Support for Interordinal Eutherian Relationships with an Emphasis on Primates and Their Archontan Relatives

MOLECULAR PHYLOGENETICS AND EVOLUTION

Vol. 5, No. 1, February pp. 78–88 1996 ARTICLE NO. 0007

Support for Interordinal Eutherian Relationships with an Emphasis on Primates and Their Archontan Relatives MARC W. ALLARD,* BARBARA E. MCNIFF,†

AND

MICHAEL M. MIYAMOTO‡

*Department of Biological Sciences, and †Department of Anthropology, George Washington University, Washington, DC 20052; and ‡Department of Zoology, University of Florida, Gainesville, Florida 32611 Received July 25, 1995; revised August 14, 1995

branches and potential sister groups (Novacek, 1986, 1994). The majority of the recent work on mammalian relationships has been conducted not to resolve those nodes regarded as uncertain, but rather to provide new hypotheses challenging prior ones of eutherian interordinal relationships. Thus, to characterize recent attempts at interordinal phylogeny reconstruction one might suggest the adage ‘‘two steps forward and one step back.’’ In this review, we will continue this trend of challenging the traditional mammalian superorders with current evidence. In particular we will examine the evidence for relationships within the superorder Archonta. This superorder traditionally includes the eutherian order Primates and its supposed relatives: tree shrews, Scandentia; bats, Chiroptera; and flying lemurs, Dermoptera. We will assess the support for other proposed eutherian superordinal relationships as well. We have attempted to survey approximately the past 5 years of systematic mammalian literature. This review is not intended to be an exhaustive treatment of all of the available evidence concerning eutherian relationships but rather only a synopsis of the most recent advances in the field. Due to the growing number of independent investigators conducting systematic mammalogy, the literature is vast and growing rapidly. Thus, we expect that some important material may be overlooked. In our treatment of the Eutheria, we have specifically focused on mammalian systematics issues that have been introduced recently into the literature. Our intention is not to fully examine all of the mammalian relationships which have been proposed, but only to examine the evidence presented recently which modifies or strengthens traditional groupings of the Mammalia. To simplify examination of the literature, we have provided many of the hypotheses and references for the primary data and analyses (Table 1). We have also attempted to categorize how well each phylogenetic hypotheses is supported. Any qualitative categorization of this sort is inherently subjective and we expect that some investigators will disagree with our choices. We have done this regardless, because it is

Current knowledge about mammalian interordinal relationships is growing rapidly; thus this contribution is an attempt to summarize the past 5 years of this literature. We have focused on the recent controversies in mammalian phylogenetics including hypotheses concerning the monophyly of Archonta, the diphyly of Chiroptera, and the polyphyly of Rodentia. All of these issues have been proposed recently, challenging these phylogenetic hypotheses. We have attempted to include all of the comprehensive analyses of eutherian mammal systematics with an emphasis on morphological and molecular data sets where discrete characters are listed so they could be compiled and used in support of interordinal relationships. Particular attention is given to determining which of the living eutherian orders is the closest relative to primates. In reviewing relationships among the mammals, we have focused on collating all of the available evidence so that one could know where each of the specific data sets is in support of the various relationships.  1996 Academic Press, Inc.

INTRODUCTION In recent years, interordinal mammalian systematics has undergone a period of renewed activity, with both morphological and molecular systematists providing new and exciting data for improving our understanding of the mammalian radiations (Novacek, 1992a; Honeycutt and Adkins, 1993). This activity has motivated a host of investigators both to reexamine the morphological evidence as well as to consider alternative weighting strategies for analyzing molecular data (Honeycutt and Adkins, 1993; Luckett and Hartenberger, 1993; Novacek, 1992a, 1993, 1994). This newly acquired data has energized the field and is helping to unravel the relationships among the mammalian radiation. All of the possible nodes necessary to resolve the 18 extant eutherian orders have had various hypotheses of relationships proposed, and many of these nodes are considered well supported with dichotomous 1055-7903/96 $18.00 Copyright  1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

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important to know whether a study strongly or weakly supports or refutes an hypothesis (Table 1). In the text, we have included lists of the characters (when available in the literature) which have been proposed to support or refute each clade or we have cited the studies where those characters can be found. For these reasons, we largely have limited this review to studies which have included character-based analyses where all of the primary data are available for reanalysis and reexamination. Our sampling of taxonomic problems and the detail which is covered under each hypothesis are somewhat unbalanced largely due to the historical treatment given to each of these groups, by the respective investigators, over the past 5 years. We have attempted to include the most important recent studies which have collected primary data or reviews of that literature. We have also limited our review to larger published data bases and taxonomic samples. One recent review of Archonta (Simmons, 1993) cites 10 published phylogenies since 1980. In her review of those studies, Simmons suggested that no viable consensus had been reached between morphological and molecular systematists, and she provided a discussion of possible methodological alternatives for exploration to resolve the eutherian phylogeny. In contrast, Novacek (1993, 1994, see Fig. 1) considered the morphological evidence supporting archontan relationships largely to be uncontested. He found that much of the recent contradictory morphological and molecular evidence is of either questionable homology, and thus of uncertain utility to the questions posed, or provides only weak character support to bear directly on interordinal relationships. While, admittedly, the character support for archontan monophyly was also weak, it was the most convincing data available (Novacek, 1993; Wible, 1993). Interest in Primates and their relatives has continued with numerous studies in the past 5 years, including reviews, symposia, and new morphological and molecular studies (Honeycutt and Adkins, 1993; MacPhee, TABLE 1 Evidence in Support of Phylogenetic Relationships among Eutherian Mammal Orders Which Have Been Challenged Recently in the Literature Hypothesis supported

Data

Analysis type Source(s)

Well-characterized relationships Rodentia monophyly AA* ML AA, DNA* P BC1 RNA D AA, DNA* NJ & P AA* ML, NJ & P M P Rodentia polyphyly AA* P COB NJ AGT1/ID D

1 2 3 4 5 6 7–10 11 12

TABLE 1—Continued Hypothesis supported Chiroptera monophyly**

Data

Analysis type Source(s)

IRBP NJ & P EG P COII ML & P AA, DNA, M* P M & COII P 12S & COI L, P M D vWF NJ & P Chiroptera polyphyly** M P AA, DNA, M* L, P Tethytheria monophyly M P (Proboscidea/Sirenia) COB NJ & P 12S L, P Basal Edentata M P Possible relationships Edentata/Pholidota M P Polyphyly Edentata/Pholidota M P Monophyly Lipotyphla monophyly M P Lipotyphla polyphyly Albumin/ID D Glires monophyly M P IRBP NJ & P AA, DNA* P Archonta polyphyly** COII P (Primates/Dermoptera/ IRBP NJ & P Chiroptera/Scandentia) EG P 12S P Archonta monophyly** M P Paenungulata monophyly M P (Tethytheria/Hyracoidea) 12S L, P Paenungulata polyphyly M P Artiodactyla polyphylya COB P & NJ AA, DNA* ML, NJ & P

13 14 15 16 17 18 19 36 20,21 22 23–25 26 27 23,28 28,37 23,24 29–31 32 6,23,24 13 2 2 13 14 33 17,23,24 23,24,25 27 34 26 35

Note: The first grouping listed is the relationship supported by the strongest evidence as opposed to an alternative hypothesis. Members of superorders (according to Novacek et al., 1988) are listed in parentheses. Data abbreviations used: *several different genes were sampled, see source; AA, amino acid; AGT1, alanine:glyoxylate aminotransferase 1; BC1 RNA, neural-specific small cytoplasmic RNA; COB, cytochrome b; COI/II: cytochrome c oxidase subunit I/II; DNA, nucleotide sequences; EG, ε-globin; ID, immunological distance; IRBP, interphotoreceptor retinoid binding protein; M, morphology; vWF, von Willebrand factor; 12S, 12S ribosomal RNA gene; a, Artiodactyla monophyly has been widely assumed and accepted as in the case of rodent monophyly. Analysis type abbreviations used: D, Descriptive: L, Lake’s invariants method; ML, maximum-likelihood; NJ, neighbor-joining; P, parsimony. **Further examination of some of the proposed relationships are presented in Fig. 1. Citation key: (1) Hasegawa et al. (1992); (2) Honeycutt and Adkins (1993); (3) Martignetti and Brosius (1993); (4) Frye and Hedges, (1995); (5) Cao et al. (1994); (6) Luckett and Hartenberger (1993); (7) Graur et al. (1991); (8) Li et al. (1992a); (9) Li et al. (1992b); (10) Graur et al. (1992); (11) Ma et al. (1993); (12) Noguchi et al. (1994); (13) Stanhope et al. (1992); (14) Bailey et al. (1992); (15) Adkins and Honeycutt (1993); (16) Simmons (1995); (17) Novacek (1994); (18) Mindell et al. (1991); (19) Thewissen and Babcock (1991); (20) Pettigrew (1986); (21) Pettigrew et al. (1989); (22) Pettigrew (1991a); (23) Novacek et al. (1988); (24) Novacek (1992b); (25) Shoshani (1993); (26) Irwin and Arnason (1994); (27) Springer and Kirsch (1993); (28) Rose and Emry (1993); (29) Butler (1988); (30) Novacek (1986); (31) MacPhee and Novacek (1993); (32) George and Sarich (1994); (33) Ammerman and Hillis (1992); (34) Fischer (1989); (35) Graur and Higgins (1994); (36) Porter et al. (1996); (37) Gaudin et al. (1996).

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1993; Goodman et al., 1994; Novacek, 1993, 1994; Schreiber et al., 1994; Simmons, 1995; Porter et al., 1996). Most of the recent molecular studies examining nucleotide sequence data have cast doubt on the validity of the superorder Archonta (Table 1, Fig. 1), with a considerable amount of evidence supporting the removal of bats from this assemblage and placing them into an unresolved polytomy of early mammalian lineages (see review in Goodman et al., 1994). Members of the Edentata and Pholidota, considered the earliest extant eutherian clade, are included in this polytomy as are the following orders: Primates, Dermoptera, Scandentia, Chiroptera, Macroscelidea, Lagomorpha, Rodentia, Carnivora, and Lipotyphla (Fig. 1). While several of these orders have well-characterized sister groups, many of these groups make up the most problematic portion of the Eutherian tree and their phylogenetic placement has been contested for some time by numerous studies (Table 1 and Fig. 1). Many of the recent studies have examined several of these problematic taxa. We will review these studies and assess the evidence for the placement of each of these orders. Marsupialia and Monotremata Any phylogenetic assessment of the Eutheria will require an appropriate outgroup to polarize the characters and to root the tree. Although Monotremata and Marsupialia are outgroups, it is becoming apparent to systematists that they are often problematic in analyses of molecular data mainly because of the increased amounts of homoplasy due to the higher levels of multiple substitutions occurring. Minimum ages of divergence for Monotremata to Eutheria and Marsupialia to Eutheria are roughly 190 and 120 million years ago, respectively (Savage and Russell, 1983). Many molecular comparisons at these levels of divergence have proven problematic (e.g., Irwin and Wilson, 1993; Stanhope et al., 1993; Honeycutt et al., 1995). The difficulty arises in finding a gene with a divergence profile that shows change to be linear over a long period of time and that remains relatively constant (Miyamotoand Boyle, 1989). A slowly evolving gene may not provide enough informative positions to produce resolution among the branches of the phylogenetic hypothesis (e.g., Eutheria), while a more rapidly evolving gene will begin to saturate with change for the most divergent comparisons (particularly problematic for outgroup to ingroup comparisons). With most of the Eutheria diverging at least 65–80 million years ago, any comparison to earlier lineages of mammals with more rapidly evolving genes (e.g., COII, COB, IRBP, Albumin) is bound to add significant levels of homoplasy to the data matrix and should thus be avoided. This is a predictable result as more distantly related taxa (e.g., Monotremata and Marsupialia) roughly double the range of divergence examined across genes. The alternative to examining rapidly evolving genes

is to sequence very large regions of highly conserved genes thus producing a large body of conservative and informative characters. Irwin and Wilson (1993) estimated that approximately 1000 codons would be necessary to resolve eutherian relationships based on estimates of cytochrome b gene sequences. No one has collected such a large body of conservative genetic data, so it remains to be seen whether this is an accurate prediction of the amount of data necessary to resolve these questions. More frequently, however, studies have examined rapidly evolving genes and extracted the more conservative substitutions (e.g., transversions) or regions (e.g., first and second codon position) from those data sets. In their study of the IRBP gene, Stanhope et al. (1992) found that adding the opossum outgroup (Marsupialia) increased homoplasy and destabilized the groupings in the most parsimonious tree, compared to an earlier analysis of the same data set with the opossum excluded. Strength of support for many of the internodes also decreased. To improve the phylogenetic resolution among the Eutheria, systematists should accomplish three goals: (1) find more conservative genes which are not saturated with change at these levels of divergence (Friedlander et al., 1994; Graybeal, 1994); (2) increase the number of taxonomic samples examined for interordinal comparisons, particularly for those groups that are thought to have older divergence times (Wheeler, 1992; Vrana, personal communication); and (3) sequence more representatives of the earliest eutherian lineages (e.g., Edentata). WELL-CHARACTERIZED RELATIONSHIPS Monophyly of Rodentia Before the monophyly of Rodentia was challenged with genetic data this phylogenetic hypothesis was widely assumed and accepted. Numerous molecular systematists have since presented evidence rejecting rodent monophyly (Li et al., 1992a,b; Graur et al., 1991, 1992; Graur, 1993; Ma et al., 1993; Noguchi et al., 1994; Table 1). Much of the above genetic evidence used to test rodent monophyly is relatively weak, thus highlighting the difficulties inherent in finding molecular evidence which supports any of the higher level mammalian relationships. While many genes and proteins have been used to test the question of rodent monophyly and the placement of the guinea pig, not enough detailed analyses have been conducted to determine which of these genetic systems are evolving at appropriate rates for accurate reconstruction of mammalian interordinal relationships. Furthermore, for many genetic systems it may be too early to assess their strength due to the limited taxonomic sampling. Various studies have discussed that when taxonomic sampling is limited the addition of other orders can dramat-

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FIG. 1. The following are selected phylogenetic hypotheses, concerning the sister group to Primates, derived from both morphological and molecular sources. (A) Transversion parsimony analysis of the mitochondrial gene cytochrome c oxidase subunit II (COII) by Adkins and Honeycutt (1993). Tree length 5 553 steps. (B) Parsimony analysis of tandemly aligned morphological and molecular characters. There are 49 morphological characters from Table 2 in Novacek (1994) and 258 informative molecular characters derived from transversions only from the mitochondrial gene cytochrome c oxidase subunit II (COII). (C) Parsimony analysis of a 257-bp fragment of the mitochondrial gene 12S rRNA by Ammerman and Hillis (1992). Tree length 5 293 steps. (D) Strict consensus tree of 20 orders of mammals (Novacek, 1992b). The four equally parsimonious trees used in this consensus were obtained from 88 morphological characters from fossil and recent data. The tree length 5 112. (E) Consensus tree obtained by analysis of interphotoreceptor retinoid binding protein (IRBP) (Stanhope et al., 1992). The segment used in this analysis is a highly conserved region of Exon 1. The aligned database was 1255 bp in length.

FIG. 1—Continued. (F) Most parsimonious cladogram from an analysis of the nuclear gene ε-globin by Bailey et al. (1992). The aligned genetic data matrix was 4200 bp in length. Tree length 5 3614 steps. (G) Transversion parsimony for tandem alignment of COII, IRBP, and ε-globin by Honeycutt and Adkins (1993). The published analysis was unrooted and is shown here rooted on Artiodactyla. Tree length 5 1839. (H) Strict consensus tree based on transversion parsimony of the mitochondrial 12S rRNA gene (Springer and Kirsch, 1993). The consensus is taken from 10 equally parsimonious trees with a length of 312 steps. (I) strict consensus tree of two trees from a 1293-bp data set from exon 28 of the von Willebrand factor gene (Porter et al., 1996). The two original trees only differ in their placement of a human pseudogene within the order Primates. We changed the terminal taxa listed on the published trees, when necessary, to indicate ordinal affiliation. The only exception is for the order Chiroptera, which includes two suborders, Megachiroptera and Microchiroptera. These are kept distinct when bat monophyly is discussed. Common names of frequently used representatives of the orders in the cladograms are: Amphibia (frog); Artiodactyla (cow); Aves (chicken); Carnivora (cat); Chiroptera (bat); Cetacea (whale); Dermoptera (flying lemur); Edentata (armadillo); Hyracoidea (hyrax); Insectivora (hedgehog); Lagomorpha (rabbit); Perissodactyla (horse); Primates (human); Pholidota (pangolin); Proboscidea (elephant); Rodentia (mouse); Scandentia (tree shrew); and Sirenia (sea cow). See original citations for detailed listings of taxa.

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ically alter the resulting tree topology (Allard et al., 1991; Novacek, 1992a; Honeycutt and Adkins, 1993; Luckett and Hartenberger, 1993; Simmons, 1994; Frye and Hedges, 1995; Porter et al., 1996). For example, the molecular evolutionary properties of AGT1 (alanine: glyoxylate aminotransferase 1) were examined in guinea pigs and considered to be ‘‘strikingly different from other rodents,’’ and partly using this evidence Noguchi et al. (1994) rejected rodent monophyly. However, this is not a valid reason to single out the guinea pig as a new mammalian order. Until a rigorous phylogenetic analysis is conducted, these unique character differences might best be interpreted as little more than autapomorphies of this unusual species. This strongly suggests that major classifications of mammals should only be considered after extensive taxonomic sampling is accomplished. In response to the hypotheses rejecting rodent monophyly, other investigators have conducted independent analyses. Most of these results have not supported the former claims, or the results of the data were inconclusive. This large body of evidence has been organized (both morphological and molecular) and these data mainly support rodent monophyly (Allard et al., 1991; Hasegawa et al., 1992; Honeycutt and Adkins, 1993; Martignetti and Brosius, 1993; Cao et al., 1994; Frye and Hedges, 1995; Porter et al., 1996) with the morphological evidence strongly supporting the monophyly of Rodentia (Luckett and Hartenberger, 1993, and the extensive references therein). Luckett and Hartenberger (1993) provide an extensive listing of the specific characters including: cranial, dental, postcranial, and fetal membrane evidence, as robust support for rodent monophyly. Based on the overwhelming evidence supporting rodent monophyly, including both the molecular and the strong morphological character support, one should consider the hypothesis of rodent monophyly as well established. The genetic systems (e.g., lipocortin, lipoprotein lipase, Graur et al., 1991; pancreatic polypeptide, α-lactalbumin, Frye and Hedges, 1995) which contradict this monophyletic grouping should be viewed with some skepticism. Those incongruent genetic systems should be closely examined to determine if they are inappropriate for assessing interordinal questions, whether due to taxonomic sampling or to gene tree problems, rate heterogeneity, gene duplication, or other such phenomena which might cause these paradoxical results between some of the molecular and all of the morphological evidence (Allard et al., 1991). Future analyses should focus on how these genetic processes confound the well-supported conclusion of rodent monophyly. Monophyly of Chiroptera Historically, Chiroptera has been considered monophyletic. A recent exception to this arrangement was a

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study in which the bat suborder Megachiroptera was found to be more closely related to Primates than to Microchiroptera (Pettigrew, 1986, 1991a,b; Pettigrew et al., 1989). This was first suggested on the basis of neural characters and was dubbed by some as the ‘‘flying primate hypothesis.’’ As with the hypotheses of rodent polyphyly, additional evidence and analysis (Table 1, both morphological and molecular) has discounted the bat diphyly hypothesis (Baker et al., 1991; Mindell et al., 1991; Simmons et al., 1991; Thewissen and Babcock, 1991; Bailey et al., 1992; Stanhope et al., 1992; Johnson and Kirsch, 1993; Luckett, 1993; Wible and Martin, 1993; Simmons, 1994; Porter et al., 1996). Simmons (1995) reviewed nine molecular studies and eight morphological studies in support of bat monophyly. Proboscidea and Sirenia (Tethytheria) The viability of Tethytheria (Proboscidea and Sirenia) and Paenungulata (Hydracoidea, Proboscidea, and Sirenia) have been debated in the literature (Fischer, 1989; Novacek, 1992a,b; Shoshani, 1993). Tethytheria has numerous morphological characters supporting this clade (e.g., Novacek et al. (1988) discussed six synapomorphies for the group; also see Shoshani (1993) and Table 1). In one morphological analysis, the node joining the Tethytheria required 46 extra Bremer steps before collapsing (Novacek, 1992b), suggesting that the data are internally consistent in support of this mammalian superordinal hypothesis. In contrast to the support of Tethytheria from morphology, the molecular data from the von Willebrand factor gene (vWF) supports the sister relationship between Sirenia and Hyracoidea (Porter et al., 1996). However, the authors note that to support Tethytheria it took only four extra steps from the most parsimonious solution. Morphological evidence did not support the Paenungulata as well, with only one additional step needed before collapsing the node, even though five morphological characters are described as supporting this clade (Novacek et al., 1988; Novacek, 1992b). Morphologists have continued to disagree on which characters to use for examining the hydracoids relationship to other mammalian orders (Fischer, 1989; Novacek, 1992a,b; Shoshani, 1993). The limited amount of molecular data tends to group these forms together (Springer and Kirsch, 1993; Irwin and Arnason, 1994; Porter et al., 1996). Edentata and Pholidota The most basal extant eutherian order is hypothesized to be Edentata (e.g., also referred to as Xenarthra, Zeller et al., 1993; Gaudin et al., 1996), which includes the sloths, anteaters, and armadillos. Pangolins (order Pholidota, genus Manis) have been considered a sistergroup to the Edentata based on morphology of the orbital wall, extensive sacral–innominate fusion, tooth and enamel morphology, and the presence of the rectus

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thoracicus muscle (Novacek et al., 1988; Novacek, 1993). If they are basal eutherian lineages, together the Edentata and Pholidota could make good outgroups for examining the relationships of other eutherians. However, it must be emphasized that several studies do not support early divergence of Pholidota or its sistergroup relationship to Edentata (e.g., Rose and Emry, 1993). For that matter, some recent morphological evidence supports a basal polytomy without clear support for a separate and early divergence of the Xenarthra (Gaudin et al., 1996). Until further evidence is obtained, only edentates should be used as the outgroup to the remaining eutherians. Little is known about the genetic variation of these forms, although ongoing work should provide some estimates soon (Pa¨a¨bo, personal communication). POSSIBLE RELATIONSHIPS Monophyly of Lipotyphla Lipotyphlans have long been considered critical taxa for understanding eutherian relationships (Novacek et al., 1988). The Lipotyphla (Mammalia; Eutheria; Insectivora) originated during the earliest radiation of placental mammals in the late Cretaceous. Today this group (shrews, moles, hedgehogs, and their relatives) is one of the most diverse mammalian orders. Yet little is known about the systematic placement of these taxa. Knowledge of lipotyphlan systematics is important because some of these taxa are hypothesized to show the most generalized, primitive eutherian morphotype, comparable to fossils from the late Cretaceous (65–75 million years ago; Walker et al., 1983; Yates, 1984; Novacek et al., 1985). Due to their numerous primitive features, this order has been considered as a useful taxonomic group for understanding the evolution of a wide range of characters (Eisenberg, 1981; MacPhee, 1981; Heaney and Morgan, 1982; Robbins and Setzer, 1985; Corbet, 1988). Recently, however, many of these features have been reexamined and the supposed primitiveness of the group questioned (MacPhee and Novacek, 1993). Before primitiveness of the lipotyphlans can be accepted or rejected, it is first necessary to determine whether they even form a monophyletic group. Divergence among lipotyphlan lineages is thought to have occurred concurrently with the mammalian ordinal radiations, although some investigators believe that a number of the lipotyphlans represent early and possibly independent lineages, as opposed to belonging to a monophyletic assemblage. Some molecular evidence (immunology) supports a polyphyletic Lipotyphla (George and Sarich, 1994; Table 1). In contrast, several morphological and molecular characters support the monophyly of the Lipotyphla (Butler, 1988; Novacek, 1986; MacPhee and Novacek, 1993), although generally, there are few characters in support of monophyly.

Even if lipotyphlan monophyly is accepted, the intraordinal relationships within this group are largely unresolved (MacPhee and Novacek, 1993) and their closest relative within the eutherian mammals is unknown. Hypotheses proposed include Tubulidentata and/or Carnivora as possible sister-groups to the Lipotyphla (Novacek, 1992b). New molecular evidence holds much promise for providing additional characters for a resolution within the Lipotyphla. As systematists begin to resolve intraordinal relationships within these early extant lineages (e.g., lipotyphlans), they should be able to improve the resolution among interordinal relationships of eutherians as well. The reason for this is because all of these groups arose at approximately the same time. Thus, some of the characters could be important for determining intraordinal and interordinal relationships. This is particularly true for molecular characters and also may be true for morphological ones. Those morphological characters affected may include hypothesized synapomorphies grouping the Archonta (Primates, Dermoptera, Scandentia, Chiroptera) such as a pendulous penis and a sustentacular facet of the astragalus; as well as characters associated with the superorder Glires (Lagomorpha and Rodentia) and their presumed sister order Macroscelidea (for a detailed list of the hypothesized morphological synapomorphies for the various groups see Novacek et al., 1988; Novacek, 1992b, 1994; MacPhee and Novacek, 1993). Rodentia and Lagomorpha (Glires) One of the clades supported by a large number of morphological characters consists of the superorder Glires (Rodentia and Lagomorpha). Characters supporting this clade include cranioskeletal and dental features associated with gnawing, as well as fetal membrane characters (Novacek et al., 1988; Novacek, 1992b; Luckett and Hartenberger, 1993). Some molecular evidence also supports the Glires clade including nuclear (Stanhope et al., 1992) and mitochondrial genes (Honeycutt and Adkins, 1993; Table 1 and Fig. 1). Chiroptera, Dermoptera, Primates, and Scandentia (Archonta) The superorder Archonta consists of four eutherian orders: Primates, Scandentia, Dermoptera, and Chiroptera. Although the relationships within this group have been disputed, several morphologists have placed Primates with Scandentia, and Dermoptera with Chiroptera (Thewissen and Babcock, 1991; Simmons, 1993; Novacek, 1994). New fossil evidence has challenged these relationships with several authors (Kay et al., 1990; Beard, 1990, 1993) suggesting that dermopterans are the sister taxon to primates. These analyses emphasized morphological characters from fossils of plesiadapiform families, Plesiadapidae and Paromomy-

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idae, taxa alleged to be primates and sharing numerous similarities to the extant dermopterans. When Novacek included Beard’s critical fossils (Paromomyidae) in a matrix combining many of the characters from the above studies, he produced a most parsimonious solution consisting of paromomyids grouping with dermopterans, and primates clustering next, to the exclusion of Scandentia and Chiroptera. Novacek (1994) suggested that this grouping might be due to the inclusion of an incomplete fossil (Paromomyidae) into the data matrix. Previously, when additional characters and taxa were analyzed (Novacek, 1992b, 1994), the Dermoptera grouped with the Chiroptera, and the sister taxon of Primates was Scandentia. Novacek further suggested that a complete data set is necessary to accurately resolve these problematic relationships and that these fossils are missing too many of the relevant characters. In addition, the interpretations of aspects of the fossils have been questioned by some (Wible, 1993; Wible and Martin, 1993). More serious challenges to Archonta relationships come from new molecular evidence which placed the Chiroptera as distant relatives to the other members of the superorder (Adkins and Honeycutt, 1991, 1993; Bailey et al., 1992; Stanhope et al., 1992, 1993; Honeycutt and Adkins, 1993; see Figs. 1A–1H). While molecular analyses support archontan polyphyly, they do not consistently support the same affinities among archontan members or with respect to Glires. Recent molecular systematic studies, incorporating a host of genetic evidence, have included both mitochondrial [12S ribosomal RNA (12S rRNA), cytochrome c oxidase subunits I (COI), and subunits II (COII)] and nuclear genes [interphotoreceptor retinoid binding protein (IRBP), von Willebrand factor (vWF), and ε-globin]. All of the molecular analyses show three results in common: (1) the support of chiropteran monophyly with a clear rejection of the ‘‘flying primate hypothesis’’; (2) the Chiroptera as distant relatives to the other orders; and (3) the rejection of a monophyletic Archonta with other orders (Rodentia, Lagomorpha, and/or Macroscelidea) as closer relatives to the remaining Archonta members, to the exclusion of bats (Bailey et al., 1992; Honeycutt and Adkins, 1993; Goodman et al., 1994). Taxa also were examined for a small fragment of 12S rRNA gene (Ammerman and Hillis, 1992; Fig 1C), although due to the small size of the gene fragment sequenced, few conclusions are supported clearly. One result from this mitochondrial gene fragment was that the monophyly of the Archonta was not supported, with the cow grouping with the other archontan representatives before bats did. COII sequences (Adkins and Honeycutt, 1993) supported a Dermoptera plus Scandentia clade separate from the Primates, based on a transversion parsimony analysis. These three orders were determined to be monophyletic and distinct from a separate monophyletic Chiroptera.

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When a combined total evidence, parsimony analysis, was conducted for the morphological characters and the conserved transversions of the COII molecular data set, a single tree was found which supported a topology similar to that determined from the morphological evidence alone (Novacek, 1994; Fig. 1B). The Dermoptera grouped with a monophyletic Chiroptera and the sister branch to this clade grouped Scandentia with Primates. The only other interordinal groupings that changed with inclusion of the COII data set was whether the Rodentia was placed basal to the Artiodactyla, according to morphology alone, or vice versa, according to the combined analysis. Novacek (1994) used this total evidence result in defending a monophyletic Archonta. He characterized the conflicting COII data as providing a weak signal that could be overridden by a smaller, compelling, and more informative morphological data matrix. His extended examination of character and taxonomic congruence will be a crucial strategy for improving resolution within the Mammalia. A larger COII data base including additional ordinal representatives (Adkins and Honeycutt, 1993) supported a sister group relationship of Primates to a (Dermoptera (Scandentia, Macroscelidea)) clade based on a transversion parsimony analysis (Fig. 1A). No comparable total evidence analysis of molecular and morphological data has been conducted for these extended data bases (Simmons, 1994). In fact, few molecular studies have included Macroscelidea sequences in their phylogenetic analyses, and often molecular and morphological analyses do not fully overlap on the taxa included in those studies. Nuclear genes also do not support a monophyletic Archonta, with either the orders Lagomorpha and/or Rodentia grouping within the superorder. The ε-globin gene did not support a monophyletic Archonta, with rabbit grouping within this hypothesized assemblage when the tree was rooted with a goat outgroup (Bailey et al., 1992; Fig. 1F). An unconstrained phylogenetic analysis using parsimony grouped Primates as a monophyletic assemblage, demonstrating that there is hierarchical structure in the ε-globin gene data. Furthermore, using the same characters and weighting strategy, an additional 52 character changes were required to support the hypothesis of Archonta monophyly [(Scandentia, Primates) (Dermoptera, Chiroptera)]. While the inclusion of Lagomorpha did result in a polyphyletic Archonta, this hypothesis of Lagomorpha within Archonta was relatively weak, requiring only two Bremer steps to collapse this node (Bailey et al., 1992; Honeycutt and Adkins, 1993). Clearly, additional analyses with an appropriate Edentata outgroup might provide further resolution for these taxa and an alternative sister group for the Scandentia (Fig. 1F), although see Gaudin et al.(1996) as to the utility of a xenarthran outgroup. The IRBP gene sequences also supported a polyphy-

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letic Archonta, with chiropterans as distant relatives to the other members of the superorder (Stanhope et al., 1992; Fig., 1E). IRBP is a single copy gene with a large conserved region in exon 1, making it a promising gene for interordinal comparisons. In the IRBP analysis, a monophyletic Glires (Rodentia and Lagomorpha) was more closely related to a Dermoptera plus Scandentia clade than were the Chiroptera or the Primates. Once again the molecular evidence did not support the hypothesis of a Volitantia clade (Dermoptera plus Chiroptera) or Archonta monophyly as the morphological evidence would predict (Table 1, Fig. 1). When a total evidence analysis of genetic data was conducted using COII, IRBP, and ε-globin sequences in tandem, the most parsimonious solution of an unrooted transversion analysis (as well as for an all characters analysis) supported chiropteran monophyly and a polyphyletic Archonta, with Lagomorpha being more closely related to the other archontans than were the Chiroptera. Numerous additional changes (67 additional steps for all characters analyzed from an initial tree length of 4527) had to be hypothesized to support Novacek’s phylogenetic arrangement (Honeycutt and Adkins, 1993; Fig. 1G). The hypothesis of archontan relationships directly affects the interpretation of mammalian character evolution with characters fitting onto the tree at specific nodes, making explicit statements about character homology. If one accepts the taxonomic relationships then one also will accept the statements of homology. If an alternative hypothesis is accepted then the placement of the characters on the tree may also change. If we accept the total genetic evidence hypothesis (Honeycutt and Adkins, 1993; Fig. 1) and interpret morphological characters (Novacek, 1992a) according to a genetic tree, then flight has only arisen once within the Chiroptera. Alternatively, the penis (character state 5 pendulous penis, Novacek, 1992b) has evolved once in the clade Primates, Scandentia, and Dermoptera, and independently in the chiropteran, suborder Megachiroptera. Further detailed analyses of these characters should reveal the nonhomologies among characters and thus the distinctiveness of their respective members. Characters associated with flight and brain neurology have been carefully scrutinized (Baker et al., 1991; Johnson and Kirsch, 1993), although no similar treatment has been recently attempted on the penis. Other characters which should be examined further include the characters supporting the sister relationship for Scandentia and the order Primates which are as follows: derived condition for a complete orbital bar, petrosal-derived osseous canals around intratympanic portions of facial nerve and stapedial artery, anterior carotid foramen in basisphenoid converted to a long tube, and tegmen tympani expanded anterolaterally to roof epitympanic recess (characters 3–6 in Novacek, 1994). Morphological features which are hypothesized ho-

mologies between the Dermoptera and Chiropteria include the following (Novacek, 1986): flattened ribs, elongation of forelimbs, patagium between digits of manus, distinct muscles in flight membranes, proximal and distal reduction in ulna, cochlea orientation, and subarcuate fossa greatly expanded (also see the list of 17 characters in Simmons, 1994). If Dermoptera is not considered the closest order to the Chiroptera then many of these character homologies must be reinterpreted. There is a lack of congruence between the various data sets in determining a sister order to Primates and in demonstrating the monophyly of Archonta. Novacek (1993, 1994) supports a sister relationship between Scandentia and Primates, and Archonta monophyly (Table 1). In contrast, the molecular data give alternative results for a sister clade to Primates. All of the molecular evidence is either weak or conflicting, and each of the following orders have been considered as possible sister groups, often with several of these clustered together: Rodentia, Lagomorpha, Scandentia, Dermoptera, Hydracoidea, Proboscidea, Sirenia, and Macroscelidea. Finally, none of the molecular data support Archonta monophyly. Artiodactyla and Cetacea Fossil evidence has long supported an Artiodactyla and Cetacea clade with each of these orders monophyletic. Recent molecular evidence has also supported the close association between these orders, although it does not indicate that the Artiodactyla are monophyletic (Graur and Higgins, 1994; Irwin and Arnason, 1994). These molecular data are unconvincing, however, because the genes examined are rapidly evolving with significant levels of homoplasy present and are poorly sampled. Molecular data must be gathered on many more taxa in both orders to test the monophyly of the Artiodactyla. We suspect that problems associated with this interordinal clade are similar to those that were found in the rodent monophyly conundrum. CONCLUSIONS It is evident that there is still much to be learned about mammalian relationships. Additional morphological and molecular evidence will need to be collected before a fully resolved eutherian phylogeny is produced. No single genetic or morphological system is going to be a panacea for this phylogenetic problem. Many of the data sets provide strong character support for a particular node while providing contradictory support for other nodes hypothesized by alternative data sets. Sorting through these complex phylogenetic signals has been thought provoking and we are beginning to see some clear patterns and unambiguous support. Recent mammalian systematic research has clearly supported several clades including monophyly of the orders Rodentia and Chiroptera. Superorders tend to be

SUPPORT FOR EUTHERIAN RELATIONSHIPS

more difficult to assess even with the most recent evidence mainly due to the conflicting signal present among the compared data sets. Tentative support is available for a basal Edentata, Glires, Paenungulata, and Archonta polyphyly. Of all of these tentative relationships a polyphyletic Archonta is the most unpredicted grouping and it has only come to light due to the recent efforts of mammalian systematists whose efforts show little sign of slowing down. ACKNOWLEDGMENTS We give a special thank you to the numerous people who have provided insightful comments on earlier drafts of our manuscript including: Ron Adkins, Brunella Bowditch, Jim Clark, Morris Goodman, Rodney Honeycutt, Diana Lipscomb, Nancy Simmons, John Wible, and the members of the systematics discussion group at the George Washington University, Department of Biological Sciences. This work was supported by a UFF grant to M.W.A. and by NSF funding (BSR-8857264) to M.M.M.

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