comment3

24,63 30 24 33 47 48 45

OK Pedicle originated OK Primitive Primitive OK Primitive

20 21 45,46

Primitive Primitive Primitive

42,33

Primitive

36,37 30,31

OK Pedicle

63,72 24

Homology and polarity unclear OK, apomorphy of inardculates OK

61

Carbonate

36 37 36 39 24

OK OK OK OK OK

24,63

OK

63 24 30

OK OK Pedicle

20 24,63 30 24,63 21 33,35, 105 42 45 47 6,14 59,60

originated

originated

Primitive Primitive Primitive Primitive OK Primitive

Primitive OK

30,58

Polarity

twice

primitive

OK Pedicle originated OK Primitive

42 24

twice

unclear

twice

twice

BRACHIOPOD PHYLaOGENY Table

147

2-cur&d. Character

Nielsen (1991)-cur&. Presence of valves on mantle folds Presence of setae on mantle edges Presence of metacoel extensions in mantle folds (as mantle canals) Lophophore with extra coelomic canal on each side Adult lophophore with double row of alternating tentacles (Popov et al. 1993) Two coelomic cavities in lophophore Filaments in single palisade about lophophore axis (w/brachial lip) Hyaline cartilage-like connective tissue in lophophore [tentacles] Dorsal and ventral mantles w/coelomic cavities (filtration chamber) Mantle with marginal setae This study Sexes always separate (not always separate) Highly modiied trochophore larvae (trochophore) Short free-swimming larval stage (long) Two pairs of larval setae (none) Ventral and dorsal mantles, w/valves, mantle canals, present (absent) Lophophore tentacles on only one side of arm axis (both sides) Two rows of lophophore tentacles on each side of arms (one row) Two coelomic spaces per lophophore arm (one space) Anus ventral to mouth, gut curves down (dorsal, up) One pair of digestive diverticula (absent) Single contractile heart present (absent) Respiratory pigments as hemerythrin (no pigments) Primary nervous ganglion subenteric (supraenteric) Muscle fibers both smooth and striated (smooth only)

Comments

24,63 29

OK Absence

24 39

OK OK

36,37

OK

39

OK

36

OK

-,

33

Poorly

in craniaceans

known

is primitive

in outgroups

24 29

OK Absence

6 13 14 16

(LOO,-,-) (1.00, -, -) (0.33,0.33,0.11) (1.00,1.00, 1.00)

24

(1.00,1.00,1.00)

36

(0.50,0.75,0.38)

37

(0.67,0.75,0.50)

39 43 44 48 49 51

(1.00,1.00,1.00) (1.00,1.00,1.00) (1.00,1.00,1.00) (0.50,0.33,0.17) (0.67,0,0) (1.00,1.00,1.00)

56

(1.00,1.00,1.00)

in craniaceans

is primitive

Rather than supporting the multiple origins of the brachiopods, Gojansky and Popov (1985, 1986) and Popov (1992) support a diphyletic model of origination. They proposed that the phosphatic-shelled brachiopods (all of which lack articulation) share more recent common ancestry with the bryozoans and phoronids than with the calcareous-shelled brachiopods (some of which possess and some of which lack articulation (Fig. 1C). In this scenario, the bivalved condition evolved twice independently, with two different mineralogies, from non-brachiopod ancestors lacking mineralized skeletons. In addition to valve mineralogy, they argue that other synapomorphies define each “clade”. Phosphatic brachiopods (placed in a new Class Lingulata) are claimed to share with bryozoans and phoronids a “schizocoelic coelom and metasomal pouch, with settlement on the ventral body wall” Gojansky and Popov, 1986: 237). Calcareous brachiopods (placed in the newly defined Phylum Brachiopoda) share an “enterocoelic coelom, large mesocoel and reduced metacoel, absence of a metasomal pouch, and settlement on the posterior part of the body.”

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The fact that brachiopods can mineralize either carbonate or phosphate valves is not sufficient to argue that they are diphyletic. The putative apomorphies proposed by Corjansky and Popov (1986) are unknown or incorrectly characterized in several critical taxa. For example, coelom formation in bryozoans (Reed, 1991) and discinaceans (Chuang, 1977) is not known; settlement is ventral, not posterior, in craniaceans (Nielsen, 1991). The status of these features as homologues and as derived, not primitive, character states is not defended, and may be indefensible. In fact, none of these characters occurs in subsequent analyses of brachiopod relationships by the same investigators (Holmer, 1991; Popov et al., 1993). In order to reproduce the cladogram topology presented by Corjansky and Popov (1985, 1986) and Popov (1992), seven additional steps are required beyond the single MPC resulting from this study (Fig. 3). Several previous analyses have argued in support of brachiopod monophyly; they differ in various respects from the study presented here (Table 2). Williams and Rowell (1965: H195) discussed a range of characters that brachiopods possess and conclude that they “emphasize the basic homogeneity of the phylum”. Brachiopod monophyly is implied, but with little explicit justification. Rowe11 (1981a,b, 1982) completed a cladistic analysis of the extant superfamilies (minus thecideaceans) as a test of Wright’s (1979) polyphyly hypothesis (Fig. 1B). He concluded that five synapomorphies support brachiopod monophyly (Table 2); all five are confirmed by the analysis presented here. Nielsen (1991) lists eight synapomorphies; Holmer (1991) and Popov et al. (1993) list five. Some of these characters are confirmed as both shared and derived in this study; others appear to be either primitive or homoplastic, or only inferred to be present in the absence of direct evidence. IMrticllIata The monophyly of the Inarticulata, with the craniaceans as sister group to the discinaceans plus lingulaceans, is supported in the single MPC obtained (Fig. 3) and in 75% of the bootstrap analyses (Fig. 3). Ten synapomorphies define the clade, five of which do not reverse or reappear elsewhere (Table 3). Discinacean and lingulacean brachiopods are sister groups in 98% of the bootstrap analyses, with 21 shared derived characters, 11 of which do not reverse or reappear. In three of the 10 cladograms two steps longer than the shortest cladogram (Fig. 5B) and in 19% of the bootstrap analyses, craniaceans share most recent common ancestry with all other brachiopods, rendering the Inarticulata paraphyletic. In one of the five cladograms of length 225 (and in three of 10 one step longer), and in 19% of the bootstrap analyses, craniaceans share most recent common ancestry with the articulates [Fig. 5(C)]. It is clear that this morphological data set, as large and seemingly comprehensive as it is, does not strongly support any one hypothesis of relationship among the inarticulates. Craniaceans share many characters with the other inarticulates, and many with the articulates. Determining which of those characters are primitive and which are derived is critical to inferring phylogenetic relationships among the brachiopods. Craniaceans as the most primitive inarticulates has the most character support, but that support is still rather weak. The arguments against inarticulate polyphyly (Wright, 1979) and diphyly (Corjansky and Popov, 1985, 1986; Popov, 1992) are the same as discussed above for brachiopod polyphyly and diphyly. Uncertainty about phylogenetic relationships

BRACHIOPOD PHYLOGENY Table 3 of inarticulate

Comparison

apomorphies. Character

Hyman (1959) Valves held together Lophophore without Anus present

by muscles only internal skeletal

support

Williams and Rowe11 (1965) Valves either phosphatic or calcareous Valves rarely articulated, held together by muscles only Valves lacking hinge teeth and dental sockets Lophophore without mineralized support Muscles located peripherally in body cavity Pedicle develops from ventral mantle Schizocoelic coelom formation Shell, alimentary canal, lophophore develop in larvae Lophophore with median tentacle Mantle reversal occurs after larval settlement Alimentary canal with functional anus Single or double row of filaments on juvenile lophophore Rowe11 (1981,1982) Hydraulic mechanism for opening Presence of larval shell

valves

This study Castrulation by imagination without epiboly (with epiboly) Three pairs of larval setae(two pairs) Mantle epithelium divided completely (continuous) Median tentacle of lophophore present initially, then lost (absent) More than two coelomic spaces per lophophore arm (two) Brachial muscles in adult lophophore strongly developed (weak) Anus to the right of mouth; gut curves to the right (ventral, down) Dorsal valve beak distinct and/or pointed (indistinct and rounded) Muscle scars in ventral valve medium size (small) Dorsal valve mantle canal markings isolated (apocopate)

149

Comments

72 105 42

Derived primitive Primitive

within

inarticulates

61

Calcareous

72 74 105 54 31 19 14 38 5 42

Derived within inarticulates No outgroup power, equally Primitive Polarity unclear Derived withii inarticulates Derived within inarticulates Derived within inarticulates OK No outgroup power, equally Primitive

37

Single

62

Questionable (muscles also) Inaccurate (absent in Cm&u) 1991)

2 16

(1.00, -, -) (1.00,1.00,1.00)

25

(1.00,1.00,1.00)

38

(1.00,1.00,1.00)

39

(1.00,1.00,1.00)

40

(0.33,0.50,0.17)

43

(1.00,1.00,1.00)

100 108

(0.33,0,0) (0.67,0.50,0.33)

112

(0.50,0,0)

is primitive

derived

derived

is primitive

(Nielsen,

among the inarticulates has in the past generated the uncertainty about the status of brachiopods as a clade. As argued above, inarticulate polyphyly is neither a parsimonious or biologically compelling interpretation of the data in this analysis. Inarticulate paraphyly, however, is a more complex and more interesting possibility. Paraphyly among inarticulates is manifest as one of two topologies (Fig. 5B, C). The possibility that craniaceans are the most primitive of all brachiopods is fairly well supported by the data. Yet, other than a brief mention by Hohner (1989)) it has not been discussed extensively in the literature. In addition to its marginally greater length, this hypothesis of relationships is considered to

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be less plausible because it requires more character reversals overall, carbonate skeletons originating twice independently, and muscles that control movement of the lophophore originating three times independently. Perhaps most convincingly, nonplanktotrophic larvae (with a short, free-swimming larval stage) are primitive in this topology and planktotrophic larvae (long free-swimming stage) are derived from them twice. Not only is this widely thought to be the reverse polarity for this character (Appendix 2)) but its independent origin twice is not considered likely. Of the two hypotheses in which inarticulates are paraphyletic, it is curious that the one receiving the least support in this analysis [craniaceans as sister group to the articulates; Fig. 5C) has received the most attention in the literature (on the basis of far fewer data). Perhaps because the calcareous shell is such an obvious feature shared by both taxa, it is tempting to assume that the feature must be derived rather than primitive. Hennig (1966: 148-154) constructed a phylogenetic diagram of extant brachiopod taxa using characters drawn exclusively from an anatomical study by Helmcke (1939)) where each character was assumed to be shared and derived. In his diagram, craniids share more recent common ancestry with the articulates than with the lingulids. The analysis was necessarily limited by the quality of Helmcke’s data, some of which are now known to be inaccurate. Hennig’s exercise was not intended to serve as a phylogenetic analysis of the brachiopods; its purpose was to demonstrate clearly the difference between illustrating morphological similarities and differences using a reticulate diagram (like Helmcke) or a branching diagram that could reflect patterns of common ancestry. In a similar spirit, Forey (1982) presented a simple analysis of phylogenetic relationships among the major groups of fossil and Recent brachiopods in order to illustrate features of cladistic methodology. He analyzed 10 or so morphological characters, and concluded that inarticulates are paraphyletic. Considering only the extant taxa in his cladogram, Crania shares more recent common ancestry with the articulates than with most of the other inarticulates. Yet, an extinct group of phosphatic inarticulates (Paterinida) is nested within the otherwise calcareous clade that includes Crania and the articulates. This led Forey to comment that -a division of brachiopods into non-calcareous and calcareous may be over simplistic” (1982: 13’7). In his study, fossil taxa played an important role in interpretations of character evolution within the brachiopods, particularly of shell mineralogy, even if they did not alter the relationships among extant brachiopods only. Arguments of homology and polarity of shell mineralogy are fundamental to the hypothesis that craniaceans are more closely related to the articulates than the other inarticulates, just as the homology and polarity of the presence of mineralized valves has been characterized as fundamental to the hypothesis that brachiopods are polyphyletic (e.g. Wright, 19’79). In the analysis presented here, there is no reason to question the status of either calcareous valves or phosphatic valves as homologues. Polarity of shell mineralogy is more difficult to resolve. Using outgroup criteria to determine polarity, as in this study, calcareous valves are clearly primitive and phosphatic valves derived. Considering the distribution of these two mineralogies among all metazoans (e.g. see Eemisse et al., 1992), not just the four outgroups used here, it is clear that phosphatic mineralization has evolved several times independently (e.g. in chordates, brachiopods, molluscs, annelids). Corjansky and Popov (1985, 1986) and Popov (1992), however, argue strongly in support of the

BRACHIOPOD

PHYLOGENY

151

homology of calcareous valves and their status as a derived character within the brachiopods. Yet, the single outgroup used (phoronids) lacks a mineralized skeleton, and is therefore unable, by itself, to polarize the direction of transformation in this character. Only reference to a larger number of outgroups can resolve polarity unambiguously in this instance (and for numerous other characters as well). Stratigraphic polarity cannot unambiguously distinguish primitive from derived shell mineralogies. Both calcareous and phosphatic mineralization appear very early in the fossil record (Brasier, 1979; Runnegar, 1989; Lowenstam and Weiner, 1989). Arguments have been made to suggest that, although phosphatic brachiopods occur only slightly earlier than calcareous brachiopods in the stratigraphic record, the difference is evolutionarily significant (Williams and Rowell, 1965; Popov, 1992). Fossil exploration over the past decade has led to the discovery of calcareous brachiopods well down in the Lower Cambrian (e.g. Ushatinskaya, 1986; Andreeva, 1987; Popov and Tikhonov, 1990), further narrowing the narrow gap in stratigraphic first appearances between the phosphatic and calcareous inarticulates, suggesting that the gap is not likely to be as significant as previously thought. Biogeochemical criteria suggest that it may have been easier for organisms to mineralize phosphate in Early Cambrian seas than it is today because concentrations of phosphate in seawater were higher then, supported by evidence of worldwide phosphatization at this time (Lowenstam and Margulis, 1980; Cook and Shergold, 1984; Lowenstam and Weiner, 1989). Surface waters of the ocean today are supersaturated with respect to calcium carbonate, but are commonly depleted in phosphorus (Holland, 1978). Phosphate mineralization by organisms in the modem oceans, particularly in shallow-water environments, is not “easy” to accomplish biogeochemically. It requires active induction of ions, otherwise low in concentration, to the site of mineralization, creating an unusual chemical microenvironment for mineralization. If, in the Cambrian, organisms began to mineralize whatever was biogeochemically easy, it is possible that phosphate and carbonate mineralization had at least more similar probabilities of occurring than they do today. However, our understanding of the many and varied organismal controls on mineralization is relatively poor (Bengtson and Conway Morris, 1992). Because organisms today can exert considerable control over their environment of mineralization, it is possible that further study of in uivo mineralization could lead to the rejection of, this simplistic chemical-environment argument in the Cambrian. Ocean chemistry may not have such a strong and direct control over mineralization. Even if it could be demonstrated that more brachiopods mineralized phosphate than carbonate in the Cambrian, polarity determination degenerates to a weak, common-is-primitive argument. Nielsen (1991) studied the embryology of Crania (calcareous inarticulate) and documented several embryological differences between it and the phosphatic inarticulates. Together with the difference in shell mineralogy, these embryological differences led him to conclude that “it is difficult to regard them [inarticulates] as a monophyletic group being a sister group to the articulates” (1991: 24). Although he did not provide a stronger argument for inarticulate pamphyly, he clearly emphasized differences between calcareous and phosphatic brachiopods in characters other than mineralogy alone. The phosphatic brachiopods do share many (21) derived characters of embryology and soft and hard anatomy. However,

152

S.J. CARUON

demonstrating a close relationship between the lingulaceans and discinaceans does not necessarily imply that there is a similarly close relationship between the craniaceans and articulates. Even though Crania may share many characters with the articulates, the polarity of the characters is more important in phylogeny reconstruction than is their overall similarity. According to the results of the analysis presented here, many of these shared characters are primitive, not derived (Table 4). Nielsen did not discuss characters of the inarticulates that appear to be both shared and derived (Table 3). Holmer (1991) and Popov et al. (1993) have argued that lack of articulation is a primitive character that cannot be used to diagnose the Class Inarticulata as a monophyletic group. A single character thought to be primitive is certainly not a valid basis for designating a clade. However, Inarticulata is something of a misnomer. It is true that all three taxa in Inarticulata lack a tooth-and-socket hinge mechanism. Yet, the polarity of this character state, by outgroup comparison, is ambiguous. Because no outgroups among metazoans possess two valves homoogous with those of brachiopods, outgroups are unable to polarize this character. In other words, lack of articulation is no more primitive than is the presence of articulation, if by articulation one means the tooth-and-socket mechanism. Stratigraphic criteria do not provide compelling support for the polarity of this character either (as in discussion above on valve mineralogy). It is unfortunate that the names of the classes reflect, in this instance, the sharing of a character whose polarity is ambiguous. Nevertheless, there are several other characters shared by these three inarticulate taxa that do appear to be derived (Table 3). If articulation is taken instead to mean the presence of points of contact between the valves that serve as a hinge axis in valve rotation, rather than the presence of teeth and sockets, then articulation is primitive for brachiopods. Craniaceans use the straight posterior edge of their valves as a fulcrum in valve opening (Atkins and Rudwick, 1962; Forey, 1982). In fact, there are a number of “inarticulate” brachiopods that appear early in the fossil record (some pate&ids, kutorginids, obolellids and acrotretids), whose valves were almost certainly in contact and forming a hinge during rotation, but do not possess teeth and sockets (Williams and Rowell, 1965; Rowell, pers. comm., 1988). The perspective provided by the fossil record underscores the importance of distinguishing these two different aspects of valve articulation. Only the discinaceans and lingulaceans lack any kind of consistent valve-to-valve contact during opening and closing (and are “true” inarticulates). Popov et al. (1993) performed a cladistic analysis of extant brachiopod superfamilies using 29 morphological characters and a “hypothetical protophoronid ancestor” as an outgroup. They obtained a single MPC (Fig. 1D) with a consistency index of 1.00, in which the inarticulates are paraphyletic. Craniacea are the sister group to the articulates, and the “synapomorphies” of this clade, which they name as a new Class Calciata, appear to be either primitive or homoplastic, according to the analysis presented here (Table 4, Carlson, 1994). As discussed before (see Experiments), experimenting with character irreversibility, the exclusion of various types of characters or taxa and the choice of outgroups can generate this result, suggesting how certain types of bias in the structure of the data matrix or the phylogenetic analysis of the data may lead to this conclusion. Other systematists have argued in favor of the monophyly of the inarticulates,

BRACHIOPOD

PHYLOGENY

153

Table 4 Comparison

of (craniacean

+ articulate)

‘apomorphies”.

Character Hennig (1966) Shell consisting of calcium carbonate Anterior part of body parenchymatous (= ?lacking protocoel) Marginal lacunae not developed Forey (1982) Posterior margin of pedicle (ventral)

valve

straight

Corjansky and Popov (1985,1986) Enterocoelic coelom Large mesocoel and reduced metacoel Absense of a (ventral) metasomal pouch Settlement on posterior part of body Nielsen (1991) Shell composition (calcareous) Larvae lecithotrophic (= nonplanktotrophic) Bilaterally symmetrical gut Larval characteristics in general, aspects of settling and metamorphosis Popov et al. (1993) Double row of filaments in the post-trocholophe stage Striated muscle fiber present in the lophophore Gonads in mantle canals One pair of oblique muscles present Calcareous shell present This study Gametes developed from folds of coelomic epithelium in mantle canals Duration of free-swimming larval stage short Origin of coelomic spaces by highly modified enterocoely Two pairs of coelomic cavities in early larval stages Muscular valve atjunction of body cavity and mantle canals absent Marginal canal in connective tissue around mantle margin absent Pedicle originates from larval rudiment Pedicle not coelomate and not muscular Shell formation begins following settlement Shell structure punctate, lacking distal brushes Chitin absent Valves in contact and rotate about a hinge axis located on valves Valve biconvexity strong Ventral valve more convex than dorsal Relative shape, size and growth pattern of two valves quite diierent Ifvalves not biconvex, dorsal is conical, ventral is planar Ventral valve beak rounded Ventral valve beak extends well beyond dorsal valve beak Ventral valve cardinal area wide Well-defined chamber in ventral valve for _. pedicle base present Median septum in dorsal valve present, but weak Pinnate mantle canal markings

Comments

61

Primitive

21 127.24

Primitive Poorly known

72

Primitive

19 -

Primitive Relative coelom size unclear Homology and polarity unclear Inaccurate [ventral] (Nielsen, 1991)

61 14 43

Primitive Primitive Primitive

37 56 9 61

Primitive Polarity unclear Originated twice in each taxon No oblique muscles in articulates Primitive

9 14

Originated Primitive

19 23

Primitive Originated

26

Poorly

27 31 32 62 ;:

Poorly known in articulates Pedicle absent in craniaceans Pedicle absent in craniaceans Primitive Autapomorphy of craniaceans Lost in craniaceans and thecideaceans

2 78

No outgroup Craniaceans Apomorphy

79

Primitive

80 86

Autapomorphy of craniaceans Ventral valve beak absent in craniaceans

87 89

Ventral valve beak absent in craniaceans V.V. cardinal area absent in craniaceans

96 103 111

in articulates

twice in each for brachiopods

twice

known

Pedicle absent Autapomorphy Autapomorphy

in each

taxon

taxon

in articulates

power, ?primitive not biconvex of articulates only

in cmniaceans of craniaceans of craniaceans

154

S.J. CAFtLSON

but the arguments have been mostly weak and unconvincing. Williams and Rowe11 (1965) list a series of characters that define the Class Inarticulata (Table 3), some of which are derived and some primitive at different levels. Rowell (1981a,b, 1982) identified two characters as inarticulate synapomorphies, but both are problematic (Table 3). In this study, even though inarticulate monophyly is not very strongly supported, it is more strongly supported than is any other alternative. These character conflicts reflect the long and complex evolutionary history of the group, resulting in substantial homoplasy and intriguing patterns of character evolution. Articulata Articulate monophyly is strongly supported in this analysis by 35 synapomorphies, 26 of which do not reverse or reappear elsewhere (Table 5), consistent with all previous studies (Williams and Rowell, 1965; Hennig, 1966, Williams and Hurst, 1977; Rowell, 1981a,b, 1982; Forey, 1982; Corjansky and Popov, 1985, 1986; Hohner, 1991; Nielsen, 1991; Popov et al., 1993). Ninetyeight of the bootstrap analyses support the monophyly of the articulates. However, articulate nonmonophyly can be generated in a cladogram just four steps longer than the shortest MPC, in which thecideaceans are the sister group to all other brachiopods. Relationships among the extant articulates (Fig. 3) are also strongly supported by the data, but are seemingly at odds with the traditional paleontological explanation of these data. The position of the thecideaceans as the most primitive member of the extant articulates is most parsimoniously explained in this analysis as the retention of many primitive features from the ancestral state. However, by the criterion of stratigraphic polarity alone, the rhynchonellaceans are thought to be the most primitive extant member of the articulates (Williams and Rowell, 1965), first appearing in the fossil record long before (more than 200 Myr) the other three superfamilies. Thus, using only stratigraphic polarity, thecideaceans would most likely occur as the sister group to the terebratulides. In the paleontological argument, “primitive” features that thecideaceans exhibit cannot be primitively retained because the group first appears so late in the fossil record. Instead, they are considered to be secondarily derived through the process of paedomorphosis (Williams and Hurst, 1977; Fouke and IaBarbera, 1986; Baker, 1970,199O). Thecideaceans are anomalous in comparison with other extant articulate brachiopods (Elliott, 1953; Williams, 1956, 1973; Pajaud, 1970). They are extremely small as adults (up to a few millimeters at most), live in tropical, not temperate or polar environments, and are cemented to the substrate, lacking a pedicle. Considerable debate has centered on the phylogenetic affinities of this poorly understood group (see Rudwick, 1970; Williams and Rowell, 1965; Baker, 1990; Carlson, 1991a,b). Paleontologists in the past have proposed common ancestry with the strophomenides, an extinct order of articulates (Schuchert, 1893; Elliott, 1953; Rudwick, 1968; Baker, 1970), and with the terebratulides (Williams, 1968). Thecideaceans are currently hypothesized to share most recent common ancestry with the “spiriferides” (Baker, 1984,1990), an extinct, nonmonophyletic group of articulates whose phylogenetic relationships are uncertain at best. Until a more detailed study of the phylogenetic relationships among all the “spiriferide” and thecideacean brachiopods is completed, it is difficult to evaluate

BRACHIOPOD

Comparison

PHYLOGENY Table 5 of articulate

155

apomorphies. character

RoweU (1981,1982) Diductor muscles and hinge Mantles fused posteriorly Secondary shell fibrous Pedicle develops from larval Mantle reversal at settlement Larval shell absent

mechanism

present

rudiment

This studv Mantle rudiment reverses at settlement (does not reverse) Sperm morphology ect-aquasperm (ent-aquaspenn) Most brood, few free-spawn to disperse gametes (all f?ee+pawn) Single band ciliary mechanism in adults only (larvae and adults) T&sue-filled epistome, lacking protocoel (with protocoel) Two pairs of coelomic cavities in early larval stage (one pair) Mantle groove in terminal branches of mantle canals (absent) Pedicle in juvenile and adult only (absent entirely) Pedicle from larval rudiment (as ventral mantle invagination) Pedicle not coelomate, not muscular (coelomate, muscular) U-shaped alimentary canal ends blindly (terminates in anus) Two pairs of digestive diverticula with two ducts (one pair) Small supraenteric secondary ganglion present (absent) “Simple” muscle system: adductor, diductor, adjustor (“complex”) Muscles originating from lophophore absent (present) Dorsal valve growth always hemiperipheral (ahvays holoperipheml) Tertiary prismatic layer often present in shell (laminar layer) Large punctae with brushes present (extremely fine punctae) Mesenchymal calcite spicules in tissues common (absent) Shell resorption common (uncommon) Teeth and sockets present and interlocking (absent entirely) Valve biconvexity strong (weak) Ventral valve more convex than dorsal valve (equal convexity) Ifvalves not biconvex, ‘tubular”with lid (biconical) Shell shape (in dorsal vie-w) oval, (circular) Ventral valve beak rounded (flat) Ventral valve beak extends well beyond dorsal (just beyond) Ventral valve cardinal area as pseudointerarea (absent) Wide ventral valve cardinal area (very narrow to absent) Ventral valve beak ridge8 welldefined(absent) WeUdefined chamber for pedicle base present (absent) Dorsal valve umbo marginal (catacline) (central [procline]) Welldeveloped median septum in donal valve (absent) Calcareous lophophore supports from cardinalia (valve ridges) Saccate mantle canal markings(biicate)

Comments

54,74 25 66 31 5 62

OK Primitive Primitive OK OK Primitive

5 8 12 18 21 23 28 30 31 32 42 44 52 54 55 65 67 68 69

(1.00,1.00,1.09) (0.50.0.67.0.33~ io.50;0.50;0.25j (0.67,0.75,0.50) (1.00,1.90.1.00) (1.00, -* -1 (1.00,1.09,1.09) (1.90,1.90,1.09) (1.00,1.00,1.00) (1.00,1.00,1.00) (1.00,1.09,1.00) ~1.90.1.00.1.00)

z 77 78 80 82 86 87 88 89 92 96 LO2 103 105 111

(weak)

ii.00;1.00;i.ooj

(1.09.1.00,1.00) (0.95.0,0) (0.W 0, 0) (1.00, -, -1 (1.00.1.09,1.00) (0.50,0.50,0.25) (0.50,0.50,0.25) (1.00,1.09,1.90) (1.00. -* -1 (0.67,0.50,0.33) il.oo,-,-) IO.75.0.0) i1.09; i,-, (1.W -, -1 (1.W -9 -1 (1.90.1.00.1.00) (1.90,1.00,1.clo) (1.00.1.09,1.00) (1.00,1.00,1.00) wo, -5 -1 (1.00,1.00.1.00) (1.00.1.09,1.00)

the relative strengths of the parsimony-based explanation of these results, or the slightly less parsimonious but highly plausible paleontological explanation. Both explanations could be reconciled if the details of “spiriferide” paraphyly/polyphyly were better documented. For example, the “spitierides” may well consist of several clades of brachiopods, some of which emerge from the “stem” between the brachiopod node, the articulate node and the terebratulide node. It is possible that one group of “spiriferides” shares most recent common ancestry with the (rhynchonellide t terebratulide) &de, and that thecideaceans evolved much later, possibly paedomorphically, from one clade in that particular spiriferide” group,

156

S.J. C&RLSON

now extinct. This hypothesis is consistent with the topology in Figure 3 and the stratigraphic record; “spiriferides” and rhynchonellides both first appear in the Ordovician. The absence of extant taxa to fill in the apparent phylogenetic “gap” between the thecideaceans and the rhynchonellides strongly suggests that an analysis including fossil and extant brachiopods would provide useful information on relationships among extant articulates. It is worth noting that paedomorphosis, as a possible explanation of the results of this rmaIysis, may not have been considered without knowledge of the fossil record. In other words, neontologists may suspect that the extremely small size of adult thecideaceans indicates a paedomorphic origin for the group, but it is their extremely late first appearance in the fossil record relative to their primitive location in the (outgroup) cladogram that provides additional, necessary support for this hypothesis. Lophophorates The lophophore is a feeding/respiratory structure consisting of ciliated tentacles that surround the mouth, exclude the anus, and contain extensions of mesocoel. The possession of a lophophore is widely considered to have arisen once among the metazoans, uniting the three lophophore-bearing taxa. Lophophorate mono phyly is often assumed (Willmer, 1990; Brusca and Brusca, 1990) and only rarely tested (Schram, 1991; Meglitsch and Schram, 1991; Eemisse et al., 1992). Many other metazoans possess structures similar in various respects to a “true” lophophore. Sipunculids have a ciliated tentacular structure that surrounds the mouth and excludes the anus, but the fluid-filled spaces within the tentacles are likely not to be homologous with the mesocoel (Brusca and Brusca, 1990). Pterobranchs have “lophophores” that exclude both the mouth and anus, but are otherwise very similar to those found in the lophophorates (Jefferies, 1986; K Halanych, pers. comm. 1993). Emig (1977, 1984) is one of the strongest proponents of lophophorate monophyly, although his evidence consists of several characters of uncertain polarity that also occur in other metazoans (Table 6). Carle and Ruppert (1983)) in a thoughtful discussion of the homology of blood vessels among the lophophorebearing taxa, suggest the monophyly of the lophophorates (Table 6), but present no clear criterion for polarity determination (other than ingroup comparison). As with Emig’s arguments, many characters are also present in other metazoans. Clearly, determining the polarity of these structures will be important in further evaluations of lophophorate monophyly. Because useful morphological data are difhcult to identify at such high taxonomic levels, molecular data are likely to play an increasingly significant role. Investigating phylogenetic relationships among the lophophorates is not the focus of this analysis, and the results discussed here are very preliminary, but they do provide a working hypothesis for future testing. Using both sipunculids and pterobranchs as outgroups, lophophorate monophyly receives relatively weak support (Table 6), with eight apomorphies, three of which do not reverse or reappear elsewhere. The three characters concern the lophophore. Nielsen and Norrevang (1985) and Nielsen (1985,1987,1991) have argued that the lophophorates are diphyletic, largely, but not exclusively, on the basis of

157

BRACHIOPOD PHYLOGENY Table 6 of lophophorate

Comparison

apomorphies. Character

Carle and Ruppert (1983) Trimery (disputed for brachiopods) Blood vessels as spaces in extracellular peritoneum Peritoneal cells myoepithelial Lophophore U-shaped gut Monociliated epidermal cells Blood vascular system Body wall musculature Mixonephridia Intraepidermal nervous system Radial cleavage, regulative development Cuticle present

Willmer (1990) Lophophore Chitinous exoskeleton Tripartite coelomate U-shaped gut Modified enterocoelic Radial cleavage Modified trochophore

reproductive

Also in pterobranchs

47 33 42 17 47 45 50 3 53

Also in Polarity OK Primitive Also in Also in ?Primitive Also in Also in Aho in Also in

20 46 42 33 37 55 21 53

Also in Also in Primitive OK Primitive Also in AIso in Also in

20 42

Also in pterobranchs Primitive

9 45 53 33

OK (probably) Also in sipunculids Also in pterobranchs OK

33 53,71 20 42 19 3 13

OK Probably primitive Also in pterobranchs Primitive OK Also in pterobranchs OK (probably)

42,43 33 17

Primitive OK (perhaps primitive) OK Also in pterobranchs

8 9 14

(0.50,0.67,0.33) (0.67,0.75,0.50) (0.33,0.33,0.11)

18

(0.67,0.75,0.50)

19 33 34

(0.67,0,0) (LOO,-,-) (1.00,1.00,1.99)

35

(1.00,1.00,1.00)

pterobranchs unclear

pterobranchs pterobranchs sipuncullds pterobranchs(7) pterobranchs pterobrapchs pterobranchs sipunculids

sipunculids pterobranchs pterobranchs

systems

body coelom

20 matrix

Emig (1984) Trimerous body plan Pair of metanephridia U-shaped gut Lophophore present Lophophore with single row of tentacles Lophophore retractable Poorly-developed protosome (epistome) Cuticle present Brusca and Brusca (1990) Tripartite body plan U-shaped gut Simple, often transient (peritoneal gonads) Metanephridia Secrete outer casings Lophophore

Comments

formation

larvae

Meglitsch and Schram (1991) Bilateral symmetry Gut coiled or looped, anus anterior Lophophore Upstream particle capture in adults This study Sperm morphology ent-aquasperm (ectaquasperm) Gametes develop in body cavity (body tissues) Long free-swimming larval stage (short) Single ciliary band mechanism in larvae and adults (absent) Coelomic spaces originate by highly modified enterocoely (schiaocoely) “True” lophophore (without mesocoel) Two arms in lophophore (more than two) Spirolophe lophophore geometry(straight, frond-like arms)

158

S.J; CARBON

embryological and larval evidence. According to the trochaea theory (Fig. 2C), brachiopods and phoronids share derived characters with some deuterostomes (e.g. echinoderms, hemichordates), while bryozoans share many derived characters with the protostomes (e.g. molluscs, annelids, arthropods). Bryozoans are difTicult to study phylogenetically because they are miniaturized and colonial, and both conditions are almost certainly highly derived relative to their ancestral state. Homologues are difficult to identify, and primitive absence is difficult to distinguish from derived loss. The trochaea theory has not been widely accepted among animal systematists, in part because of its nearly exclusive dependence on a small number of characters representative of a limited portion of whole-organism morphology and life cycle. Despite criticisms of this theory, Nielsen’s perspective on metazoan phylogeny is valuable because of his reluctance to accept uncritically the presence of the lophophore as the main (only?) character uniting the lophophorates. Several recent studies have suggested that the lophophorates may be a primitive paraphyletic group, ancestral to the deuterostomes (Fig. 2B; Schram, 1991; Meglitsch and Schram, 1991; Eemisse et al., 1992). According to this hypothesis, the lophophore evolved at the base of this clade and was then lost in the derived deuterostomes. A calcareous skeleton also evolved at the base of the clade, and was lost three times in the phoronids, the pterobranchs, and the more derived deuterostomes. The strength of this hypotheis depends on the relative ease with which evolutionary loss of characters can be evaluated (discussed by Ghiselin, 1988, 1989, 1991). Secondary loss is generally thought to be easier to accomplish than the independent origin of characters, thus calcareous skeletons are considered to be primitive for this clade rather than having evolved three times independently. However, echinoderm (and vertebrate) skeletons are mesodermal in origin, while brachiopod and bryozoan skeletons are ectodermal; it is quite possible that these two types of mineralization have evolved independently. Similar complexities in interpreting character evolution arise when evaluating character reversals. Are reversals extremely rare in evolution? Less rare than is widely thought? Rare only for certain kinds of characters, but more common for others? In order to answer these questions thoughtfully, more comparative information is needed on the origin and development of ‘a range of morphological features of the lophophorebearingtxa. The issue of lophophorate monophyly necessarily concerns the relationship of the brachiopods, bryozoans and phoronids to other metazoans. All the hypotheses discussed thus far utilize morphological or embryological data, and all resolve brachiopods (and phoronids) as more closely related to the deuterostomes than the protostomes (Fig. 2). Recent molecular evidence, however, suggests that brachiopods share more recent common ancestry with the protostomes (Fig. 2D; Field et al., 1988; R Halanych, pet-s. comm. 1993). The morphological and molecular data indicate two mutually exclusive hypotheses of relationship. Only one can be correct. An early criticism of the Field et al. (1988) study concerned the phylogenetic analysis of the data. Patterson (1989) and Lake (1990) each reanalyzed the data obtained by Field and coworkers and obtained difIerent cladogram topologies than had Field et al. These reanalyses discovered metazoan monophyly once again, but the brachiopods still clustered with the molluscs and sipunculids, suggesting that

BRAGHIOPOD

PHYLOGENY

159

data analysis alone is not responsible for the seemingly anomalous location of the brachiopods. It is possible that the molecular data have a relatively low signal to noise ratio (sen.ru Hillis, 1991). If the sequence obtained from LingaZu is relatively short, it may be difficult to unambiguously align it with other, longer sequences. Having not seen the data, it is difficult to evaluate this possibility further. 18s rRNA was analyed from only one species of brachiopod, Lingula reeui, and brachiopod monophyly was assumed. The results of this morphological study support brachio pod monophyly, but comparing sequences from several brachiopod species, ideally from several different genes, would provide a worthwhile test of brachiopod monophyly. In fact, based on the results from this study, Crania unum& would have been a better choice than Lingula & as a single primitive species to represent the phylum in a molecular systematic analysis. Lingula is relatively derived within the brachiopods, despite the fact that the fossil record of the genus extends back to the Ordovician period. One other difficulty with the molecular systematic analysis is that little morphological evidence supports it. Hemerythrin, a respiratory protein, is present in brachiopods and sipunculids (and priapulids, Joshi and Sullivan, 1973). The ultrastructure of setae in brachiopods is nearly identical to the chaetae in polychaete annelids (see Orrhage, 1973). Although these similarities have been referred to as shared, derived features (Ghiselm, 1988), a number of robust characters have distributions in conflict with them (see below; Table 6; Appendix 2). The conventional interpretation that hemerythrin and chaetae have evolved independently in these taxa is strongly supported in this analysis. Future analyses with additional outg~oups will provide further tests of this conclusion. Despite potential problems with the results of the molecular systematic analysis just discussed, it is very possible that the molecular results indicate the true pattern of relationships. If so, the question of metazoan phylogeny becomes especially intriguing from a comparative morphologist’s perspective. Many embryological characters in particular, thought to be fundamentally conservative in their evolution, may be far more “plastic” evolutionarily than previously recognized. Brachiopods, of all the lophophorates, possess a large number of very deutero stomelike characters, including the mode of mesoderm formation, type of gasmrlation and type of cleavage, in addition to monociliate cells, a tripartite body plan, open blood vascular system, and an intraepidermal nervous system. If the molecular results are correct, then brachiopods have evolved all these features independent of the deuterostomes. If so, morphologists and embryo logists will have to reevaluate long-entrenched notions about character evolution among the metazoans. Future Work Many opportunities for future research to test the results of this analysis present themselves. Additional protostome (e.g. molluscs or annelids) and deuterostome (e.g. echinoderms) taxa could be used as outgroups in other morphological analyses. Extinct taxa could be added to determine their effect on the phylogeny of the extant taxa only. Stratocladistic methods (Fisher 1980, 1991, 1992) could be used to incorporate information not only on character combinations that occur in extinct brachiopods, but also on the known stratigraphic ranges of taxa. Homeobox

160

S.J. CARLSON

genes could be investigated in brachiopods (see Raff and Kaufman, 1983; Holland and Hogan, 1986)-are they more similar to molluscs and annelids or to echino derms and chordates? Perhaps the most obvious area of investigation is in the field of molecular systematics. The analysis of longer sequences from a greater number of genes in a broad sample of species of lophophorates and other metazoans is needed to test the morphological cladogram presented here for the brachiopods and to test the perplexing (to a morphologist) results of the Field et al. (1988) study. Particularly when divergence times among taxa are very ancient, as is true for extant brachiopods, it is reasonable to ask whether morphology alone, or molecules alone, can reconstruct phylogenetic relationships with much confidence. Using all available data is likely to be the most informative approach to reach a more complete understanding of brachiopod, and lophophorate, phylogeny.

Summary and Conclusions 1. Brachiopods are monophyletic. Characters of soft anatomy provide the strongest and most definitive support for this conclusion, rendering the argument over the multiple origins of a bivalved shell irrelevant to determining brachiopod monophyly. A large body of comparative information on brachiopod morphology and embryology has been assembled and evaluated phylogenetically. These analyses have generated explicit, testable hypotheses of character evolution within the brachiopods. 2. Articulate brachiopods are monophyletic. The many characters supporting articulate monophyly are listed and discussed explicitly. Thecideaceans are the most primitive group of articulates, despite their late first appearance in the fossil record. Future analyses will test the hypothesis that they represent a paedomorphic crown group remaining after the pseudoextinction of the “spiriferide” brachiopods, a paraphyletic group with which they share common ancestry. 3. Inarticulates appear to be monophyletic, but the results are not convincingly robust and require testing from additional sources of comparative information. The polarity of articulation between the valves, in the form of teeth and sockets, cannot be determined because outgroups have no power to polarize this character. The presence and absence of teeth and sockets are equally derived. However, articulation in the form of valve-to-valve contact about a hinge axis is primitive in this analysis. By outgroup comparison, carbonate mineralogy is primitive, not derived. Stratigraphic polarity alone does not provide compelling support for the hypothesis that phosphatic shell mineralogy is primitive for brachiopods. The hypothesis that the calcareous inarticulates and the calcareous articulates are sister taxa receives very little support in this study, but this result can be generated by (ad hoc) experimental manipulation of the data. The characters shared by these two groups appear to be either primitive (not derived) or homoplastic (not homologous). 4. Lophophorate monophyly is suggested here, but is supported only by very tentative morphological evidence. Additional studies of molecular systematics are needed to test these results.

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ROWELL, A. J. 1960. Some early stages in the development of the brachiopod Crania anomula (Miiller). Ann. Mag. Nat. Hist. 13: 35-52. ROWELL, A J. 1981a. The Cambrian radiation: monophyletic or polyphyletic origins? In: M. E. Taylor (ed.). Short papers for the Second International Symposium on the Cambrian System. U.S. Geol. Surv. Open File Report 81-743: 184-187. ROWELL, A. J. 1981b. The origin of the brachiopods. In: T. W. Broadhead (ed.). Lophophorates, Notes for a Short Course. Univ. Tennessee, Enoxville, pp. 97-109. ROWELL, A. J. 1982. The monophyletic origin of the Brachiopoda. Lethaia 15: 299-30’7. ROWLEY A. F. AND P. J. HAYWARD. 1985. Blood cells and coelomocytes of the inarticulate brachiopod Lingulu anutina. J. Zool., Lond. (A) 205: 9-18. RVDW~CK, M. J. S. 1968. The feeding mechanisms and affinities of the Triassic brachiopods ThecospiraZugmayer and Bactyium Emmrich. Palaeontology 11: 329-360. RUDWEK, M. J. S. 1970. Living and Fossil Brachiopods. Hutchinson and Co., London. RUNNEGAR, B. 1989. The evolution of mineral skeletons. In: R E. Crick (ed.). Origin, Evolution, and Modem Aspects of Biomineralization in Plants and Animals. Plenum, New York, pp. 75-94. RUNNEGAR, B. 1992. Evolution of the earliest animals. In: J. W. Schopf (ed.). Major Events in the History of Lie. Jones and Bartlett, Boston, pp. 65-93. RUPPERT, E. E. AND K J. &RLE. 1983. Morphology of metazoan circulatory systems. Zoomorphology 103: 193-208. RYLAND, J. S. 1970. Bryozoans. Hutchinson and Co., London. SANDERSON, M. J. 1989. Confidence limits on phylogenies: the bootstrap revisited. Cladistics 5: 113-130. SANDERSON, M. J. AND M. J. DONOGHIJE. 1989. Patterns of variation in levels of homoplasy. Evolution 43: 1781-1795. SAVAZZI, E. 1991. Burrowing in the inarticulate brachiopod Lingula anutinu. Palaeogeogr., Palaeoclimatol., Palaeoecol. 85: 101-106. SAWADA, N. 1973. Electron microscope studies on gametogenesis in Lingulu ungub Zool. Mag. (Tokyo) 82: 178-188. SCHOPF, T. J. M. ANII F. T. I&lhPIEIM. 1967. Chemical components of Ectoprocta (Bryozoa). J. Paleontol. 41: 1197-1225. SCHRAM, F. R. 1991. Cladistic analysis of metazoan phyla and the placement of fossil Problematica. In: A. M. Simonetta and S. Conway Morris (eds). The Early Evolution of Metazoa and the Significance of Problematic Taza. Cambridge Univ. Press, Cambridge, England, pp. 35-46. SCHUCHERT, C. 1893. A classification of the Brachiopoda. Am. Geol. 11: 141-167. SCHUCHERT, C. 1897. A synopsis of American fossil Brachiopoda, including bibliography and summary. Bulletin U. S. Geological Survey (U.S.) 87: l-464. SENN, E. 1934. Die Geschlechtsverhaehnisse der Brachiopoden, im besonderen die Spermato und Oogenese der Gattung Lingda Acta Zool. (Stockh.) 15: 1-154. SIDDALL, M. E. 1995. Random Cladistics. Virginia Institute of Marine Science, College of William and Mary. SUN, L. 1954. On the nervous system of Phoronis.Ark. Zool. 2 (6) : l-40. SOBER, E. 1983. Parsimony in systematics: philosophical issues. Annu. Rev. Ecol. Syst 14: 335- 357. SOBER, E. 1985. A likelihood justification of parsimony. Cladistics 1: 209-233. STORCH, V. AND U. WELSCH. 1972. Uber bau und Entstehung der Mantehandstachehr von Lingulu unguis L. (Brachiopoda). Z. Wiss. Zool. 183: 181-189. STORCH, V. AND U. WELSCH. 1976. Electron microscopical and enzyme histochemical investigations on lophophore and tentacles of Lingula unguis L. (Brachiopoda). Zool. Jahrb. (Anat.) 96: 225-237. STRATHMANN, R. R. 1978. The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32: 894-906. STRATHMANN, R. R. 1985. Feeding and nonfeeding larval development and life history evolution in marine invertebrates. Annu. Rev. Ecol. Syst. 16: 339-361. STRKXER, S. A. AND C. G. REED. 1985a. The ontogeny of shell secretion in Terebmtalia tranruersa (Brachiopoda, Articulata). I. Development of the mantle. J. Morphol. 183: 233-250.

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S. A. AND C. G. REED. 1985b. The ontogeny of shell secretion in Tembratalia &utuuersa (Brachiopoda, Articulata) . II. Formation of the proteguhun and juvenile she&J. Morphol. 183: 251-272. Srnrm S. A. AND C. G. REED. 1985c. Development of the pedicle in the articulate brachiopod Terdmtah transversa (Brachiopoda, Terebratuhda). Zoomorphology 105: 253-264. STRIS. A. AND C. G. REED. 1985d. The protegtdum and juvenile shell of a Recent artidate brachiopod: patterns of growth and chemical composition. Lethaia 18: 2954303. STRICIZER,S. A, C. G. REED AND R. L. ZIMMER. 1988. The cyphonautes larva of the marine bryozoan Membran$wra membmnucea. I. General morphology, body waII, and gut. Can. J. Zool. 66: 368-383. .C&OFFORD, D. L. 1993. PAUP-Phylogenetic Reconstruction Using Parsimony, Ver. 3.1.1. IlIinois Natural History Survey, Champaign, Blinois. TA~ENER-!%~TH, R. AND A. WILLIAMS. 1972. The secretion and structure of the skeleton of living and fossil Bryozoa. PhiIos. Trans. R Sot. Land. Ser. B Biol. Sci. 264: 97-159. TI-IOMSON, J. A. 1927. Brachiopod morphology and genera (Recent and Tertiary). New Zealand Board of Science and Art, Manual 7: l-338. TVROS, N. AND L. W. USHER. 1986. The proteins in the shell of L&g&u In: R E. Crick (ed.). Origin, Evolution, and Modern Aspects of Biomineralization in Plants and Animals. Plenum, New York, pp. 325-328. USHATINS~AYA, G. T. 1986. Brachiopods of the Cambrian (review of localities and some patterns of geographic distribution). In: L. P. Tamarinov et al (eds) . Problems in the Paleobiogeography of Asia. Joint Soviet-Mongolian Paleontologic Expedition. Trudy, vyp. 29. Nauka, Moscow, pp. 8-34. VALENTINE. J. W. 1975. Adaptive strategies and the origin of grades and ground-plans. Am. Zool.15: 391-404. VALENTINE, J. W. 1987. Invertebrate organization: a review. In: R S. Boardman, A. H. Cheetham, and A J. RoweII (eds). Fossil Invertebrates. Blackwell Scientific, Palo Alto, pp. 4-18. VALENTINE, J. W. 1992. The macroevolution of phyla. In: J. H. Lipps and P. W. Signor (eds) . Origin and Early Evolution of the Metazoa. Plenum Press, New York, pp. 525-553. VALENTINE, J. W. AND D. H. ERWIN. 1987. Interpreting great developmental experiments: the fossil record. MBL (Mar. Biol. Lab.) Lect, Biol. 8: 71-107. VAN Bm, J. F. 1883. Untersuchungen tiber den anatomischen und histologischen Bau der Brachiopoda Testicardinia. Jenaische Z. Nattuw. 16: 88-161. Vm, G. J. 1989. The origin of skeletons. Palaios 4: 585-589. WAAGEN, W. 1882-1885. Salt Range Fossils. Pt 4(2). Productus Limestone fossils, Brachiopoda. Paleontologia Indica 13: 329-770. Wm~m, C. D. 1912. Cambrian Brachiopoda. U.S. Geol. Surv. Monograph 51:1-872. WATABE, N. AND GM. PAN. 1984. Phosphatic shell formation in atremate brachiopods. Am. Zool. 24: 977-985. WATROUS, L. E. AND Q. D. WHEELER 1981. The outgroup comparison method of character analysis. Syst. Zool. 33: 83103. WHEELER, W. C. 1992. Extinction, sampling, and molecular phylogenetics. In: M. J. Novacek and Q. D. Wheeler (eds). Extinction and Phylogeny. Columbia Univ. Press, New York, pp. 205-215. WILEY, E. 0. 1981. Phylogenetics, The Theory and Practice of Phylogenetic Systematics. J. Wiley 8c Sons, New York. WILLIAMS, A. 1956. The calcareous shell of the Brachiopoda and its importance to their classification. Biol. Rev. Camb. Philos. Sot. 31: 243-287. WAS, A 1968. Evolution of the shell structure of the articulate brachiopods. Spec. Pap. Palaeontol. 2: l-55. WILLIAMS, A 1970. Origin of 1aminar~helIed articulate brachiopods. Lethaia 3: 329-342. WILLIAMS, A 1971. Comments on the growth of the shell of articulate brachiopods. Smithson. Contrib. Paleobiol. 3: 47-64. WILLIAMS, A 1973. The secretion and structural evolution of the shell of thecideidine brachiopods. Phiios. Trans. R Sot. Lond. 264B: 439-477. Srtua

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In: J. Bereiter-Hahn, A G. Matoltsy and E. S. Richards (eds.). Biology of the Integument, Vol. 1, Invertebrates. Springer-Verlag, Berlin, pp. 728-745. WILLIAMS, A. 1990. Biomineralization in the lophophorates. In: J. G. Carter (ed.). Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends, Vol. 1. Van Nostrand Reinhold, New York, pp. 67-82. WILLIAMS, A. ANII J. M. HURCX. 1977. Brachiopod evolution. In: A Hallam (ed.). Patterns of Evolution as Illustrated by the Fossil Record. Elsevier, Amsterdam, pp. 79-121. WILLIAMS, A. AND A J. ROWELL.1965. Brachiopod anatomy and morphology. In: R C. Moore (ed.). Treatise on Invertebrate Paleontology, Part H. Geol. Sot. Am. and Univ. Kansas, Boulder, Colorado and Lawrence, Eansas, pp. H6H155. WILLMER,P. 1990. Invertebrate Relationships. Cambridge Univ. Press, Cambridge, England. WOOL,LX~TT, R M. AND R L. ZMMER 1971. Attachment and metamorphosis of the cheilostome bryozoan Bugulu titinu (Linni). J. Morphol. 134: 351-382. WRIGHT, A. D. 1979. Brachiopod radiation. In: M. R House (ed.). The Origin of Major Invertebrate Groups. Academic Press, London, pp. 235-252. YANo, H., K SATAKE, Y. UENO, R KONDO AND A. Tsucrr~. 1991. Amino acid sequence of the hemerythrin alpha subunit from Lingula zcnguti. J. Biochem. 110: 376380. ~TSU, N. 1962. On the development of Lingula unutinu. Journal of the College of Science, Tokyo Imperial Iniversity 17: 1-l 12. ZIMMER,R L. 1964. Reproductive biology and development of Phoronida. Ph.D. diss. Univ. Washington. ZIMMER,R L. 1973. Morphological and developmental affinities of the lophophorates. In: G. C. Larwood (ed.). Living and Fossil Bryozoa. Academic Press, New York, pp. 593400. I ZIMMER,R L. 1991. Phoronida. In: A. C. Giese, J. S. Pear-se and V. B. Pearse (eds). Repro duction of Marine Invertebrates, Vol. 6. Boxwood Press, Pacific Grove, California, pp. 145. ZIMMER, R L. AND R M. WOOLLACOTT.1977. Metamorphosis, ancestrulae, and coloniality in bryozoan life cycles. In: R M. Woollacott and R L. Zimmer (eds.). Biology of Bryozoans. Academic Press, New York, pp. 91-142. ZUMWALT,G. 1976. The functional morphology of the tropical brachiopod 77uxidefine congreguta Cooper 1954. M.S. thesis. Univ. Calif. Davis.

90 100 NNNNNNNNNN NNNNNNNNNN 2000N3NONN NOOONNlNO2 OOOONONUOO OlOlNOOOOl llOON20U02 lllPN00312 NNNNNNNNNN NNNNNNNNNN NNNNNNNNNN NNNNNNNNNN 1320011323 1200210102 NNNNNNNNNN NNNNNNNNNN llOP111322 1201PlOlPl 1101111314 1200010101 1200N11132 02010N0001

80 ONNNNNNNNN llNOllN211 OONOllNOOO OONO2OOOON ONNNNNNNNN 1NNNNNNNNN 011210221N ONNNNNNNNN 011220111N 011220111N 110201N122

Bryozoa Craniacea Discinacea Lingulacea Phoronida Pterobranch Rhynchonell Sipuncula Terebratell Terebratul Thecideacea

30 PlUONNNNOO 1021111000 llUllOOlll 11011001~1 lOUONNNNO0 lOUONNNNO0 21ulOUU212 UNUONNNNOO 2111OUU212 21ulOuU212 21UlOUU204

20 12NOlUOlUl 1011131121 UO402311Ul 0040241101 P130001121 UO21001211 u211P21221 lOOPlOOOOO U111121221 ulllP21221 U2111212Ul

10 UOlUUOPlll lUlUO11121 lUlU31OUlU 1210210110 lllONPPll1 1lllNPlOOU 1110111021 OUOONPUOOU lllOlP102U 1110111021 lUlUlllUll

Character

Bryozoa Craniacea Discinacea Lingulacea Phoronida Pterobranch Rhynchonell Sipuncula Terebratell Terebratul Thecideacea

Taxon

110 NNNNONNNNN 2OlNONNlON OOONONN2ON 12PNONN20N NNNNONNNNN NNNNONNNNN 012111NOOl NNNNONNNNN P121121102 OlP1120102 01202NNO13

NN 23 12 13 NN NN 32 NN 42 42 UU

50 OOOOONlOOU 1031101221 1022102121 1026101121 1000103011 20002NllOl 111311112U 1005102020 1113101121 111310112U 111410112U

60 001N000211 1010010200 lOlOOUOOOO 1010110100 2OONlON200 000NlU0210 1111111000 000N000300 1111111000 1111111000 lllllUO2OO

N = not applicable; P = polymorphic.

40 NNlOOOOOOO NN11111121 0011112121 0011112121 NNlllOOOOO NN22400001 1111111011 NNO2400000 1111201010 1111201010 lN113.lOUlO

Data matrix. Data coded as “missing” indicated as: U = unknown;

Appendix1

7Q 112NNNNP00 1210010100 2111ONNOOl 21031NNOOO ONNNNNNNON ONNNNNNNON 121210N301 12NNNUUUOU 121210N221 1212101221 121111N221

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Appendix 2 EMBRYOLOGY 1. Mesoderm: 0 = from 4d stage (entomesoderm) ; 1 = from archenteron (pouches). [l.OO, -, -1. Mesoderm forms from the archenteron in ah brachiopods and pterobranchs; this is the “typical” deuterostome condition (Long, 1964; Zimmer, 1973; Brusca and Brusca, 1990; Chuang, 1990; Long and Snicker, 1991). Sipuncuhds represent the “typical” protostome condition. Mesodetm formation in bryozoans is poorly known (Zimmer, 1964; Reed, 1991). In phoronids, mesoderm formation is “dissimilar totally from typical protostomes”, and is “comparable to enteropneusts,” but Ts not developed from archenteric diverticula” (Zimmer, 1964); phoronids are coded as deuterostomes because they are much closer to this mode of formation than any other (G. Freeman, pers. comm. 1994). 2. Gastrulation: 0 = delamination; 1 = imagination with epiboly; 2 = invagination without epiboly. [ 1.00, -, -1. Gastrulation is by imagination with epiboly in pterobranchs, phoronids (Zimmer, 1991; Long and Snicker, 1991), and aII brachiopods (Hyman, 1959; Long, 1964; Chuang, 1990), except lingulaceans and perhaps thecideaceans (Nielsen, 1991). Kovalevsky (1874) claimed to document gastrulation by primary delamination in Lacuzellu (Williams and Rowell, 1965), as observed in bryozoans (Hyman, 1959). No one has attempted, to date, to reproduce Kovalevsky’s analysis, and its accuracy is doubtful (Long, 1964). LinguIaceans invaginate without epiboly (G. Freeman, pers. comm. 1994). Sipunculid gastrulation is coded as unknown. 3. Cleavage mode: 0 = spiral; 1 = radial or biradial. [ 1.00, -, -1. Cleavage mode in all but sipunculids is radial (or biradial) and regulative (Hyman, 1959; Long, 1964; Zimmer, 1964, 1973, 1991; Brusca and Brusca, 1990; Willmer, 1990; Long and Snicker, 1991). This is the “typical” deuterostome condition; sipuncuhds exhibit the protostome condition (spiral and mosaic) which, in this analysis, appears as an autapomorphy, rendering the character phylogenetically uninformative. Zimmer (1964) claims that brachiopods “corre spond more closely to phoronids than do the bryozoa” in details of cleavage patterns. 4. Origin of mouth: 0 = from blastopore; 1 = from elsewhere (but usually near the blastopore) . [ 1 .OO,-, -1. The mouth originates from the blastopore in protostomes, and from some site other than (but often close to) the blastopore in deuterostomes. Phoronids (Zimmer, 1964,1973,1991; Nielsen, 1991) and sipunculids (Brusca and Brusca, 1990) exhibit the protostome condition; pterobranchs are deuterostomous (Brusca and Brusca, 1990). Bryozoms are problematic; Nielsen (1991) states that the “fate of the blastopore is uncertainn while Zimmer (1964) claims that the mouth is clearly not related to the site of gastrulation, implying that bryozoans are deuterostomous with respect to this character. Brachiopods appear to exhibit the protostome condition, although this is not without controversy, either (Reed, 1987). Long (1964) states that, in the articulates, the mouth forms very near the anterior end of the blastopore, perhaps in the same spot, but only after the blastopore closes completely (also G. Freeman, pers. comm. 1994). Hyman (1959), Brusca and Brusca (1990), Chuang (1990) and Nielsen (1991) characterize

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both articulates and inarticulates in this manner, but the condition in craniaceans, discinaceans, and thecideaceans is actually not known. Lingulaceans are clearly protostomous (Yatsu, 1902). 5. Mantle rudiment (from larva): 0 = does not reverse (appear in adult position) at settlement; 1 = reverses at settlement and metamorphosis; 2 = reverses during embryogenesis; 3 = reverses during the pelagic stage of development. wm -9 -1. A larval mantle rudiment is present only in brachiopods; this character does not apply to any of the four outgroups. Although cyphonautes larvae (of some bryozoans) possess a bivalved mineralized shell, the valves are shed at or shortly after metamorphosis; the epidermis that secretes the valves is not considered to be a umantle rudiment”. The mantle rudiment does not reverse in the craniaceans (Nielsen, 1991). In the lingulaceans, the mantle first appears in the adult position during embryogenesis (Yatsu, 1902)) while in discinaceans it first appears later in development (G. Freeman, pers. comm., 1994). In all articulate brachiopods, the mantle rudiment reverses (turns “inside out”) at settlement and metamorphosis, prior to mineralizing the valves (Chuang, 1977; Reed, 1987). This is considered to be an apomorphic condition for Articulata (Williams and Rowell, 1965; Rowell, 1982), but none of the outgroups in this study have the power to polarize the direction of character change.

6. Sexes: 0 = not always separate, 1 = always separate. [l.OO, -, -1. All brachiopods are dioecious (Hyman, 1959; Percival, 1960; Chuang, 1983; Reed, 1987; Brusca and Brusca, 1990; Nielsen, 1991; Long and Snicker, 1991; James et al., 1992), except certain terebratellaceans (Senn, 1934; Hyman, 1959; Williams and Rowell, 1965) that are monoecious. Some species of sipunculids, phoronids, and pterobranchs (Emig, 1983; Brusca and Brusca, 1990; Zimmer, 1991) are monoecious; others are dioecious. Bryozoans are mostly monoecious (Hayward, 1983; Brusca and Brusca, 1990), which is thought to represent the primitive condition (Emig, 1983). 7. Egg size: 0 = small (from 50-100 pm), with little or no yolk (typical plankto trophs); 1 = large (from 110-200 pm), with lots of yolk (brooders or nonplanktotrophs) . [ 1 .OO,-, -1. Egg size is generally large among craniaceans and articulate brachiopods (Percival, 1960; Long, 1964; Zumwalt, 1976; Chuang, 1983; Reed, 1987; Nielsen, 1991; James et al., 1992). Lingulacean eggs are small (Chuang, 1983a; Nielsen, 1991). Discinaceans also have small eggs (G. Freeman pers. comm., 1994). Egg size varies widely among species of bryozoans (Hayward, 1983; Reed, 1991) and phoronids (Emig, 1982; Zimmer, 1991). Pterobranchs have relatively large, yolky eggs (Hyman, 1959). I could find no report of egg size among sipunculids. A substantial number of characters related to larval ecology (in this study, characters 7, 10, 11, 12, 14) have been demonstrated to covary in a complex manner, to a greater or lesser extent, among marine invertebrates (Suathmann, 1978, 1985). Planktotrophic (feeding) larvae spend a long time (weeks to months) in the plankton. They tend to have parents that free-spawn (over a long period of time) large numbers of small eggs with little yolk. Non-plankto

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trophic (non-feeding) larvae are in the plankton for only a short time (hours to days) ; their parents tend to either brood (and have small body sizes) or free-spawn (for a short period of time) smaller numbers of relatively large yolky eggs. 8. Sperm morphology: 0 = ect-aquasperm (“primitive type”-small acrosome, short midpiece, long flagellum); 1 = ent-aquasperm (large acrosome, >I mitochondrion). [0.50,0.67,0.33]. Several different types of sperm morphologies have been distinguished (Franzen, 1956, 1977; Sawada, 1973; Afzelius and Ferraguti, 1978; Chuang, 1983b; Rouse and Jamieson, 1987). Wtihner (1990) claims that pterobranchs and sipunculids have ect-aquasperm, present also in articulate brachiopods (James, 1989; Long and Stricker, 1991; James et al., 1992) except for thecideaceans, whose sperm morphology, like discinaceans, is not known. This type is common among animals with external fertilization (Afielius and Ferraguti, 1978) and is characteristic of lower deuterostomes (Jarnieson, 1985). Bryozoans, phoronids, and lingulacean and craniacean brachiopods have more complex types of sperm, usually with larger (or no) acrosome, longer midpiece, spherical nucleus, more numerous and more and less complex anchoring apparatus. spherical-shaped mitochondria, Complex ent-aquasperm appears to be primitive, while ect-aquasperm has evolved at least twice independently. 9. Gametes develop from folds of coelomic epithelium: 0 = in body tissues; 1 = in body cavity, where they stay; 2 = move from body cavity to mantle canals. [0.67,0.75,0.50]. Gametes develop from the body tissues (metasome) in both sipunculids and pterobranchs, before being released into the coelom where they mature (Brusca and Brusca, 1990). In bryozoans (Hayward, 1983; Reed, 1991) and phoronids (Emig, 1982; Zimmer, 1991), gametes develop entirely in the body cavity; this is the primitive condition in this study. Mantle canals, which are tube-like extensions of the body cavity within the mantle, serve as gonads for craniaceans and the articulates (Hyman, 1959; Williams and Rowell, 1965; Chuang, 1983; Long and Snicker, 1991; James et al., 1992); they appear to have evolved independently in each. Gametes develop in the body cavity, on the ileoparietal band, and don’t migrate to the mantle canals in discinacean and lingulacean brachiopods (Williams and Rowell, 1965). Thecideaceans are problematic. Pajaud (1970) and Zumwalt (1976) claim that gonads are located in the ventral body cavity, while Hyman (1959) says they are located in the mantle lobes. No mantle canals have been described for thecideaceans, and I have tentatively coded them as “1”. 10. Number of gametes released per spawning: 0 = large number (5&150 000); 1 = small number (443000). [ 1.OO,-, -1. The number of gametes (usually eggs per female) released in each spawning event, as a rough measure of fecundity, is diicult to accurately quantify and many uncertainties exist (pterobranchs, sipunculids, and discinacean and terebratellacean brachio pods). Consistent with their planktotrophic larval ecology, lingulaceans release large numbers of eggs (up to several thousand per day) over long spawning periods (Williams and Rowell, 1965; Reed, 1987; James et al., 1992). Bryozoans (Hayward, 1983; Reed, 1991), phoronids (Emig, 1982; Zimmer, 1991), craniaceans (Nielsen, 1991), terebratulaceans (Long, 1964), rhynchonellaceans (Percival, 1960) and thecideaceans (Zumwalt, 1976) that

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freespawn all release relatively few gametes per spawning. Brooders typically develop very small numbers of gametes per brood. 11. Time span of gamete release: 0 = long time (over weeks or months); 1 = short time (in a single burst). [l.OO, -, -1. Information on the timing of gamete release is quite sketchy among most of these taxa. Bryozoans (Hayward, 1983; Reed, 1991), sipunculids (Hyman, 1959), and craniaceans (Nielsen, 1991) appear to release gametes in single bursts lasting from a few hours to days, . while lingulaceans (Kume, 1956; Chuang, 1959, 1983; Williams and Rowell, 1965; Long and Stricker, 1991) spawn in a succession of bursts for periods of up to three months. Phoronids vary from species to species (Zimmer, 1991). The more that breeding season is studied, the more it appears to vary considerably among species and with the temperature of the environment, and to persist through much of the year, rather than being concentrated in a narrow, seasonal time interval. 12. Gamete dispersal mode: 0 = all free-spawners; 1 = some free-spawn, some brood; 2 = most brood, a few free-spawn. [0.50,0.50,0.25]. The frequency of brooding varies among these taxa, although the homology of this character is certainly not clear. Brooding is most common among species of very small adult body size, regardless of their phylogenetic affinity, but also occurs in some larger-bodied species. Sipunculids, pterobranchs and the inarticulate brachiopods only free-spawn (the primitive condition here), whereas brooding is quite common among bryozoans (Hayward, 1983; Brusca and Brusca, 1990; Chuang, 1990; Reed, 1991; although some gymnolaemates free-spawn), as it is in rhynchonellacean (Percival, 1960; Long, 1964) and thecideacean brachiopods (Hyman, 1959, citing Lacaze-Duthiers, 1861) and has been reported in phoronids (Zimmer, 1964, 1991; Brusca and Brusca, 1990) and terebratulide brachiopods (Hyman, 1959; Long, 1964; Williams and Rowell, 1965; Reed, 1987; Long and Stricker, 1991; James et al., 1992). LARVALBIOLOGY 13. Larval type: 0 = trochophore; 1 = unnamed larva (“highly modified trochophore”); 2 = dipleurula; 3 = actinotroch; 4 = “pelagic adults.” [ 1.00, 1 .OO,1 .OO]. Trochophore larvae are characteristic of many protostome taxa, including sipunculids, while dipleurula larvae characterize the deuterostomes, including pterobranchs (Hyman, 1959; Zimmer, 1973; Brusca and Brusca, 1990; Willmer, 1990). The larvae of all brachiopods are described almost universally as “highly modified trochophores” (Brusca and Brusca, 1990; Nielsen, 1991), but they are consistently and very distinctly different from typical trochophore larvae. Lingulaceans and discinaceans have twolobed larvae rather than the three-lobed larvae characteristic of articulates, and may be more accurately called “pelagic adults” (Chuang, 1990; James et al., 1992; G. Freeman, pers. comm., 1994); craniaceans may also have two-lobed larvae (Nielsen, 1990), but more comparative work is needed to confh-m. The construction into lobes is considered to be a superficial feature, affecting only the ectoderm (Chuang, 1990). Phoronids have actinotroch larvae, which Hyman (1959) claims are the most trochophore-like of all the lophophorates, but Zimmer (1964) claims are unlike either trochophore or dipleurula larvae.

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They are morphologically unlike brachiopod modified trochophores. Bryozoan larvae are morphologically diverse and do not fit easily into any of these categories. 14. Duration of free-swimming larval stage: 0 = long time (weeks to months), related to direct development; 1 = short time (hours to days), related to indirect development [0.33,0.33,0.11]. The length of time a larva remains in the plankton is frequently related to its ability to feed or not, and is easier to observe than actual feeding behavior. Phoronids (Zimmer, 1991), some non-brooding bryozoans (Hyrnan, 1959; Hayward, 1983), and all lingulacean and discinacean brachiopods (Yatsu, 1902; Brusca and Brusca, 1990; Nielsen, 1991) enjoy relatively long-lived planktotrophy; these planktotrophs also possess statocysts (Chuang, 1977) as mechanoreceptors. Pterobranchs (Hyman, 1959) and craniacean (Nielsen, 1991) and articulate brachiopods (Hyman, 1959; Percival, 1960; Williams and Rowell, 1965; Chuang, 1977, 1990; Reed, 1987) have short-lived non-planktotrophic larvae, although they may have achieved this state independently. Sipunculids include species of each type. Not surprisingly, the length of time larvae remain in the plankton is related to the relative timing of early developmental events. Planktotrophic larvae commonly exhibit direct development, in which the initiation of develop ment of the lophophore, mixonephridia, and adult alimentary canal occurs before larval settlement (e.g. bryozoans with cyphonautes larvae, lingulaceans, discinaceans) . Organisms with nonplanktotrophic larvae (e.g. craniaceans, articulate brachiopods) exhibit indirect development, where these events occur after settlement and metamorphosis. 15. Larval sense organs: 0 = present as papillae or cilia; 1 = present as pigment spots or “eye spots” or ocelli; 2 = absent. [0.67, 0.50, 0.331. Bryozoan and sipunculid larvae have well-developed ocelli (light-sensitive pigment spots; Hyman, 1959; Brusca and Brusca, 1990). Phoronid actinotrochs have sensory papillae (Zimmer, 1964); pterobranch dipleurula larvae have a long tuft of cilia that functions as an apical sense organ (Hyman, 1959). Many brachiopod larvae have’pigment spots (Yatsu, 1902; Hyman, 1959; Percival, 1960; Long, 1964; Williams and Rowell, 1965; Nielsen, 1991; James et al., 1992). Discinaceans, lingulaceans and some rhynchonellides and some terebratulids lack pigment spots, however (Long, 1964; Long and &ticker, 1991; G. Freeman, pers. comm., 1994). 16. Larval setae (chaetae) ; number of pairs of bundles: 0 = none (absent); 1 = one pair, 2 = two pairs; 3 = three pairs; 4 = not in bundles (all around larva). [l.OO, 1.00, l.OO]. Phoronids (Zimmer, 1964), pterobranchs (Hyman, 1959) and sipunculids (Brusca and Brusca, 1990) have no larval setae (the primitive condition). Bryozoan cyphonautes larvae possess “sensory bristles”, but their relationship to setae is unclear (Hyman, 1959; Reed, 1991). All brachiopods have larval setae (apomorphic for the phylum). The articulates (Hyman, 1959; Williams and Rowell, 1965; Reed, 1987; Chuang, 1977, 1990; Nielsen, 1991; Long and &ticker, 1991) have two pairs of setal bundles (apomorphic for the class), craniaceans (Nielsen, 1991) and discinaceans (Yatsu, 1902; Hammond, 1980; Nielsen, 1991) have three pairs, and lingulaceans (Yatsu, 1902) have setae present around the periphery of the larvae, not clustered in discrete bundles.

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Some, but not all, brachiopods possess setae (chaetae) as adults (see character 29). They are not retained from the larvae, but are shed and then redeveloped. Reed (1987) made the interesting suggestion that the loss of larval chaetae may mark the occurrence of metamorphosis in brachiopods. This event takes place while planktotrophic larvae are in the plankton, but occurs post-settlement in nonplanktotrophic brachiopods. If Reed (1987) is correct, this event can serve as a “correlation datum” with which to compare developmental patterns among all brachiopods. 17. Cell ciliation and ciliary bands for feeding: 0 = multiciliate cells (downstream collectors); 1 = monociliate cells (upstream collectors). [0.50, 0, 01. Nielsen (1987; Willmer, 1990) characterized patterns of cell ciliation and the fimctional morphology of ciliary bands in larvae. In general, protostomes are claimed to have largely multiciliate cells, and be “downstream collectors” of food particles, while deuterostomes have monociliate cells, and are “upstream collectors.” Bryozoans and sipunculids have multiciliate cells, apparently evolved independently in each; all brachiopods, phoronids, and pterobranchs have monociliate cells with ciliary bands that are upstream collecting systems. 18. Single band ciliary feeding mechanism: 0 = absent in both larvae and adults; 1 = present in both larvae and adults; 2 = absent in larvae, present in adults. [0.67, 0.75, 0.501. Strathmann (1978) characterized ciliary feeding mechanisms in marine invertebrates as either “opposed band systems”, typical of protostomes, or “single band systems”, typical of deuterostomes. Sipunculids possess the protostome condition; all other taxa in this study possess single band systems at some stage (s) in their ontogeny. In bryozoans, phoronids and inarticulate brachiopods, the single band system is present in both larvae and adults; this appears to be the primitive state. Delayed appearance in ontogeny (present only in adults) occurs independently in pterobranchs and articulate brachiopods. COELOM 19. Origin of coelomic spaces: 0 = schizocoely; 1 = enterocoely; 2 = highly modified enterocoely. [0.67, 0, 01. Schizocoely is characteristic of protostomes (including sipunculids), while enterocoely is characteristic of deuterostomes (including pterobranchs; Zimmer, 1973; Brusca and Brusca, 1990; Wtlhner, 1990). Although this is widely considered to be a character of funda-’ mental importance in metazoan evolution, the mode of origin of coelomic spaces is acknowledged to be a fairly labile character phylogenetically (Reed, pers. comm. 1987; Nielsen, 1991), as is born out by this study. In phoronids (Ziimer, 1964; Brusca and Brusca, 1990), craniaceans (Nielsen, 1991) and most articulate brachiopods (Long, 1964, Reed, 1987; Chuang, 1990; Long and Stricker, 1991; James et al. 1992), coelomic spaces originate by a highly modified type of enterocoely that can apparently be consistently distinguished from more typical enterocoely. Franzen (1969) claims that Tere~utulina is schizocoelous. Lingulaceans are also reported to be schizocoelous (Yatsu, 1902; Hyman, 1959; Chuang, 1990). The mode of origin of the coelom in discinaceans and thecideaceans is not known, although Hyman (1959) suggests

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21.

22.

23.

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schizocoely and enterocoely, respectively. Bryozoans, perhaps because of their small adult size and greatly reduced coelom, are not well understood (Woollacott and Zimmer, 1971; Brusca and Brusca, 1990; Reed, 1991). Zimmer (1964) claims that all three lophophorate groups exhibit mesenchymatous (enterocoelic) coelom formation, yet Nielsen (1991) cautions that the homology of this character in bryozoans and the other lophophorates is uncertain. Three-fold regionation of body into protosome, mesosome, metasome: 0 = absent (other than three-fold); 1 = present. [l.OO, -, -1. Pterobranchs (and other deuterostomes) and all the “lophophorates” are characterized by a three-fold regionation of the body (Zimmer, 1973; Carle and Ruppert, 1983; Brusca and Brusca, 1990; Willmer, 1990). Sipunculids have a twopart body plan (introvert and trunk), that is clearly different from both deuterostomes and segmented animals (Hyman, 1959). Epistome (from protosome): 0 = absent entirely; 1 = with coelomic cavity (protocoel) ; 2 = without coelomic cavity (tissue-filled). [ 1.00, 1 60, 1 .OO]. Ptero branchs (in preoral disc; Hyman, 1959), phoronids (in preoral hood; Brusca and Brusca, 1990), and inarticulate brachiopods (Yatsu, 1902; Hyman, 1959; Brusca and Brusca, 1990; Nielsen, 1991) possess an epistome with a small, unpaired protocoel (the primitive state), although Nielsen (1991) questions the presence of a protocoel in all brachiopods (craniaceans possess a protocoel in only the earliest larval stages). The epistome is small and filled with tissue in all articulate brachiopods (Hyman, 1959; Zimmer, 1964, 1973; Brusca and Brusca, 1990). An epistome is apparently absent in all bryozoans except the phylactolaemates (Brusca and Brusca, 1990), where its homology is uncertain (Nielsen, 1991). Sipunculids do not possess an epistome (Brusca and Brusca, 1990); homology of the epistome to the introvert is uncertain, but unlikely. Separation between mesocoel (lophophore) and metacoel (body cavity): 0 = distinct regionation; 1 = imperfect separation. [0.50, 0.50, 0.251. The mesocoel and metacoel in pterobranchs, phoronids and craniacean brachiopods (Hyman, 1959; Brusca and Brusca, 1990) are distinctly separated by mesenteries or septae. In bryozoans and all other brachiopods (Hyman, 1959), these two coelomic cavities are imperfectly and indistinctly separated (the primitive state in this study). Sipunculids do not possess a mesocoel; they do, however, possess a separate, fluid-filled “coelom” (termed a “compensation , system”) associated with the tentacles (Brusca and Brusca, 1990). Number of coelomic cavities in early larval stages: 0 = one pair; 1 = two pairs; 2 = four pairs. [ 1.00, -, -1. Lingulacean larvae possess a single pair of coelomic cavities (Yatsu, 1902, also notes the presence of an additional unpaired peduncular cavity), terebratellaceans possess two pairs, and craniaceans possess four pairs (Nielsen, 1991). Variability in this character is very poorly known, and the study of other taxa would be quite valuable.

MANTLESAND SETAE 24. Dorsal and ventral mantles, with mantle canals, that secrete mineralized valves: 0 = absent; 1 = present. [ 1.00, 1.00, 1.001. Mantles are prolongations of

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26.

27.

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S. J. CARTSON

the body wall as folds of ectodermal epithelium; they function to secrete the bivalved shell and enclose the “mantle cavity” in ail brachiopods (Williams and Rowell, 1965; Rowell, 1982; Snicker and Reed, 1985a; Nielsen, 1991; James et al., 1992). They are absent in all four outgroups, with the possible exception of the cyphonautes larva of certain cheilostome bryozoans. These larvae possess a bivalved chitinous shell (Ryland, 1970; Snicker et al., 1988), but the homology of the two valves to brachiopod valves is completely unknown, as is the homology of the “mantle” tissue to the brachiopod mantle. Mantle canals are extensions of the metacoel in folds of the mantle, and occur in all brachiopods with the possible exception of thecideaceans, where mantle canals are quite modified relative to other brachiopods (Hyman, 1959; Williams and Rowe& 1965; Pajaud, 1970; Zumwalt, 1976). This character is often interpreted as three separate characters (e.g. Nielsen, 1991)) yet none ever occurs without the others. Assuming that they are highly correlated with one another, they are coded here as a single character. Mantle epithelium: 0 = continuous at posterior; 1 = divides completely. [l.OO, 1.00, 1.001. Articulate brachiopod mantles are said to be “fused” posteriorly, near the hinge line (Helmcke, 1939, in Hennig, 1966; Williams and Rowe& 1965). Inarticulate mantles are discrete; “a strip of body wall intervenes between the two mantle edges, even around the pedicle” (Williams and Rowell, 1965, p. H9). Nielsen (1991, p. 25) claims that “brachial [dorsal] and pedicle [ventral] valves develop from one epithelial area which becomes completely divided in the three inarticulate groups, but remains continuous along the hinge line in the articulates”. This suggests that discrete mantles are derived relative to continuous mantles according to ontogenetic polarity criteria, consistent with outgroup polarity here. Muscular valve at junction of body cavity and principal mantle canals: 0 = present; 1 = absent. [l.OO, -, -1. Muscular valves are present in both discinacean and lingulacean brachiopods; they are absent in craniaceans (Williams and Rowell, 1965). Their absence in articulates is implied, but never stated; they are coded as “missing” until more definite evidence exists. Marginal canal in connective tissue around mantle margin: 0 = present; 1 = absent. [ 1.00, -, -1. The marginal canal is present in both discinacean and lingulacean brachipods and absent in craniaceans (Hyman, 1959; Williams and Rowell, 1965). Unlike the mantle canals, the marginal canal is not in communication with the body cavity. It contains muscles that control the movement of the mantle margin and setae. As with the previous character, their absence in articulates is implied but never stated (Hyman, 1959); they are coded as “missing” until more definite evidence exists. Mantle groove separating the inner and outer lobes of mantle edge: 0 = absent; 1 = present in marginal canal; 2 = present in terminal branches of mantle canal system. [ 1 .OO, 1 .OO, 1 .OO]. A mantle groove, which contains the setal follicular bases, is (primitively) absent in craniacean brachiopods, but is present in all other brachiopods, either in the marginal canal (in discinaceans and lingulaceans, possessing a marginal canal) or in the mantle canals (Williams and Rowell, 1965). Setae (chaetae) in the marginal canal are more densely arranged than in the mantle canals (Williams and Rowell, 1965).

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29. Adult setae (chaetae) along mantle margin: 0 = absent, 1 = present [0.50, 0.75, 0.381. Setae (sensory bristles) are present, often with barbs or thorns, along the mantle margin in all adult brachiopods (Hyman, 1959) except craniaceans (Williams and Rowell, 1965; Nielsen, 1991), thecideaceans (Williams, 1973) and some terebratellaceans (James et al., 1992). All four outgroups lack setae (chaetae); they have evolved independently in inarticulates and articulates. The setae tend to be clumped along the mantle edge in inarticulates and evenly spaced in articulates; their length varies among taxa. Starch and Welsch (1972), Gustus and Cloney (1972) and Orrhage (1973) documented that brachiopod setae are indistinguishable ultrastructurally from the chaetae of certain annelids and pogonophorans, but question their homology in these apparently distantly related taxa (however, see Ghiselin, 1988).

30. Pedicle: 0 = absent entirely; 1 = present in latest larval stage, juvenile, and adult; 2 = present in juvenile and adult only; 3 = present in larval and juvenile only; 4 = present in larval only. [l.OO, 1.00, 1.001. Pedicles are tough but flexible, cuticle-covered structures that serve as %alks” to anchor most brachiopods to the substrate (Stricker and Reed, 1985c). All four outgroups lack pedicles. They are present in all brachiopods except craniaceans and thecideaceans, both of which have, according to this analysis, retained the primitive, apediculate condition. An alternative, but less parsimonious, possibility is that they have independently lost their pedicles and become cemented to hard substrata from a pediculate common ancestor (Williams and Rowell, 1965). A “pedicle” lobe is apparently present in thecideacean (Lac~Uu) larvae, as in other articulate brachiopods (James et al., 1992), but it degenerates immediately following settlement on the substrate (Kowalevsky, 1874; Pajaud, 1970); the validity of this observation has been questioned, however (Williams and Rowell, 1965). Craniaceans clearly lack both an adult pedicle and a larval pedicle lobe (Nielsen, 1991). Pedicles develop just prior to metamorphosis in lingulacean and discinacean brachiopods; they first appear after settlement and metamorphosis in the articulates. Because the developmental time and place of origin (and morphology) of the pedicle is different in the two classes (see character 31,32), the pedicle is not considered to be strictly homologous in the inarticulates and the articulates (Williams and Rowell, 1965), a conclusion supported here by phylogenetic congruence. 1 = from larval 31. Origin of pedicle: 0 = as ventral mantle imagination; rudiment. [ 1.00, 1.00, 1.001. The pedicle in lingulacean and discinacean brachiopods originates from the inner epithelium as an extension of the ventral body wall; it is covered with a chitinous cuticle, and is continuous with the periostracum covering the mineralized valves (Williams and Rowell, 1965; Rowell, 1982). The pedicle originates from a larval rudiment (the larval “pedicle lobe”) in all articulates. Both states are equally “derived” with respect to the primitive, apediculate condition. 32. Pedicle characteristics: 0 = coelomate and muscular; 1 = not coelomate and

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S.J. CARISON not muscular. [ 1.00, 1.00, 1.001. The pedicle in lingulacean and discinacean brachiopods contains a coelom that is continuous with the main body coelom and has a thick layer of strong muscles under the pedicle epithelium (Williams and Rowell, 1965; MacRay and Hewitt, 1978). Lingulacean pedicles are long and flexible, while discinacean pedicles are very short. The proximal end of these pedicles usually tapers to a thin thread and is not located in a deep infold of cuticle and pedicle epithelium. The distal end, which interacts with the substrate, is usually blunt and often glandular. In terebratulides and rhynchonellides, the pedicle is a short or very short, solid (but flexible) cylinder, containing neither coelom nor muscle (Helmcke, 1939, in Hennig, 1966; Williams and Rowell, 1965). Its proximal end is usually bulbous and located deep in a fold of cuticle and pedicle epithelium. Hyman (1959) attributes this condition to the overgrowth of the larval mantle lobe on the pedicle lobe. The distal end often has rootlets or short papillae. Both states are equally “derived” with respect to the primitive, apediculate condition.

LOPHOPH~RE

33. Lophophore: 0 = ciliated feeding tentacles that surround the mouth and exclude the anus; 1 = as above, with extensions of mesocoel inside tentacles (= “true” lophophore); 2 = as above (with mesocoelic extensions), but does not surround mouth. [ 1.00, -, -1. A “true” lophophore is present in all the lophophorate taxa. Both pterobranchs and siptmculids have tentaculate structures that share several similarities with a true lophophore; at least some of the similarities are homoplastic (Willmer, 1990). Sipunculid “lophophores” contain fluid-filled spaces (the “compensation system”) apparently not homologous with the mesocoel (Brusca and Brusca, 1990); pterobranch “lophophores” exclude both the mouth and anus. Nielsen (1985, 1987) claims that lophophores are not homologous among all the lophophorates. In bryozoans, the larval lophophore degenerates at metamorphosis and adult tentacles develop later as budding occurs. No such degeneration occurs in brachiopods or phoronids. with the information presently in hand, coding this state differently in bryozoans would appear as an uninformative autapomorphy, as it appears in pterobranchs and sipunculids. A comparative analysis of the development of tentaculate structures in a broad range of metazoan taxa is needed to clarify this potentially important character. 34. Number of arms of adult lophophore: 0 = no arms; 1 = two arms; 2 = more than two arms (typically 10-18). [l.OO, 1.00, 1.001. All brachiopods and phoronids possess twoarmed lophophores. Among the pterobranchs, Rhabdopleura also has two arms, although C@m!odi.scus possesses an interesting tentaculate structure with from five to nine pairs of arms (Brusca and Brusca, 1990). Bryozoans have no arms, per se, just a ring of tentacles; this is most likely related to their miniaturized body size. Sipunculid “lophophores” vary from a simple circlet of tentacles to more than 10, highly dissected “lobe-arms”; the number of tentacles increases with the age of the animal (Hyman, 1959).

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35. Lophophore geometry (adult): 0 = trocholophe (may be followed by schizolophe); 1 = spirolophe; 2 = plectolophe (always preceded by aygolophe); 3 = ptycholophe; 4 = other (circular base with straight, frond-like arms). [l.OO, 1.00, 1.001. The arrangement and shape of the arms in the lophophore varies ontogenetically and among adult lophophorates (Rudwick, 1960, 1970; Brusca and Brusca, 1990). Spirolophe lophophores, the primitive adult lophophore geometry, occur in phoronids, all the inarticulates and the rhynchonellides; they point dorsally and coil counter-clockwise in all except the discinaceans where they point ventrally and coil clockwise (Hyman, 1959; Rowell, 1960; Williams and Rowell, 1965). Bryozoans possess trocholophes, which are also characteristic of the youngest (smallest) juvenile brachiopods. Thecideaceans, also small, possess an unusual multi-lobed ptycholophe lophophore. Most terebratulides have plectolophe lophophores in which the arms double-back on themselves before coiling into a central spirolophe (Rudwick, 1970); a few species with very small adult body sizes have trocholophes. Both pterobranchs and sipunculids have a circular base from which more than two straight, flexible “lophophore” arms emerge. 36. Arrangement of lophophore tentacles (= filaments): 0 = along both sides ofarmaxis; l- on only one side of arm axis. [0.50, 0.75, 0.381. Lophophore tentacles are present (primitively) on both sides of the arm axis; all four outgroups share this attribute (Brusca and Brusca, 1990). Terebratulides also possess this characteristic (Hyman, 1959), but have apparently acquired it secondarily, as a reversal to the primitive condition. The inarticulates (Hyman, 1959; Paine, 1962; Williams and Rowell, 1965; Rowell, 1982), rhynchonellides (Rudwick, 1970) and thecideaceans (questionably; Williams and Rowell, 1965) have tentacles on only one side of the lophophore arms, with the brachial lip on the other side. 37. Number of rows of tentacles per side in adult lophophore: 0 = one row (unpaired) throughout ontogeny; 1 = two rows (paired) post-trocholophe stage only; 2 = two rows throughout ontogeny. [0.67, 0.75, 0.501. Tentacles are unpaired in all four outgroups (Brusca and Brusca, 1990). All brachiopods except for thecideaceans possess paired tentacles on either one or both sides of the arm axis (see character 36; Rowe& 1982). The ablabial tentacles are added to the adlabial tentacles (nearest the food groove) in the posttrocholophe stage of development in lingulaceans and discinaceans (Wiiams and Rowell, 1965). Craniaceans, rhynchonellaceans and terebratulides have paired ‘tentacles throughout their ontogeny. Thecideaeans (Williams and Rowell, 1965) have unpaired (adlabial only) tentacles. They are likely to have been derived secondarily from the primitive brachiopod condition of paired tentacles, possibly because of their small (progenetic?) adult size, as a truncation of the development of the ablabial tentacles. 38. Median tentacle of lophophore: 0 = absent throughout ontogeny; 1 = present initially, then lost later in development. [ 1.00, 1.00, 1.001. The lophophore tentacles develop in pairs in all the outgroups (Hyman, 1959). All inarticulates possess a median tentacle early in ontogeny, which is lost at the five pair stage in craniaceans or the 15 pair stage in lingulaceans (Williams and Rowell, 1965). The median tentacle in discinaceans is present as a broad projection of the anterior margin, which is reduced in size after settling (Williams and

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Rowell, 1965). All articulates apparently lack a median tentacle; it is not mentioned in extensive discussions in Hyman (1959), Long (1964) or James et al. (1992). Only Notosutia possesses an %zygous lobe” which later forms the brachial lip; the relationship (if any) of this structure to the median tentacle is not clear (Beecher, 1897, in Rowell, 1960; Williams and Rowell, 1965). A “terminal knob” filled with gland cells is present in a comparable position in pterobranchs (Hyman, 1959)) but is not a median tentacle. 39. Lophophore coelom (mesocoel): 0 = one coelomic space per arm; 1 = two coelomic spaces per arm; 2 = more than two coelomic spaces per arm. [ 1.00, 1.OO, 1.001. All four outgroups possess a single, blindended coelomic space per arm (Hyman, 1959; Brusca and Brusca, 1990). Pterobranch arms contain a single extension of the collar coelom (mesocoel) which is divided into right and left halves by a dorsal and ventral mesentary (Hyman, 1959). All articulates possess two coelomic spaces per arm, a large brachial canal and small brachial canals that arise laterally from extensions of the main body cavity (metacoel) Hyman, 1959; Williams and Rowell, 1965; Zumwalt, 1976). In terebratulides, the metacoel is actually prolonged as a pair of brachial “pouches” along the lophophore arms up to the loop (Williams and Rowell, 1965). In addition to the large and small brachial canals in each arm, all inarticulates also possess various periesophageal spaces in the connective tissue around the pharynx that connect to the small brachial canals (Williams and Rowell, 1965). 40. Internal musculature in adult lophophore arms: 0 = brachial muscles absent or weakly developed; 1 = brachial muscles strongly developed. [0.33, 0.50, 0.173. In sipunculids, the tentacles become mobile from changes in hydrostatic pressure alone (Brusca and Brusca, 1990). Phoronids possess only a few longitudinal muscles that appear to have “slight powers of movement” (Hyman, 1959). Internal musculature is absent or greatly reduced in bryozoan lophophores (Brusca and Brusca, 1990). Strongly developed muscles have evolved at least three times independently in the pterobranchs (with strong longitudinal muscles; Hyman, 1959), the rhynchonellides, and the inarticulates (Williams and Rowell, 1965)) which all lack internal skeletal support for the lophophore. Despite the presence of strong internal muscles, the lophophore in these taxa is apparently not capable of great extension (i.e. beyond the confines of the valves when open; see Ager 1987). Terebratulide tentacles are sheathed by myoepithelium (Reed and Cloney, 1977; James et al., 1992), but the lophophore arms are not very mobile because of stiff connective tissue and the presence of the loop. Thecideaceans also possess tentacles with myoepithelium (Pajaud, 1970) but lack additional muscles, most likely because the lophophore arms are not free, but attached to ridges on the brachial valve. 41. Mucus production of lophophore tentacles: 0 = little or no mucus produced; 1 = produce some mucus (e.g. lining tentacles, etc.); 2 = produce a great deal of mucus (e.g. mucus feeding nets). [l.OO, -, -1. All brachiopods, phoronids, and sipunculids produce some mucus lining the food groove and along the tentacles; bryozoans produce very little or no mucus. Pterobranchs produce elaborate mucus nets important in their feeding behavior (Brusca and Brusca, 1990).

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42. U-shaped alimentary canal: 0 = terminates in anus; 1 = ends blindly. [l.OO, 1.00, 1.001. In all four outgroups and the inarticulate brachiopods, the alimentary canal ends in an anus; it ends blindly in all articulates (Hyman, 1959; Williams and Rowell, 1965; McCammon, 1981; Brusca and Brusca, 1990). 43. Position of anus (relative to mouth) and curvature of gut (from mouth to anus or blind end of gut): 0 = dorsal, curves up; 1 = ventral, curves down; 2 = to the right, curves laterally to the right side; 3 = posterior, does not curve, is straight and along midline. [ 1 .OO,1 .OO,1.001. In all four outgroups, the gut curves up and the anus is dorsal (Hyman, 1959; Brusca and Brusca, 1990; Nielsen, 1991). In all four articulate brachiopods, the gut curves down from the mouth along the midline; no anus is present. The gut curves to the right and the anus is located to the right of the mouth in both lingulaceans and discinaceans (Nielsen, 1991). In craniaceans, the gut does not curve at all and the anus is at the median posterior of the animal (Nielsen, 1991); beyond comparison with these four outgroups (which all have U-shaped alimentary canals), this is considered to be the more primitive condition (Hyman, 1959). 44. Number of digestive diverticula (= liver): 0 = absent entirely; 1 = two (one pair) ; 2 = three (one pair plus one unpaired); 3 = four (two pairs, two ducts); 4 = more than four (from 6 to 16 pairs) ; 5 = one (unpaired) ; 6 = four (one pair plus two unpaired, four ducts). [ 1.00, 1.00, 1.001. Bryozoans, phoronids, and pterobranchs are all apparently lacking digestive diverticula that open through ducts into the stomach (Hyman, 1959; Brusca and Brusca, 1990). Sipunculids possess one rectal gland (diverticulum) off the intestine that secretes digestive enzymes (Brusca and Brusca, 1990). Craniaceans possess one pair of dorsal diverticula with one pair of ducts, discinaceans have one dorsal pair and an additional unpaired ventral diverticulum, and lingulaceans have three dorsal and an unpaired ventral diverticulum, with four separate ducts (Williams and Rowell, 1965). Terebratulides and rhynchonellides (apparently) possess four digestive diverticula; one pair of posterior lobes and one pair of anterior lobes, with one pair of ducts (Hyman, 1959; Williams and Rowell, 1965). Thecideaceans have from 10 to 16 pairs of elongate tubules, and bear little resemblance to the other brachiopods (except for Argyrothecu, a very small-bodied terebratellid that has six to eight pairs of elongate tubules) (Williams and Rowell, 1965). The number of digestive diverticula has increased over time. 45. Metanephridia: 0 = absent entirely; 1 = function also as gonoducts (=mixonephridia); 2 = do not function also as gonoducts (present as glomerulus). [l.OO, -, -1. In all brachiopods, phoronids and sipunculids, the metanephridium (= kidney) also serves as a gonoduct, ridding the body of both waste products and gametes (Hyman, 1959; Brusca and Brusca, 1990). Sipunculid coelomic fluid also contains special multicellular structures called “urns” that function in waste collection. Bryozoans have no distinct excretory system (again, probably related to their miniaturization); they remove wastes by phagocytosis (Hyman, 1959). Pterobranchs possess a weakly developed glomerulus, a structure present in hemichordates and vertebrates. The glomerulus consists of finger-like outpocketings of peritoneum associated

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with the blood sinuses (Brusca and Brusca, 1990); unlike the mixonephridium, it does not act as a gonoduct. 46. Number of mixonephridia: 0 = one pair; 1 = two pairs. [ 1.00, -, -1. Phoronids, sipunculids and all brachiopods except for the rhynchonellides have one pair of mixonephridia; rhynchonellides have two pairs (Hyman, 1959; Brusca and Brusca, 1990). The mixonephridia are short and cornucopia-shaped in all except the lingulaceans where they are long, broad, and flattened (Hyman, 1959). CIRCULATORYAND RESPIRATORY SW-EMS 47. Blood vascular system (circulatory system): 0 = present and closed (confined to vessels, common among protostomes); 1 = present and open (unconfined within body); 2 = absent entirely; 3 = intermediate state between open and closed. [0.67, 0, 01. Articulate, lingulacean and craniacean brachiopods and pterobranchs have fairly well developed blood vascular systems in addition to their coelomic circulatory system (Carle and Ruppert, 1983; Ruppert and Carle, 1983). In all these taxa, the systems are technically “open” because no fully-developed system of vessels is present, but the blood is confined to distinct passages between organs and peritoneal epithelium (Hyman, 1959; Carle and Ruppert, 1983; Brusca and Brusca, 1990). Curiously, the circulatory system in discinaceans is very poorly developed relative to other brachiopods (Hyman, 1959; Williams and Rowell, 1965). Phoronids have a system that is “almost completely closed” (Mill, 1972) or closed “for the most part” (Hyman, 1959); I have coded it as a state intermediate between closed and open. Gas exchange takes place primarily across the walls of the polypide and lophophore tentacles in bryozoans (Hyman, 1959), although Carle and Ruppert (1983) claim that the funiculi between zooids function as a system of “blood vessels” and are homologous to the circulatory systems present in the other lophophorates. I tentatively accept their conclusions and code bryozoans “l”, although the individual/colony homology is problematic. Sipunculids have no blood vascular system, but circulation of fluids and exchange of gases occurs in the ample body coelom (Brusca and Brusca, 1990). Some pterobranchs ( Cqbhalodiscus not RhabdopZeuru) possess gill slits; they are absent in all other taxa in this study. Gill slits are used primarily for feeding and digestion, but they are richly vascularized and clearly important in respiration as well (Brusca and Brusca, 1990). 48. Contractile heart (for nutrient distribution, more than oxygen exchange): 0 = absent; 1 = single heart present; 2 = multiple hearts present. [0.67, 0.50, 0.331. All articulate and lingulacean and discinacean brachiopods and pterobranchs possess a single contractile heart (Buchan et al., 1988; Brusca and Brusca, 1990; G. Freeman, pers. comm., 1994), evolved independently. Bryozoans (Hyman, 1959; Carle and Ruppert, 1983) and sipunculids (Hyman, 1959; Brusca and Brusca, 1990) lack a contractile heart. Craniaceans, strangely, possess several hearts (Hyman, 1959). Phoronids have a non-contractile “haemal plexus” located in the stomach (Hyman, 1959; Mill, 1972); the walls of some of the blood vessels (particularly the lateral, ascending vessel) are highly contractile, however.

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49. Respiratory pigments (as coelomocytes in coelomic fluid): 0 = no special respiratory system or pigments; 1 = present as hemoglobin; 2 = present as hemerythrin. [0.67, 0, 01. Coelomic fluid in the coelomic circulatory system provides a medium for oxygen transport. Respiratory pigments occur as coelomocytes, which are abundant and morphologically diverse (as amoebocytes, granulocytes, erythrocytes, etc.) in the brachiopods (Blochmann, 1900; Morse, 1902; Yatsu, 1902; Prenant, 1928; Ohuye, 1936; James et al., 1992). Hemerythrin is reportedly present in some coelomocytes of all brachiopods (Brusca and Brusca, 1990), but its presence has been confirmed only in Lingula (Kawaguti, 1941; Joshi and Sullivan, 1973; Rowley and Hayward, 1985; Richardson et al., 1987; Yano et al., 1991). Sipunculid (and priapulid) red blood cells also contain hemerythrin (Brusca and Brusca, 1990; Curry and Runnegar, 1990), evolved independent of brachiopods. Phoronids are unusual in that their coelomocytes contain hemoglobin (Zimmer, 1964; Brusca and Brusca, 1990). Bryozoans and pterobranchs lack any special respiratory pigments. Gas exchange occurs across the body walls and across the gill slits in pterobranchs; coelomocytes are rare in their coelomic fluid (Brusca and Brusca, 1990). NERVOUS&STEM 50. Nervous system: 0 = below epidermis of body wall (subepidermal); 1 = within epidermis of body wall (intraepidermal) . [ 1.00, -, -1. Subepidermal nervous systems are common among protostomes; sipunculids are no exception (Hyman, 1959; Zimmer, 1973; Brusca and Brusca, 1990). Bryozoans have a nerve plexus (although much reduced; Brusca and Brusca, 1990), which some locate below the epidermis throughout the body wall (Hyman, 1959; Zimmer, 1964, 1973; Bullock and Horridge, 1965) and others locate intraepidermally (Lutaud, 1973; Carle and Ruppert, 1983). Phoronids apparently possess the deuterostome condition of intraepidermal nerves (Silen, 1954; Zimmer, 1964, 1973; Bullock and Hot-ridge, 1965), however Brusca and Brusca (1990) claim that the nerves are either intraepidermal or immediately subepidermal. Pterobranchs apparently have an intraepidermal plexus in the base of the epidermis (Hyman, 1959; Dilly, 1972), although Brusca and Brusca (1990) claim that it is a subepidermal net-like nerve plexus. Inarticulate brachiopods are mostly intraepidermal (van Bemmelen, 1883, cited by Hyman, 1959), with a nerve plexus in the base of the epithelial lining of the digestive tract, Controversy surrounds the nature of the nervous system in articulate brachiopods. Hyman (1959) claims that van Bemmelen’s drawings of Gq@zus (a terebratulid) show a nerve plexus in the epidermis, although he describes it as being located below the epidermis. She then goes on to say that articulate brachiopod nervous systems are largely subepidermal, in contrast to the intraepidermal systems of the inarticulates. However, Reed and Cloney (1977) demonstrated that the nerves are clearly intraepidermal in Terebrutulia (terebratellid) . Zimmer (1973) claims that brachiopods as a whole are largely intraepidermal; James et al. (1992) agrees. 51. Primary (“cerebral”) ganglion: 0 = supraenteric (dorsal to gut); 1 = subenteric (ventral to gut) 2 = lacking entirely. [LOO, 1.00, LOO]. Bryozoans, ptero

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branchs and sipunculids all possess a supraenteric ganglion only (Brusca and Brusca, 1990). In bryozoans, it is located dorsally on the mesosome, near the pharynx, and gives rise to a circumenteric nerve ring. In pterobranchs, it consists of little more than a thickening of the dorsal nerve plexus. Pterobranchs also possess a short, mesosomal, dorsal nerve cord; its homology with the chordate nerve cord is uncertain (Brusca and Brusca, 1990). Sipunculids have a dorsal, bilobed cerebral ganglion in the introvert. The entire nervous system in phoronids is somewhat diffuse; a cerebral ganglion is lacking. All brachiopods have a large, conspicuous subenteric ganglion (Hyman, 1959, citing van Bemmelen, 1883; Bullock and Hoi-ridge, 1965; Williams and Rowell, 1965). 52. Secondary ganglion: 0 = absent; 1 = present as small supraenteric ganglion. [ 1.00, 1.00, 1.001. A small and inconspicuous secondary ganglion, dorsal to the gut, is present in all the articulate brachiopods; it is absent in the four outgroups and the inarticulates (Hyman, 1959, citing van Bemmelen, 1883; Bullock and Horridge, 1965; Williams and Rowell, 1965; Brusca and Brusca, 1990). MUSCULAR&STEM 53. “External” muscles that attach body to external “casing”: 0 = absent (body moves by internal muscles and hydrostatic change); 1 = present (move body with respect to zooecia or valves). [ 1 .OO, 1.OO, 1 .OO]. Lophophorates exhibit a “tendency” to secrete tubes, outer casings (Brusca and Brusca, 1990) or cuticles (Carle and Ruppert, 1983). All bryozoans and brachiopods with mineralized (or non-mineralized) zooecia or valves possess “external” muscles that attach these structures to the body. Phoronids live in chitinous tubes; pterobranchs live in non-chitinous tubes. Their bodies can be retracted (and protracted) within the tubes, but this is accomplished by the action of muscles (longitudinal, also circular in some) within the body of the animal, not external to it (Hyman, 1959; Brusca and Brusca, 1990). Sipunculids have no external casing, and thus no external muscles. 54. Muscle system (with respect to mineralized valves): 0 = “complex” (3-4 adductors, no diductors, 2-3 prs obliques, (+/-) 1 pr. lateral, and other minor muscles) ; 1 = “simple” (2 pr. adductors, l-2 pr. diductors, (+/-) 2 pr. adjustors; no obliques). [ 1.OO, 1.00, 1.001. All brachiopods possess muscles that attach the body to the valves, move the valves relative to one another, and move the setae and mantle at the mantle edge; some also have muscles that move the lophophore (see character 40,55), move the pedicle (character 32) and move the body relative to the pedicle (Hyman, 1959; Williams and Rowell, 1965; Rudwick, 1970; Brusca and Brusca, 1990). All inarticulates have a muscle system consisting of various numbers of adductor, oblique and lateral muscles (Bulman, 1939); all lack diductor muscles, in keeping with the lack of true articulation between the valves. All articulates except thecideaceans have a muscle system consisting of two pairs each of adductors, diductors and adjustors (which move the body relative to the pedicle) ; they lack oblique muscles, in keeping with the presence of articulating hinge structures that prevent the oblique movement of one valve relative to the

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other. Thecideaceans have only one pair of diductors and no adjustors, since they lack pedicles. 55. Lophophore muscles: 0 = present; 1 = absent (but may be present within tentacle epithelium) . [0.25,0,0]. Bryozoans, sipunculids and craniacean and discinacean brachiopods possess muscles (brachial elevator, protractor and retractor muscles), external to the lophophore, that move the lophophore relative to the rest of the body (Hyman, 1959; Williams and Rowell, 1965; Brusca and Brusca, 1990). Phoronids, pterobranchs and lingulacean and articulate brachiopods all lack these muscles; they have apparently been lost at least three times independently. 56. Muscle fibers: 0 = smooth only; 1 = smooth and striated. [ 1.00, 1.00, 1.001. Lingula (Chuang, 1956; Starch and Welsch, 1976; Kuga and Matsuno, 1988), Crania and the articulates (Rudwick, 1970; Brusca and Brusca, 1990) possess smooth and striated muscles (Atkins, 1958; Williams and Rowell, 1965 [H34]; Reed and Cloney, 1977). Muscle fibers in the body wall of phoronids and sipunculids are smooth (Hyman, 1959). Bryozoan muscles, when present, appear to be smooth also (Ryland, 1970). Pterobranchs apparently possess only smooth muscles also; Hyman (1959) is skeptical of the report of crossstriated fibers in the collar region of Cqbhabdiscus (Ridewood, 1907). There appears to be a strong functional component to the presence or absence of striated muscle fibers in lophophore tentacles (Reed and Cloney, 1977); they occur in taxa with mobile tentacles, in which the speed of retraction of the tentacles is critical. Interestingly, striated fibers occur in six subtidal individuals of Terebratalia transversa, but are consistently lacking in six intertidal individuals examined by Reed and Cloney (1977). Interspecies (and apparently intraspecific) variation in this character is high. 57. Muscle type: 0 = columnar muscles; 1 = tendinous muscles. [l.OO, 1.00, 1.001. External muscles (outside the body wall) of bryozoans, pterobranchs, sipunculids and thecideacean and inarticulate brachiopods are columnar; muscle fibers extend from origin to insertion with no intervening tendons (Hyman, 1959; Williams and Rowell, 1965; Rudwick, 1970). Phoronids have no comparable muscles. Muscles in the rhynchonellides and terebratulide brachiopods are tendinous; muscle fibers extend only a short distance from their origin on each valve and are united by a tendon spanning the mantle cavity. ECOLOGY AND MODE OF LIFE

58. Mode of attachment to substrate: 0 = pediculate and attached to hard substrate; 1 = pediculate free-living (mobile) in soft substrate; 2 = apediculate (as adults) and cemented to (or immobile on) hard substrate; 3 = apediculate (as adults) and free-living (but sedentary) on soft substrate. [0.75,0.67,0.50]. All four outgroups lack a pedicle and, except sipunculids, are either cemented or permanently attached to the substrate (Hyman, 1959; Williams and Rowell, 1965; Brusca and Brusca, 1990). Some bryozoans (MonoZqozoon) are somewhat mobile, but this is a rare exception. Sipunculids are free-living and can burrow into soft or semi-hard substrates (Rice, 1969), but are basically sedentary animals. Craniacean and thecideacean brachiopods appear

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to retain this primitive apediculate, cemented condition. Discinacean, rhynchonellide and terebratulide brachiopods are pediculate and live attached to hard substrates (although see Richardson and Watson, 1975). Lingulaceans are pediculate and secondarily free-living, exhibiting a burrowing behavior unique among the brachiopods. Consistent with the differences in pedicle morphology and developmental time and position of origin in the two classes, the pedicle is not strictly homologous in the inarticulates and the articulates (Williams and Rowell, 1965); this conclusion is further supported here. 59. Mode of life: 0 = always solitary; 1 = colonial or aggregating (rarely solitary). [0.50,0,0]. Bryozoans are colonial, with interzooidal connections via funiculi (Carle and Ruppert, 1983). Pterobranchs are colonial or aggregating; some have inter-individual connections, others do not (Brusca and Brusca, 1990). Brachiopods, phoronids and sipunculids are all solitary organisms, but they are commonly gregarious and live in clusters. 60. Habitat: 0 = exclusively marine; 1 = some in fresh water. [l.OO, -, -1. Only certain bryozoans (the phylactolaemates) have successfully invaded freshwater habitats; all other taxa in this study are fully marine (Brusca and Brusca, 1990). MINERALIZATION

AND VALVE GROWTH

61. Mineralized skeleton: 0 = absent; 1 = calcium carbonate (low magnesium calcite); 2 = calcium phosphate (francolite). [0.67, 0.50, 0.331. Carbonate skeletons are widely (but not universally) considered to be primitive for metazoans, while phosphatic skeletons have evolved several times independently in brachiopods, chordates, annelids, molluscs and others. Craniaceans and the articulate brachiopods mineralize two valves of low magnesium calcite, while discinaceans and lingulaceans mineralize two valves of francolite (Lowenstam, 1961; Lowenstam and Weiner, 1989; Williams, 1990). Some, but not all, bryozoans mineralize zooecia of calcite or, less commonly, aragonite (Schopf and Manheim, 1967). Phoronids and pterobranchs lack mineralized skeletal elements (Hyman, 1959; Brusca and Brusca, 1990). One family of sipunculids (the Aspidosiphoniformes) mineralize granules or plates in their shields made of calcite (Lowenstam and Weiner, 1989)) not aragonite (Rice, 1969). Not surprisingly, shell proteins are intimately related to the nature of shell mineralization (Williams and Rowell, 1965; Jope, 1977, 1986; Tuross and Fisher, 1986). Thus, lingulacean and discinacean brachiopod valves have similar shell organic matrices and associated organic constituents: abundant organics and chitin (up to 40% ash-free dry weight), longchain (80K) proteins, with prolinecoding high. The five calcareous-shelled brachiopod groups have similar organic constituents, different from the phosphatic-shelled brachiopods: minimal organics and chitin (usually less than 5% ash-free dry weight), short-chain (50K) proteins, with praline-coding low, low alanine and n-end histidine. 62. Timing of initiation of shell formation: 0 = embryonic; 1 = larval; 2 = postlarval (post-settlement). [0.50, 0.50, 0.251. Sipunculids mineralize their plates post-settlement (Hyman, 1959), which is the primitive condition indicated by

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this study. Mineralization earlier in ontogeny is derived. Cyphonautes larvae, characteristic of some bryozoans, have bivalved chitinous shells (Zimmer and Woollacott, 1977; Stricker et al., 1988). Craniaceans (Nielsen, 1991) and articulate brachiopods (Pajaud, 1970; Reed, 1987; Snicker and Reed, 1985b,d; Williams, 1990) begin mineralizing valve protegulae following settlement on a substrate. However, Percival (1944) reports that shell formation begins minutes before mantle reversal in Wultonia (a terebratellid). Discinaceans and lingulaceans form valves during their planktotrophic larval stage (Yatsu, 1902; Chuang, 1977,199O; Watabe and Pan, 1984). 63. First-formed shell mineralized as: 0 = one valve (one nucleation site) that later folds and splits into two valves; 1 = two valves (two nucleation sites) present throughout ontogeny; 2 = two valves present only in larvae; valves absent in adult. [l.OO, -, - I. In craniacean, discinacean and articulate brachiopods, two discrete centers of mineralization form two discrete valves (Williams and Rowell, 1965; Stricker and Reed, 1985b,d; Nielsen, 1991). Both valves are dorsal, developmentally, in the craniaceans; the adult dorsal (brachial) valve forms first, followed by the ventral valve (Nielsen, 1991). Thecideaceans also mineralize the dorsal valve first, while the larval “pedicle” is still present; the ventral valve forms after the “pedicle” degenerates (Pajaud, 1970). Lingulaceans exhibit a curious developmental feature-one valve is mineralized as a circular (phosphatic) plate that folds along a diameter, breaks, and forms two separate valves that grow “away from” the broken edge (Yatsu, 1902; Hyman, 1959; Rowell, 1960; Nielsen, 1991). Chuang (1990) disputes this claim, however, implying that lingulaceans also have two centers of mineralization (the primitive condition). Cyphonautes larvae are bivalved, but the valves are lost post-settlement (Zimmer and Woollacott, 1977). 64. Growth of ventral valve: 0 = holoperipheral throughout ontogeny; 1 = hemiperipheral to holoperipheral (switches very early in ontogeny, at metamorphosis); 2 = hemiperipheral to holoperipheral (switches later in ontogeny, post-juvenile; = mixoperipheral); 3 = hemiperipheral throughout ontogeny. [ 1 .OO, 1.00, 1.001. The pattern of growth of the valves through ontogeny is complex. Three styles of growth [that concern where (in three dimensions) and how fast shell material is added to the valve] are common, and these growth styles can and do change as the animals grow (Thomson, 1927; Williams and Rowell, 1965; character states are coded by my interpretation of growth patterns). In holoperipheral growth, exhibited by craniaceans, shell material is added around the entire valve perimeter; growth vectors at the posterior and anterior margins of the valve are pointed in opposite directions. In hemiperipheral growth exhibited by the lingulaceans (mixoperipheral according to Thomson, 1927, but I disagree), shell material is added around only a portion of the perimeter (not posteriorly). True mixoperipheral growth is similar to holoperipheral, except that the valve in lateral profile appears “folded” to an acute angle, and the posterior sector of the valve increases in size anteriorly. The growth vectors at the posterior and anterior edges of the valve are pointed in the same general direction. Discinaceans and thecideaceans are largely holoperipheral, but their earliest valve growth is hemiperipheral; this appears to be the primitive state in this analysis. Rhynchonellide and terebratulide brachiopods are largely holoperipheral

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(mixoperipheral; accommodating a notch for the pedicle opening), and switch from hemiperipheral later in ontogeny than the thecideaceans or discinaceans. 65. Growth of dorsal valve: 0 = holoperipheral throughout ontogeny; 1 = hemiperipheral throughout ontogeny. [0.50,0,0]. The dorsal valve usually exhibits a different, and simpler, growth pattern than the ventral valve. Craniaceans and discinaceans are holoperipheral; lingulaceans and articulates are hemiperipheral SHELL

.%RUCl-URE

66. If calcitic, shell structure with nonfibrous primary layer and: 0 = persistent secondary fibrous layer; 1 = impersistent secondary fibrous layer. [ 1.00, 1.00, 1 .OO]. Patterns of similarity in shell structure have had a profound influence on the higher-level organization of the brachiopods (Williams 1956, 1968a,b, 1970, 1971, 1973, 1984, 1990; Williams and Rowell, 1965; Stricker and Reed, 1985b,d), particularly among fossil articulate brachiopods. All brachiopods have a thin, nonfibrous (crystalline) primary shell layer immediately under the periostracum. Rhynchonellides and terebratulides have a persistent secondary fibrous layer under the primary layer; most of the shell is composed of secondary fibrous shell material (the derived state of this character). The secondary layer is developed impersistently in the craniaceans (only in the dorsal valve) and thecideaceans. Thin primary and thick secondary layers under the periostracum is the standard succession of carbonate shell structures in extant brachiopods. 67. If calcitic, shell structure with: 0 = persistent (?secondary) laminar layer, 1 = tertiary prismatic layer often present. [l.OO, -, -1. Laminar layers are present in craniacean shell structure where they occupy the same position as the fibrous secondary shell layer in extant articulate brachiopods; laminar shell layers are more commonly developed in extinct articulate brachiopods (e.g. strophomenaceans; Brunton, 1972). Terebratulids often possess a tertiary layer of prismatic shell in addition to the secondary fibrous layer; these are present intermittently among extinct articulates (e.g. pentameraceans; Williams, 1990). 68. Shell structure: 0 = punctate (“canalicular”), extremely fine structures; 1 = punctate (“punctae”), large structures lacking distal brushes; 2 = punctate (“endopunctae”) , large structures with distal brushes; 3 = impunctate (without punctae of any kind); 4 = pseudopunctate. [l.OO, 1.00, 1.001. AI1 extant brachiopods except the rhynchonellides are punctate, possessing cylindrical perforations of the shell filled with caecae (mantle extensions). At least three distinct types of punctae are recognized; their homology is contested (Williams and Rowell, 1965; Cooper, 1969). The phosphatic-shelled inarticulates have extremely fine punctae (-60 pm wide; canaliculi) containing mere cytoplasmic strands. Craniaceans possess punctae that contain true caecae (~100 nm wide), but lack the distal brushes filled with microvilli that connect the caecae to the valve surface; the punctae commonly branch toward the shell exterior. Terebratulides and thecideaceans possess endopunctae (simple or branching), that have distal brushes (Gwen and Williams, 1969).

BRACHIOPOD

PHYLOGENY

Rhynchonellides lack punctae, which morphy. Stratigraphic polarity, based indicates that impunctate shells are rhynchonellides retain the primitive developing it independently.

191

is here represented as an autapoon the oldest fossil brachiopods, primitive for articulates and that impunctate condition, rather than

MISCELLANEOUSSKELETALCHARACTERS 69. Spicules (mesenchymal) in mantle (and body wall) and lophophore tissues: 0 = absent; 1 = uncommon (present in some taxa); 2 = common (present in most taxa). [0.50, 0.50, 0.251. Mesenchymal singlecrystal spicules form in the mantle tissue and lophophore of many species of terebratulide and thecideacean brachiopods (Williams and Rowell, 1965; Blochmann 1900), and provide additional structural support to the lophophore. They are absent in rhynchonellides and all inarticulate brachiopods, as well as the four outgroups. 70. Shell resorption: 0 = uncommon (or unknown); 1 = common (or ubiquitous). [0.50, 0.50, 0.251. The resorption of shell material after its deposition is a common phenomenon in all extant articulate brachiopods and in the discinaceans, where it has apparently evolved twice independently. Details of the biochemical mechanism of shell dissolution and reprecipitation are not known, but resorption clearly plays an important role in structuring shape change as size increases during growth (Jaanusson, 1971; Carlson, 1989). Shell resorption around the pedicle foramen during growth enables the opening to enlarge as the animal gets larger, teeth and sockets resorb during growth to maintain their interlocking fit, calcareous lophophore supports must resorb as the lophophore grows (Williams and Rowell, 1965; MacKinnon, 1974, 1991). Craniaceans and lingulaceans show no signs of resorption during growth; neither (apparently) do bryozoans. 71. Chitin: 0 = present (in shell, pedicle, cuticle, or outer body tube); 1 = absent (in shell, periostracum, and elsewhere). [0.33, 0, 01. Chitin is present primitively in the cuticle of sipunculids, the entire exoskeleton of certain bryozoans (ctenostomes and cheilostomes) and in the tubes (but not the body) of phoronids (Hyman, 1958, 1959; Brusca and Brusca, 1990). The shells and pedicle of both discinaceans and lingulaceans contain chitin; the articulate pedicle contains chitin but the periostracum generally lacks chitin, although a small amount is present in the periostracum of the rhynchonellides (Tavener-Smith and Williams, 1972). Chitin has not been found in either the shell or periostracum of the craniaceans nor the thecideaceans, which both lack pedicles. It is also absent from the coenecium of the pterobranch Rhabdophru (Hyman, 1958); its absence appears to be typical for the deuterostomes (Willmer, 1990). VALvE ARTICULATION 72. Valves: 0 = not in contact, and rotate only slightly about an obscure hinge axis; 1 = in contact, and rotate about a hinge axis located on valves. [l.OO, 1 .OO, 1 .OO]. Because the muscular system in all brachiopods is located in the

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posterior half of the animal, contraction of the muscles will effect some (if only very minor) rotation of the valves. Contraction of the umbonal muscle in lingulaceans and the paired posterior adductor muscles in craniaceans and discinaceans accomplish this slight rotation. In discinaceans and lingulaceans, the axis of rotation is located in the soft tissues themselves, since the valves are not in contact with one another. Craniaceans have an interesting nonarticulating “articulation”. According to Atkins and Rudwick (1962: 474), “when the shell [of Crania] opens, it does so by a rotation of the dorsal valve about an axis corresponding to the posterior side of the shell, where the valve edges remain in contact”. This observation is consistent with the fact, noted by Forey (1982), that the posterior margin of the dorsal valve of Crania is straight. In all the articulates, the valves rotate about a distinct hinge line where the valves are in contact with one another (Williams and Rowell, 1965). 73. Hinge line: 0 = strophic (straight; hinge axis colinear with hinge line); 1 = astrophic (curved; hinge axis intersects hinge line at only two points). [l.OO, -, -1. Rhynchonellides and terebratulides have astrophic hinge lines. Thecideaceans have strophic hinge lines; they appear to have retained this primitive state from their early Paleozoic ancestors. However, it is possible that thecideaceans developed strophic hinge lines independently; their late appearance in the fossil record has traditionally supported this interpretation (Williams and Rowell, 1965). 74. Pair of teeth and sockets: 0 = absent; [l = present and non-interlocking]; 2= present and interlocking. [l.OO, 1.00, 1.001. This is the character that names the two current classes of brachiopods. Inarticulate brachiopoids lack teeth and sockets as articulator-y structures; all articulates possess them. All Recent articulates have interlocking teeth and sockets; all articulates with noninterlocking hinge structures are extinct (Jaanusson, 1971; Carlson, 1989, 1992). Because none of the outgroups in this study possess two valves, they have no power to polarize character transformation here; the presence or absence of teeth and sockets are equally derived relative to the lack of two valves. SHELL

FORM

75. Adult size (in greatest dimension): 0 = all exceptionally small (less than 1 cm) ; 1 = all fairly small (from l-3 cm); 2 = most medium-sized (from 3-6 cm); 3 = some very large (more than 6 cm). [0.67,0.50,0.33]. Small adult size appears to be primitive, with valves becoming somewhat larger twice (lingulaceans and terebratulides), and exceptionally small once (thecideaceans) . 76. Adult valve outline, in lateral profile: 0 = biconvex; 1 = not biconvex. [0.50, 0.50, 0.251. Biconvexity has evolved twice independently in the lingulaceans (very weak) and the rhynchonellides and terebratulides (strong). 77. If valves biconvex: 0 = weak biconvexity (length ZDdepth); 1 = strong biconvexity (length > depth); 2 = very strong biconvexity (approaching spherical). [l.OO, -, -,]. Valve convexity appears to increase over time; more highly biconvex valves are derived. 78. Relative convexity of the two valves: 0 = equal or subequal; 1 = ventral valve more convex (usually along length axis) ; 2 = dorsal valve more convex (usually

BRACHIOPOD

79.

80.

81.

82.

83.

PHYLOGENY

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along width axis). [0.67, 0.50, 0.331. Equal valve convexity appears to be primitive; craniaceans and rhynchonellides have more highly convex dorsal valves, while the terebratulides (and, in a sense, thecideaceans) have more highly convex ventral valves. Relative shape, size, and growth patterns of the two valves: 0 = very similar to identical to one another; 1 = somewhat to quite different from one another; 2 = very different from one another. [l.OO, 1.00, 1.001. The ventral valve is primitively larger than the dorsal valve and somewhat different in shape. Valves of similar size and shape evolved in the lingulaceans and discinaceans, while valves of very different sizes and shapes evolved in the thecideaceans. If valves not biconvex: 0 = biconical; 1 = conical dorsal, planar ventral; 2 = tubular (extremely long ventral valve “area”), with lid. [ 1 .OO, -, -1. Each non-biconvex brachiopod shape is quite different from the others: conical (craniaceans) , biconical (discinaceans), tubular (thecideaceans) . Valve dimensions, dorsal view: 0 = length = width; 1 = length > width; 2 = length < width. [l.OO, -, -1. Valve length is primitively greater than valve width; discinaceans are nearly circular, craniaceans are wider than long. Coding sequence is consistent with ontogenetic polarity. Valve shape, dorsal view: 0 = circular; 1 = oval; 2 = semicircular; 3 = triangular. [0.75, 0, 01. Valve shape varies considerably; circular (or oval) valves appear to be more primitive than other shapes. Commissural margin: 0 = rectimarginate; 1 = fold (dorsal valve) and sulcus (ventral valve) present, but gentle; 2 = fold and sulcus present and strong. [l.OO, -, -1. The lack of a fold and sulcus is the primitive state; they have developed independently in some terebratellids and rhynchonellides, and were much more common among several groups of extinct brachiopods than they are today (Williams and Rowell, 1965).

SHELL ORNAMENT

84. Ornament on valve exterior: 0 = smooth; 1 = costate (radial ribs extending from umbo). [l.OO, -, -1. I n g eneral, smooth valve exteriors are primitive; ornament is derived. Ornament was commonly developed in extinct brachio pod groups (Williams and Rowell, 1965). 85. Costellae (secondary ribs intercalated between costae): 0 = absent (but costae present) ; 1 = present (multicostellate, fine and even). [ 1 .OO,-, -1. Among extant brachiopods, costellae are either absent (rhynchonellides) or present as multicostellae (terebratulides) . VENTRAL VALVE EXTERIOR AND INTERIOR

86. Shape of ventral valve beak: 0 = flat; 1 = rounded; 2 = pointed; 3 = absent. [l.OO, -, -1. Beaks are absent on the ventral valve in craniaceans. Pointed beaks are present in lingulaceans (and some rhynchonellides); rounded beaks are present in most articulates. 87. Length of ventral valve beak: 0 = extends barely beyond dorsal valve beak; 1 = extends well beyond dorsal valve beak. [l.OO, -, -1. Consistent with ventral valves typically longer than dorsal valves, the beak commonly extends well beyond the dorsal valve beak.

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88. Ventral valve cardinal area (area between the posterior valve margin and the point of attachment [pedicle opening or cementation scar]): 0 = absent entirely; 1 = present as pseudointerarea; [2 = present as interarea (in strophic valves)] ; 3 = present as palintrope (in astrophic valves). [ 1 .OO,-, -1. Cardinal areas in the inarticulates are generally absent or present as pseudointerareas (Williams and Rowell, 1965). They are present in the articulates as palintropes, or as pseudointerareas in thecideaceans. 89. Width of ventral valve cardinal area: 0 = very narrow to obsolete; 1 = narrow (to very narrow); 2 = wide (to narrow); 3 = exceptionally wide. [l.OO, 1.00, 1.001. Wider cardinal areas, present in articulates, are generally more derived; very narrow or obsolete cardinal margins are primitive and present in the inarticulates. 90. Orientation of ventral valve cardinal area: 0 = procline; 1 = catacline; 2 = apsacline (+/- 45”); 3 = orthocline; 4 = anacline (+/- 45”). [l.OO, -, -1. Apsacline ventral valve cardinal area orientation appears to be primitive in this study, but varies considerably among these taxa. 91. Shape of ventral valve cardinal area: 0 = straight; 1 = curved. [0.50,0,0]. Both discinaceans and thecideaceans have straight cardinal areas; other extant brachiopods have curved (concave) cardinal areas. 92. Ventral valve beak ridges: 0 = absent; 1 = poorly defined; 2 = well defined. [ 1.00, 1.00, 1.001. All articulates have welldefined beak ridges; both discinaceans and lingulaceans have poorly defined beak ridges, while craniaceans have none. The presence of beak ridges is generally derived relative to their absence. 93. Ventral valve umbo: 0 = open; 1 = solid. [ 1.00, -, -1. All extant brachiopods except the lingulaceans have open ventral valve umbos. 94. Median septum in ventral valve: 0 = absent; 1 = small, inconspicuous or poorly developed. [0.33, 0, 01. Discinaceans (and some lingulaceans; Glottidia) have a small, short median septum, as do terebratellids and thecideaceans (supporting the hemispondylium; Williams, 1973). The presence of a median septum is derived relative to its absence (in craniaceans, rhynchonellides and terebratulids) . 95. Dental plates (extend from under hinge teeth to ventral valve floor): 0 = absent; 1 = small and simple: 2 = large and exaggerated, but do not form spondylium (parallel or divergent). [l.OO, -, -1. The presence of dental plates in rhynchonellides (and some terebratellids) is derived relative to their absence in other articulates. PEDICLE OPENING

96. Well-defined chamber in ventral valve for reception of pedicle base: 0 = absent; 1 = present. [ 1.OO, 1.OO,1.001. A well-defined chamber is present in the rhynchonellides and terebratulides, and absent in the discinaceans and lingulaceans (and not applicable to apediculate brachiopods) . 97. Delthyrial/pedicle opening: 0 = present at some stage(s) in ontogeny; 1 = absent entirely. [ 1 .OO,-, -1. A “pedicle” opening is present at some stage in ontogeny in the ventral valve of all brachiopods except the craniaceans. Even thecideaceans, which lack pedicles as adults, very briefly possess an opening that is lost immediately after settlement on a substrate (Pajaud, 1970).

BRACHIOPOD PHYLOGENY

195

98. Delthyrial/pedicle opening present in ventral valve as: 0 = slit or foramen (supra-apical) in pseudodeltidium; 1 = fox-amen (apical or subapical) enclosed by deltidial “plates”; [2 = gap or notch (subapical), open delthyrium] ; 3 = groove running along “pseudointerarea”, no delthyrium, per se. [l.OO, 1.00, 1.001. Rhynchonellides and terebratulides possess either apical or subapical foramina; lingulaceans have a simple groove on the ventral surface of the “pseudointerarea”; discinaceans have a slit that is closed by a listrium in some taxa; thecideaceans possess a supra-apical foramen, if only very briefly in their ontogeny (the stratigraphically primitive state; Williams and Rowell, 1965). 99. Notothyrium (= delthyrium in dorsal valve): 0 = absent entirely; 1 = present and open; [2 = present and covered by chilidium]. [l.OO, -, -1. Only lingulaceans (and some terebratellids) possess a feature that could be considered a notothyrium; they are lacking in all other extant brachiopods. DORSALVALVEEXTERIOR AND INTERIOR 100. Shape of dorsal valve beak: 0 = flat (absent); 1 = rounded and indistinct; 2 = pointed and distinct. [0.33,0,0]. An indistinct and rounded dorsal valve beak is primitive, and present in discinaceans, terebratulides and thecideaceans. Craniaceans and lingulaceans have distinct dorsal beaks. 101. Width of dorsal valve cardinal area (“interarea/pseudointerarea”): 0 = absent entirely; 1 = narrow to obsolete; 2 = well developed and fairly wide. [l.OO, -, -1. Dorsal valve interareas are absent entirely in discinaceans and all articulates, except certain terebratellaceans. 102. Orientation of dorsal valve umbo and cardinal area (if present): 0 = central (procline); 1 = marginal (catacline); 2 = terminal (apsacline) . [ 1.00, 1.00, 1.001. The dorsal valve umbo is central (and primitive) in craniaceans and discinaceans, and terminal in lingulaceans; it is marginal with a catacline cardinal area (if present) in all the articulates. 103. Median septum in dorsal valve: 0 = absent; 1 = present, but weak and poorly developed; 2 = present, strong and well developed. [ 1.00, -, -1. The dorsal valve in most articulate and craniacean brachiopods possess a median septum; all discinaceans, some lingulaceans, and some terebratulids lack median septae. 104. Hinge plates: 0 = absent = 1 = present. [ 1.00, -, -1. Socket plates are present in all articulates except the thecideaceans; they support the socket ridges, which are present and welldeveloped in all articulate brachiopods. CAL~ARE~~~

LOPHOPHORE

SUPPORTS

105. Calcareous lophophore supports: 0 = absent entirely; 1 = present as projections from cardinalia; 2 = present as ridges on dorsal valve floor. [l.OO, 1.00, 1.OO]. Calcareous lophophore supports are absent primitively in all inarticulates and all four outgroups; they occur as projections of secondary shell material from the cardinalia in both rhynchonellides and terebratulides. Thecideaceans have raised ridges on the floor of the dorsal valve that serve to support the lophophore.

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106. If calcareous lophophore supports are present as projections from cardinalia: [0 = brachiophores (long, blade-like extensions from socket ridges)]; 1 = crura; 2 = loop. [LOO, -, -1. Both terebratulides have loops. Rhynchonellides have short, prong-like crura that support only the base of the lophophore near the mouth. 107. Loop: 0 = short, from cardinalia only; 1 = long, from cardinalia and dorsal median septum. [l.OO, -, -1. Terebratellid loops are long; terebratulid loops are short.

108. Relative size of the group of muscle scars in ventral valve: 0 = small, up to l/4 length of valve; 1 = medium, from l/4 to l/2; 2 = large, more than l/2 [0.67, 0.50, 0.X3]. The muscle scars in discinaceans and lingulaceans occupy a relatively large area on the valve; they are relatively small in rhynchonellides and thecideaceans. In all extant articulates, the ventral muscle field is located well forward of the umbonal chamber; it fills the umbonal chamber in many extinct articulates and is located in the posterior half of the valve in the inarticulates. 109. Muscle platforms: 0 = absent entirely; 1 = present in ventral valve only. [l.OO, -, -1. Muscle platforms are absent in all extant brachiopods except the thecideaceans, which possess hemispondylia. The adjustor muscles in terebratulides insert on a kind of platform (cardinal plate) in the posterior of the dorsal valve, but this is not a true platform. 110. Cardinal process: [0 = insignificant, low ridge] ; 1 = small lobe (unilobed, bilobed or trilobed) ; 2 = medium to large lobe; 3 = long, wide process. [l.OO, -, -1. Diductor muscles originate from the dorsal valve on cardinal processes in all extant articulates. Rhynchonellides have rather small cardinal processes; in terebratulides, they are medium-sized, while thecideaceans have long and wide (in comparison to their body size) cardinal processes. 111. Shape of mantle canal markings (primarily the vascula genitalia) : [0 = baculate (vascula lateralis simple, do not bifurcate); 1 = bifurcate (v.1. bifurcate); 2 = pinnate (v.l./vascula genitalia of radially disposed canals), 3 = saccate (v.g. pouch-like, no branches); 4 = lemniscate (v.g. sac-like, but with branches). [ 1.00, 1.00, 1.001. Mantle canal markings are present in the form of faint grooves or ridges on the interior surfaces of both valves of all extant and many extinct brachiopods (see character 24). Many different types have been named (Williams and Rowell, 1965); four types are present in extant taxa. Terebratulides have either pinnate or lemniscate markings, while rhynchonellides have either saccate or lemniscate markings. 112. Distribution of mantle canal markings (on dorsal valve only): [0 = equidistributate (v.g., v. myaria, and v. media all well developed and active); 1 = inequidistributate (v.g. saccate and contributes little to mantle circulation)]; 2 = apocopate (only 1 pair canals [v. media] present in addition to vascula genitalia); 3 = isolated (vascula media lacking entirely). [0.50, 0, 01. Craniaceans and lingulaceans have only vascula genitalia, and lack vascula media.

BFWXIOPOD

PHYLOGENY

Discinaceans, rhynchonellides and terebratulides are apocopate; ceans have not been characterized (Williams and Rowell, 1965).

197

thecidea-