The phylogenetic relationships of argyrolagid marsupials

Zoological Journal of the Linnean Society (2001), 131: 481–496. With 5 figures doi:10.1006/zjls.2000.0272, available online at http://www.idealibrary.com on

The phylogenetic relationships of argyrolagid marsupials ´ NCHEZ-VILLAGRA MARCELO R. SA Lehrstuhl fu¨r Spezielle Zoologie, Universita¨t Tu¨bingen, Auf der Morgenstelle 28, D-72076 Tu¨bingen, Germany Received July 1999; accepted for publication February 2000

New material of the oldest known argyrolagid marsupial Proargyrolagus bolivianus from the late Oligocene of Bolivia is described. The new specimen preserves previously unknown aspects of the anterior dentition that solve the long-standing homology problem concerning the identity (i2) of the procumbent lower incisors in argyrolagids. This new anatomical information is incorporated into a morphology-based phylogenetic analysis of all extant marsupial families and Argyrolagidae, with the aim of testing the monophyly of Paucituberculata and evaluating the relationships among extant marsupial families. Eleven features support the monophyly of Paucituberculata, the following three unique among Marsupialia: small size of the paraconid, procumbent second lower incisor, and supraoccipital without distinct lambdoid crest resulting in globular form of braincase. Paucituberculata is the sister group of an Australian clade of marsupials that includes Dromiciops, but these results are not robust, as shown by sensitivity analyses. The foramen ovale surrounded completely by the alisphenoid supports the association of  2001 The Linnean Society of London Dromiciops with diprotodontians. ADDITIONAL KEYWORDS: phylogeny – anatomy – South America – Metatheria – Marsupialia – Argyrolagidae – Proargyrolagus – Caenolestidae – Dromiciops.

as marsupials. Others have raised the possibility of eutherian affinities (McKenna, 1980; Reig, 1981; Reig, Kirsch, & Marshall, 1987; Kirsch et al., 1991), or that argyrolagids represent a third extant group of therian mammals (Clemens, Richardson & Baverstock, 1989). Recently Sa´nchez-Villagra & Kay (1997) and Sa´nchezVillagra (1998) have argued for the marsupial affinities of argyrolagids after the description of previously unknown cranial anatomy of the oldest argyrolagid, Proargyrolagus bolivianus, from the late Oligocene of Bolivia (see also Sa´nchez-Villagra, Kay & Anaya-Daza, 2000). Two recent comprehensive treatments of marsupial systematics and taxonomy (Szalay, 1994; Kirsch, Lapointe & Springer, 1997) also include Argyrolagidae in this group. However, the relationships of argyrolagids among marsupials remain a matter of speculation, as not a single phylogenetic analysis of marsupials including this group has ever been conducted. The current prevailing opinion on argyrolagid relationships is that they are most closely related to the shrew-like opossums of South America, the caenolestids (Kirsch et al., 1997). Extant caenolestids are represented by just three genera and seven species

INTRODUCTION The Argyrolagidae is an extinct group of South American mammals convergent in locomotion and inferred diet with bipedal and granivorous desert rodents in its most derived species (Simpson, 1970), with no ecological counterparts in the extant South American fauna (Mares, 1993). The phylogenetic affinities of argyrolagids have been a matter of wild speculation for about a century, as reviewed by Simpson (1970: 2), who stated: ‘‘Something has been lacking in knowledge of animals that have been considered rodents, ruminant artiodactyls, lagomorphs, notoungulates, diprotodont marsupials, paucituberculate marsupials, and polyprotodont marsupials, each after sober consideration by a vertebrate morphologist.’’

Several authors besides Simpson (1970) have also discussed the affinities of argyrolagids. Most of them followed Ameghino (1897) in classifying argyrolagids

E-mail: [email protected] 0024–4082/01/040481+16 $35.00/0

481

 2001 The Linnean Society of London

482

´ NCHEZ-VILLAGRA M. R. SA

of small-sized insectivorous forms of restricted geographic distribution (Bublitz, 1987; Nowak, 1991; Redford & Eisenberg, 1992). In the past, however, caenolestids were much more diverse taxonomically and ecologically (Marshall, 1980; Bown & Fleagle, 1993). It has been well established that the procumbent front lower incisors (‘diprotodonty’) of Caenolestidae (‘pseudodiprotodonts’, Ride, 1962) is not homologous to that of the Australian Diprotodontia. Ameghino (1897) named ‘‘Paucituberculata’’ to include caenolestids and argyrolagids. This arrangement has been followed by several authors in the last 30 years (Ride, 1964; Kirsch, 1977a,b; Aplin & Archer, 1987; Marshall, 1987; Marshall, Case & Woodburne, 1990; Szalay, 1994; Kirsch et al., 1997). Of particular importance to support the hypothesis of paucituberculatan monophyly was the assumption that the procumbent lower incisors of argyrolagids and caenolestids are homologous. However, this was never demonstrated by complete fossil material of basal argyrolagid taxa, with a dental formula not as reduced as the Miocene-Pliocene forms revised by Simpson (1970). In this paper a snout of Proargyrolagus bolivianus that preserves aspects of the anterior dentition previously unknown is described, solving the homology problem concerning the identity of the procumbent lower incisors. This new anatomical information from this basal argyrolagid is incorporated into a phylogenetic analysis of all extant marsupial families and Argyrolagidae. The main goal of this analysis is to test the monophyly of Paucituberculata. Additionally, the relationships among extant marsupial families are considered. Since argyrolagids are an extinct group known only from osteological remains, only morphological features form part of this discussion. Springer, Kirsch & Case (1997) have compiled a data set of 102 anatomical characters (cranial, dental, postcranial, and soft tissue) for all extant marsupial families that synthesizes much of the anatomical information concerning marsupial systematics that has been discussed since the 1960s (e g. Ride, 1962; Archer, 1976, 1984; Kirsch & Archer, 1982; Szalay, 1982, 1994; Reig et al., 1987; Springer & Woodburne, 1989; Luckett, 1994). The data matrix used in this work is a modified and expanded version of that presented by Springer et al. (1997). Institutional abbreviations used are: Museo Nacional de Historia Natural, La Paz, Bolivia (MNHNBol-V), Field Museum of Natural History, Chicago (FMNH), and Smithsonian Institution, Washington DC (USNM). Dental terminology throughout the text follows Crompton (1971). Lower case font signifies lower teeth, while upper case refers to upper teeth. The term ‘Marsupialia’ is used as a node-based name (Hennig, 1983; de Queiroz & Gauthier, 1992) that

refers to the taxon stemming from the last common ancestor of extant marsupial species and all its descendants, a crown group. The taxon ‘Metatheria’ includes Marsupialia, and all therians that are more closely related to Marsupialia than to Eutheria, so it is a stem-based name (Rougier, Wible & Novacek, 1998).

SYSTEMATIC PALAEONTOLOGY SUPERCOHORT MARSUPIALIA ILLIGER, 1811 ORDER PAUCITUBERCULATA AMEGHINO, 1897 FAMILY ARGYROLAGIDAE AMEGHINO, 1904 GENUS PROARGYROLAGUS WOLFF, 1984 PROARGYROLAGUS BOLIVIANUS WOLFF, 1984 New material

MNHN-Bol-V-008925, the anterior region of a skull with incomplete attached lower jaws (Fig. 1). The zygomatic arch is broken at its root and the orbital region is not preserved. Age and provenance

The specimen comes from the Salla Beds, formed as an alluvial fill of a basin cut into deformed Palaeozoic strata at the edge of the eastern Andean Cordillera of northern Bolivia (McBride et al., 1987; Sempere et al., 1990). The Salla Beds contain a rich mammalian Deseadan fauna (Hoffstetter, 1968). The Proargyrolagus specimen described here comes from the Branisella level at Tapial Pampa (Villarroel & Marshall, 1982). This level is approximately 25.8 Ma (late Oligocene) following Kay et al. (1998), who reported new Ar39/Ar40 dates and revised all previous date estimates for this locality. Description

The following diagnostic features of the monospecific genus Proargyrolagus (Wolff, 1984; Sa´nchez-Villagra & Kay, 1997) are present in MNHN-Bol-V-008925: the posterior end of each nasal projects posteriorly in its lateral portion (cf. Sa´nchez-Villagra & Kay, 1997, fig. 3); a large infraorbital foramen situated above the second premolar; a well-developed antorbital fossa craniad from the infraorbital foramen; a shallow mandibular ramus; a large mental foramen located below the last premolar; and the bilobed molars, with vertical grooves both labially and lingually, show the diagnostic proportions between lobes described by Sa´nchez-Villagra & Kay (1997). What is here named a posterior projection in the lateral portion of the nasals in Proargyrolagus, was described by Rougier et al. (1998) as a medial internasal process of frontals (their character 84). Rougier et al. (1998) listed absence of this feature as diagnostic of a

ARGYROLAGIDAE AND MARSUPIAL PHYLOGENY

483

Figure 1. Stereopairs of the right lateral view (A) and detail (B) of Proargyrolagus bolivianus MNHN-Bol-V-008925. Maximum preserved dorsal length=17.5 mm.

clade including South American and Australian metatherians. So the condition of Proargyrolagus is a plesiomorphic retention or a reversal to the groundplan metatherian condition. MNHN-Bol-V-008925 shows unequivocally that there is a very narrow contact between the premaxilla and the frontal that excludes a maxillary-nasal contact, as was suggested for Proargyrolagus with uncertainty by Sa´nchez-Villagra & Kay (1997). On the right dentary the large mental foramen is followed posteriorly by a much smaller extra foramen, absent on the left jaw. In the specimen described by Sa´nchez-Villagra & Kay (1997), MNHN-Bol-V-003454, there are two of those extra mental foramina. MNHN-Bol-V-008925 shows that the number of front teeth as reconstructed by Sa´nchez-Villagra & Kay (1997, fig. 2) is correct. Three upper incisors and one alveolus (I4) are present in the premaxilla. Two premolars are preserved anterior to the four upper molars. In between the four incisors and the two preserved

premolars are two alveoli. The upper dental formula is interpreted as 4.1.3.4. The mandibles preserve the root of a large procumbent incisor and two small empty alveoli anterior to three ante-molar teeth. Four molars are preserved. The lower dental formula is interpreted to be 3.1.2.4. The identity of the preserved teeth cannot be established with certainty (as is the case with many marsupial living taxa) given the absence of histological evidence from early ontogenetic stages. However, parsimony can be used to propose hypotheses of character homology (Lee, 1998). No known marsupial lacks a canine while possessing supernumerary upper and/ or lower incisors (Marshall et al., 1990). This and morphological considerations lead to the proposition that Proargyrolagus had a canine. If, as suggested by Luckett (1993, and references therein), the primitive dental formula of marsupials included four lower incisors, and if the lower dental formula of Proargyrolagus is 3.1.2.4, then it is parsimonious to

484

´ NCHEZ-VILLAGRA M. R. SA

hypothesize that the procumbent incisor of Proargyrolagus is i2, as in caenolestids. This view seems parsimonious given other interpretations concerning incisor loss from the metatherian Grundplan condition in several other marsupial taxa (Ride, 1962; Murray, Wells & Plane, 1987).

METHODS PARSIMONY ANALYSIS

A parsimony analysis was conducted of 107 characters, 269 character states, in 17 extant marsupial families and Argyrolagidae, as well as a hypothetical ancestor, using the program PAUP∗ version 4.0b2 (Swofford, 1999). The Appendix presents the character matrix, which is mostly based on that of Springer et al. (1997). Several characters and character states were revised or eliminated, and five characters were added. The monophyly of the families assumed in the analysis has been supported by numerous molecular and morphological studies of different kinds (Aplin & Archer, 1987; Luckett, 1994; Springer, Westerman & Kirsch, 1994; Springer et al., 1997; Kirsch et al., 1997). Museum work in institutions listed in the Acknowledgments was carried out to revise the data matrix and code the new characters. The coding of cranio-dental characters of argyrolagids is based mostly on published descriptions (Wolff, 1984; Sa´nchez-Villagra & Kay, 1997) and original observations of Proargyrolagus bolivianus; that of postcranial characters follows the descriptions of Simpson (1970) and Szalay (1994) of Argyrolagus. Diagnosis for the other terminal taxa (families) incorporated, where possible, data on inferred ancestral conditions based on both fossil and extant members. Information on basal metatherian taxa (Muizon, 1998; Rougier et al., 1998) was incorporated in the codification of the hypothetical ancestor. Justification for this methodological procedure is provided by Wa¨gele (1994; see also Meacham, 1984). Other fossil terminal taxa were not incorporated in the analysis, since they were either poorly known, or not directly relevant for the problem at hand, namely, testing the monophyly of Paucituberculata. Future studies could expand the taxonomic sampling of this analysis. The multistate characters from Springer et al. (1997) were treated as ordered (O) or unordered (U) (Swofford & Maddison, 1992) following the original designations of these authors. All the new characters in the matrix are unordered. The size of the data matrix precluded the use of exact searching techniques. Thus, searches on PAUP∗ were heuristic, using TBR (tree bisection-reconnection), branch-swapping and 500 random-addition replicates (see Maddison, 1991). The TBR procedure is the most effective algorithm to find the

most parsimonious tree in a heuristic search (see Swofford, 1993: 36). Bootstrap (Felsenstein, 1985; Sanderson, 1995) and branch support were used (Bremer, 1988, 1994) as measures of confidence. Bootstrap values were calculated based on 100 replications of a heuristic search using TBR. Branch support indices reported here are only approximations, as they must be calculated heuristically due to the large size of the data matrix. Specifically, indices were calculated by configuring PAUP∗ to retain trees within 5 steps of the MPT, and subsequently filtering out strict consensus trees at intervals of 1 step. In order to deal with equally most-parsimonious trees (MPT), a strict consensus of them is presented. Additionally, a modified version of the method outlined by Carpenter (1988, see also Goloboff, 1998) was used, based on the a posteriori successive approximation approach of Farris (1969). Character weight was assigned based on the rescaled consistency indices (or ‘RC’, Farris, 1989), using a base weight of 100, that resulted from the initial, equally-weighted analysis. Maximum values of the RC were used. This approach constitutes a process of “checking, correcting, and rechecking” (Hennig, 1968; Carpenter, 1988) within the context of the same analysis. SENSITIVITY ANALYSIS

Several searches besides the one described above were conducted, in order to examine the robusticity of the results concerning argyrolagid relationships. As discussed by Asher (1999), there is a variety of parameters in parsimony analysis that require some a priori treatment by the investigator. Wheeler (1995) outlined a technique called ‘sensitivity analysis’ that varied parameters and iteratively re-ran data analyses, allowing an assessment of the ‘sensitivity’ of particular clades to changes in the assumptions. Asher (1999) presented a clear application of this technique and a discussion of some parameters of interest (see also Simmons, 1993; Ross, Williams & Kay, 1998). A modified version of his approach is followed here. The following variable assumptions were used. (a) Missing data. In the original analysis, some of the 107 characters showed a relatively high percentage of missing data, condition a1. In additional analyses (condition a2), characters for which 20% or more of the data were missing were excluded (see Appendix), an arbitrarily chosen limit. The total number of characters in this case was 82. (b) Character ordering. In the main analysis, some characters were treated as ordered and some as unordered, condition b1 (see above). Wilkinson (1992)

ARGYROLAGIDAE AND MARSUPIAL PHYLOGENY

recommended the examination of the effects of both ordered and unordered hypotheses of character-state change on resulting topologies (see Asher, 1999 for a discussion). In additional analyses, all characters were treated as unordered, condition b2.

(c) Equal weight for multistate characters. In the main analysis, Springer et al. (1997) was followed in that every evolutionary transformation across all character states is given equal weight, condition c1. In this case, multistate characters have a larger weight in the analysis, since they serve to atomize the observed variation into more categories. In a second analysis, each character was weighted equally, condition c2. Thus multistate characters are given equal weight as binary characters. In this case, transformations between character states in a multistate character have a smaller weight than those in a binary character. In other words, the multistate characters are scaled in such a way that individual steps in a morphocline count for proportionally less as character states are added (Maddison & Maddison, 1992: 197–199; see Kay & Williams, 1994: 388). Eight different analyses were perfomed, each a different combination of assumptions: a1b1c1 (analysis on which the main discussion is based); a1b1c2; a1b2c1; a1b2c2; a2b1c1; a2b1c2; a2b2c1; and a2b2c2. A strict consensus tree was found in the cases in which more than one MPT was found (after a heuristic search, with TBR and 500 replicates).

DESCRIPTION OF CHARACTERS

A list of the first 102 characters used in the phylogenetic analysis can be found in Springer et al. (1997). One of them was modified (33), and others require an explanation or clarification (10, 39, 57, 76, 79, 83, 84).

Revised characters from Springer et al. (1997)

Character 10. “Metaconule: 0=absent or not-well developed; 1=well-developed or enlarged”. Comment: According to Sa´nchez-Villagra & Kay (1996), what Springer et al. (1997) identified as the ‘metaconule’ in diprotodontians (following Tedford & Woodburne, 1987) is actually the hypocone, based on topographical and functional considerations. The hypocone is present in caenolestids (pers. obs.), and it is secondarily reduced in many species of peramelinans (Groves & Flannery, 1990). Tedford & Woodburne (1998) responded to the comments of Sa´nchez-Villagra & Kay (1996), and maintain that the distolingual cusp of diprotodontians is a metaconule. The analysis was run twice. The first time following the original character definition (Character 10 of the Appendix) and

485

coding of Springer et al. (1997). The second time the character was defined as follows: Character 10B: Hypocone (O): 0=absent or not-well developed; 1=well-developed or enlarged. Character 33. “Procumbent lower i2: 0=no; 1=yes”. Modified: “Procumbent lower i3: 0=no; 1=yes”. Comment: What Springer et al. (1997) called i2, is called here i3 (see Murray et al., 1987). The ‘pseudodiprotodont’ tooth of caenolestids is hypothesized to be i2 (Ride, 1962; Kirsch et al., 1997), as in argyrolagids (see character 103). Character 39. “Upper C (O): 0=caniniform; 1=reduced; 2=absent”. Comment: Even though this tooth is not fully preserved in any specimen of Proargyrolagus so far described, based on the alveolus of this tooth in MNHN-BolV-008925, it is clear that this tooth was ‘reduced’. Obviously the term ‘reduced’ implies small size in comparison to what is assumed to be the outgroup, an assumption well substantiated given canine form within Metatheria and in the nearest relatives of this clade (Rougier et al., 1998). Character 57. “Anterior extent of lacrimal (O): 0= within the orbit; 1=just behind the orbit; 2=onto the rostrum”. Comment: The coding for argyrolagids is based on Hondalagus, since the region anterior to the orbit is not preserved in Proargyrolagus. As mentioned by Sa´nchez-Villagra et al. (2000), in Hondalagus altiplanensis, the lacrimal bone is seen outside the orbit. Character 76. “Ossicular axis (O): 0=[20 degrees; 1= 10 to 20 degrees; 2=<10 degrees”. Comment: The codification of this trait follows the data presented by Segall (1969a, 1969b) about the ear ossicles of marsupials. Character 79. “Stapedial ratio: 0=<1.5; 1=>1.5”. Comment: The stapedial ratio is the length/width of the stapedial footplate, following Segall (1970). Character 83. “Calcaneo-cuboid joint pattern (O): 0= ovoid; 1=triple-faceted, with CaCum [medial calcaneocuboid] facet”. Modified: Calcaneo-cuboid joint pattern (O): 0=ovoid; 1=double-faceted calcaneocuboidal joint pattern; 2= triple-faceted, with neomorph CaCum facet. Comment: The coding for this character presented in the original matrix by Springer et al. (1997) is correct, but the explanation for what the states represent is not.

486

´ NCHEZ-VILLAGRA M. R. SA

The corrected information has been kindly provided by J. A. W. Kirsch (pers. comm., 1998). Character 84. “Secondary CaAd [calcaneoastragalar] facet (O): 0=absent; 1=present and continuous with AN [astragalonavicular] facet”. Comment: See Szalay (1994: 224) for description of the condition in Argyrolagus scagliai and in an undescribed argyrolagid from the Colhuehuapian. New characters

Character 103. Procumbent i2 (i1 of Springer et al., 1997): 0=no; 1=yes. Character 104. Supraoccipitals without distinct lambdoid crest, resulting in globular form of braincase (Marshall et al., 1990): 0=no; 1=yes. Character 105. Location of the foramen ovale (U): 0= alisphenoid/petrosal; 1=just alisphenoid; 2=alisphenoid/squamosal. Comment: Observations on the location of the FO in marsupials are abundant in the literature (e.g. Reig et al., 1987; Marshall & Muizon, 1995), and this trait has been previously used in phylogenetic analyses (Marshall, 1977a; Archer, 1982; Kirsch & Archer, 1982). Two recent papers have reviewed literature and presented new data on FO location in several marsupials and eutherians (Gaudin et al., 1996; Wroe, 1997). Sa´nchez-Villagra (1998) presented a review of the condition at the genus level for marsupials, providing a discussion of variability at different taxonomic levels and examples from different museum specimens. The alisphenoid/petrosal location of the foramen ovale is considered plesiomorphic for didelphids (Marshall & Muizon, 1995; contra Marshall, 1977a), caenolestids (Sa´nchez-Villagra, 1998), and peramelinans (Muirhead, 1994 cited by Wroe, 1997). All 14 specimens in six species of peramelinans examined have an alisphenoid FO. But in contrast to this observation, Muirhead (1994, cited in Wroe, 1997) concluded that an alisphenoid/petrosal FO is plesiomorphic for peramelinans, based on the study of Oligocene and Miocene bandicoots. In Dromiciops the FO is enclosed by the alisphenoid (Wroe, 1997). It was not possible to establish with certainty the location of the FO in specimens of Tarsipes and Burramyidae. Character 106. Position of the carotid foramen: 0=in the basisphenoid; 1=in the basisphenoid-basioccipital suture. Comment: Sa´nchez-Villagra (1998) presented a detailed list of the position of the carotid foramen (CF) in marsupials. In most marsupials the CF is situated

in the basisphenoid (e.g. Chironectes minimus, USNM296200), the condition characteristic of didelphids and perhaps plesiomorphic for Marsupialia (Jollie, 1968: 247). Some diprotodontians have the CF in the border of the suture of the basisphenoid and the basioccipital. This is the case for all macropodoids, with the exception of Potorous tridactylus (USNM154082). Acrobates was first reported by Wincza (1896) and later by de Beer (1937) to be unique among marsupials in having the carotid foramen not perforating the basisphenoid but rather positioned lateral to it, between the petrosal and alisphenoid (as in some Tachyglossus and several multituberculates, Wible, 1986: 317). Aplin (1990: 5–54), on the basis of the study of sectioned material, instead proposed that the position of the CF in Acrobates is between the basisphenoid and basioccipital. Character 107. Transverse canal foramen location: 0= absent; 1=just anterior and lateral to the carotid foramen; 2=numerous foramina in pterygoid fossa. Comment: Most marsupials have a foramen anterior to the CF that transmits an extracranial vein, or a pterygoid plexus, that communicates with the cavernous sinus. In some species this bilateral vein communicates also transversely with its antimere. Following Archer (1976: 223) this vein is called here the ‘transverse canal’ (TC), and its opening the ‘transverse canal foramen’ (TCF). The TCF was first named ‘‘transverse canal’’ by Gregory (1910: 223), and described as ‘‘a prominent foramen or canal which tunnels the floor of the basisphenoid transversely’’. Gregory (1910) cited Wortman (1901) as the first to point out the significance of the TCF. Wortman (1901: 130) identified the TCF in Didelphis as a small foramen anterior to the foramen ovale that transmits a vein to the cranial cavity. The TCF varies in its position, number, and endocranial configuration. This variation has not been thoroughly documented or discussed, except for a handful of taxa. The potential of the TCF as a source of phylogenetic information has often been overlooked in treatments of marsupial systematics (but see Marshall, 1977a; Archer, 1982; Kirsch & Archer, 1982). The TCF is mentioned in descriptions of fossil metatherians (Marshall, 1977a, 1977b; Aplin, 1987; Murray et al., 1987; Archer, Hand & Godthelp, 1988; Marshall & Muizon, 1995; Muizon, 1994, 1998; Rougier et al., 1998). Marshall (1977a), Archer (1982), and Kirsch & Archer (1982) coded the absence/presence of a TCF in many marsupial taxa in their cladistic analyses. Archer (1976) presented information on the TCF and associated veins in some didelphids and dasyurids, and Aplin (1990) did the same for some diprotodontians. Archer (1981) examined the variation in the size of the TCF in species of Sminthopsis, the

ARGYROLAGIDAE AND MARSUPIAL PHYLOGENY

only detailed consideration of this feature in a study of a marsupial genus or species. Sa´nchez-Villagra (1998) presented a detailed review and survey of transverse canal foramen diversity among extant marsupials, which is followed to code this character here. Rougier et al. (1998) recorded absence/presence of this feature in a suite of fossil and extant metatherians and their closest relatives. The TCF is absent in some marsupial species, and the endocranial configuration of the transverse canal (unknown in argyrolagids) is variable among marsupials (Sa´nchez-Villagra, 1998). Some specimens of Dromiciops gliroides show a TCF (FMNH50072unnumberedA-unnumberedB), but some do not (AMNH92147) so character 107 is coded as polymorphic for this species (Rougier et al., 1998 code the TCF as absent in Dromiciops). There are reports of a TCF in some eutherians (reviewed in Sa´nchez-Villagra, 1998). This feature is not present in the Late Cretaceous species from Asia, Asioryctes, Barunlestes, Kennalestes, and Zalambdalestes (Marshall & Muizon, 1995, and references therein; Rougier et al., 1998). Ocurrence of the TCF is reported for species quite removed from the eutherian root, making the assumption of homology with the marsupial condition unparsimonious.

RESULTS AND DISCUSSION The heuristic search resulted in six equally mostparsimonious trees (MPT) of length (TL) 381 steps, consistency index (CI)=0.42, and rescaled consistency index (RC)=0.24. Figure 2 is a strict consensus of these trees; bootstrap values are reported for nodes that appear in at least half of the replicates. Figure 3 is the MPT resulting from a posteriori weighting based on the character RC values of the first search. Only one run was necessary to find a fully resolved tree. SUPPORT FOR THE MONOPHYLY OF PAUCITUBERCULATA

The strict consensus of MPTs shows a monophyletic Paucituberculata, with a 95% bootstrap value (Figs 2, 3). Concerning the sensitivity analysis, the results about argyrolagid relationships are very clear. In all cases the monophyly of Paucituberculata is supported. Additionally, the analysis with the alternative definition and coding of character 10 also showed the same result. The following shared-derived features support the monophyly of Paucituberculata (see Springer et al., 1997 for alternative character states): (1) Rectangular upper molar shape (5–1). (2) Location of the paracone and metacone in the buccal margin (6–2).

487

(3) Paracone and metacone of equal size (7–1). (4) Approximately 90 degrees angle between protoconal cristae (9–1). (5) Small paraconid (15–1). (6) Entoconid at posterolingual corner of the tooth (21–1). (7) Hypoconulid near posterolingual corner of tooth (22–1). (8) Size of I3
MARSUPIAL INTERORDINAL RELATIONSHIPS AND PAUCITUBERCULATAN AFFINITIES

Current classifications distribute living marsupials among seven orders, and additional extinct orders are recognized (Aplin & Archer, 1987; Marshall et al., 1990; Pascual, Goin & Carlini, 1994; Kirsch et al., 1997). In this work, as in many others of recent years, the monophyly of all polyfamilial orders has been corroborated. However, in the strict consensus of the six MPT of the first run, Myrmecobiidae and Dasyuridae (Order Dasyuromorpha) do not form a monophyletic group. This must be an artifact, since there is overwhelming support for the monophyly of this order (Kirsch et al., 1997; Wroe, 1997). The parsimony analysis of their original morphological data set by Springer et al. (1997) suggested that: (1) Dromiciops is the sister-taxon of diprotodontians, and peramelinans are the sister-group to them; (2) there is no evidence for allying caenolestoids and didelphimorphs, and (3) a dasyuroid+Notoryctes clade constitutes the sister group to all other marsupials. The bootstrap support for most clades in the MPT of Springer et al. (1997) was under 50%, as with the strict consensus reported in Figure 2 of the present paper. The parsimony analysis of a modified matrix that includes Argyrolagidae (Figs 2, 3) results in some deviations from the results of Springer et al. (1997). A departure from the result of Springer et al. (1997) analysis, is that Didelphidae is the most basal taxon in the MPT (Figs 2, 3). In the original analysis of Springer et al. (1997), it was Dasyuromorpha. The analyses of Retief et al. (1995) and Springer et al. (1994, 1998) of molecular data also placed didelphids close or at the base of the marsupial tree. In contrast to the original morphological analysis of Springer et al. (1997), Australasian orders plus Dromiciops form

488

´ NCHEZ-VILLAGRA M. R. SA Didelphidae Argyrolagidae 95% Caenolestidae

3

Dasyuridae Myrmecobiidae Peramelidae 85% 4+

Thylacomyidae Notoryctidae Microbiotheriidae Pseudocheiridae

Phalangeridae Petauridae

100% 4+

Burramyidae 1

66%

1

Vombatidae 2

99% 4+

Phascolarctidae Tarsipedidae Acrobatidae Macropodidae

Figure 2. Strict consensus of six equally most parsimonious trees of 107-character matrix with assumptions a1b1c1 (TL=381; CI=0.42; RC=0.24). Bootstrap values (%) are reported for nodes that appear in at least half of the replicates. The other numbers represent Bremer support, calculated based on strict consensus of heuristic searches with 100 replicates of trees 5 steps longer than the MPT and successive filtering.

a monophyletic group, the hypothesis originally formulated by Szalay (1982, 1994), and the result obtained by the combined analysis of molecular and morphological data of Luckett (1994). The phylogeny presented here (Fig. 3) suggests that either syndactyly has evolved independently in peramelinans and diprotodontians (Kirsch et al., 1997; Springer et al., 1998; contra Luckett, 1994), or that it evolved in the last common ancestor of these two groups and was subsequently lost by Notoryctes and Dromiciops.

Concerning the relationships of Paucituberculata, the results of the analysis do not appear robust. In the tree based on a posteriori weighting (Fig. 3), Paucituberculata is one of the basal group of marsupials after didelphids. But the topologies resulting in the different runs of the sensitivity analysis are incongruent (Fig. 4). Many different topologies result, and very little is in common among them concerning paucituberculatan relationships.

ARGYROLAGIDAE AND MARSUPIAL PHYLOGENY

489

Didelphidae Argyrolagidae

Caenolestidae Dasyuridae

Myrmecobiidae Peramelidae

Thylacomyidae Notoryctidae Microbiotheriidae Pseudocheiridae

Phalangeridae Petauridae

Burramyidae Vombatidae

Phascolarctidae Tarsipedidae Acrobatidae Macropodidae

Figure 3. Most parsimonious trees based on parsimony analysis of the data matrix with a posteriori weighting based on the RC values of the first search. DISCUSSION OF NEW CHARACTERS

SUMMARY AND CONCLUSIONS

Figure 5 presents the mapping of the new anatomical characters described here onto the marsupial phylogeny illustrated in Figure 3. As discussed above, characters 103 and 104 support the monophyly of Paucituberculata. The foramen ovale surrounded completely by the alisphenoid (105–1) supports the association of Dromiciops with diprotodontians. The other two characters, location of carotid foramen (106) and of transverse canal foramina (107), serve to support the monophyly of Macropodidae (Sa´nchez-Villagra, 1998), but provide no autopomorphies for any supra-familial clade.

The monophyly of Paucituberculata (Caenolestidae+ Argyrolagidae), based on the analysis of a revised and expanded version of the morphological data matrix by Springer et al. (1997), is well supported by several synapomorphies. The monophyly of Paucituberculata still holds even when parsimony is relaxed and trees several steps longer than the MPT are considered. The high explanatory power of this hypothesis is also demonstrated by the fact that all seven additional topologies of the sensitivity analysis also show a monophyletic Paucituberculata.

490

´ NCHEZ-VILLAGRA M. R. SA A

C

E

G

Didelphidae

B

Didelphidae

PAUCITUBERCULATA

PAUCITUBERCULATA

Dasyuridae

Dasyuridae

Myrmecobiidae

Myrmecobiidae

PERAMELINA

PERAMELINA

Notoryctidae

Notoryctidae

DIPROTODONTIA

Microbiotheriidae

Microbiotheriidae

DIPROTODONTIA

Didelphidae

D

Didelphidae

PAUCITUBERCULATA

Notoryctidae

DIPROTODONTIA

PERAMELINA

Microbiotheriidae

Myrmecobiidae

Notoryctidae

Dasyuridae

Dasyuridae

PAUCITUBERCULATA

Myrmecobiidae

Microbiotheriidae

PERAMELINA

DIPROTODONTIA

Didelphidae

F

Didelphidae

PERAMELINA

PERAMELINA

PAUCITUBERCULATA

PAUCITUBERCULATA

DIPROTODONTIA

Microbiotheriidae

Myrmecobiidae

DIPROTODONTIA

Dasyuridae

Notoryctidae

Notoryctidae

Myrmecobiidae

Microbiotheriidae

Dasyuridae

Didelphidae

H

Didelphidae

PAUCITUBERCULATA

PAUCITUBERCULATA

Dasyuridae

DIPROTODONTIA

Myrmecobiidae

Microbiotheriidae

PERAMELINA

PERAMELINA

Notoryctidae

Notoryctidae

DIPROTODONTIA

Myrmecobiidae

Microbiotheriidae

Dasyuridae

Figure 4. Topologies resulting in the different runs of the sensitivity analysis. In all cases are Diprotodontia and Paucitiuberculata monophyletic, but other than that there is little congruence among results. See text for an explanation concerning the different assumptions valid in each analysis. (A) a1b1c1 (B) a1b1c2, (C) a1b2c1, (D) a1b2c2, (E) a2b1c1, (F) a2b1c2, (G) a2b2c1, (H) a2b2c2.

With regard to the relations among extant families, the new characters and the incorporation of the fossil group have the effect of placing didelphids as basal in the tree (instead of dasyurids as in the original analysis of Springer et al., 1997). Also, Australasian marsupials plus Dromiciops form a monophyletic group. However, these results do not seem robust, as different assumptions in the parsimony analysis result in different topologies, as shown by the sensitivity analysis.

ACKNOWLEDGEMENTS This work is partially based on a portion of my doctoral dissertation, which was conducted at Duke University under the guidance of R. F. Kay and K. K. Smith. I thank them for their support and many discussions, as well as the other members of my committee: M. Cartmill, V. L. Roth, and J. R. Wible. For discussion of ideas, I wish to thank the following individuals: P.

C

D D id e A lph rg id C yro ae ae la n g D ole ida as st e y i M ur dae yr id a Pe me e ra cob Th me iid yl lid ae N aco ae ot m o y M ryc id ic ti ae ro da Ps bi e eu ot Ph do her al che iid Pe ang iri ae ta er da B uri ida e ur d a e Vo ram e m yi b Ph at dae a ida Ta sco e rs lar i A ped ctid cr ob ida ae M a e ac tid ro ae po di da e

B

D id e A lph rg id C yro ae ae la n g D ole ida as st e y i M ur dae yr id a Pe me e ra cob Th me iid yl lid ae N aco ae ot m o y M ryc id ic ti ae ro da Ps bi e eu ot Ph do her al che iid Pe ang iri ae ta er da B uri ida e ur d a e Vo ram e m yi b Ph at dae a ida Ta sco e rs lar i A ped ctid cr ob ida ae M a e ac tid ro ae po di da e

D id e A lph rg id C yro ae ae la n g D ole ida as st e y i M ur dae yr id a Pe me e ra cob Th me iid yl lid ae N aco ae ot m o y M ryc id ic ti ae ro da Ps bi e eu ot Ph do her al che iid Pe ang iri ae ta er da B uri ida e ur d a e Vo ram e m yi b Ph at dae a ida Ta sco e rs lar i A ped ctid cr ob ida ae M a e ac tid ro ae po di da e

A

D id e A lph rg id C yro ae ae la n g D ole ida as st e y i M ur dae yr id a Pe me e ra cob Th me iid yl lid ae N aco ae ot m o y M ryc id ic ti ae ro da Ps bi e eu ot Ph do her al che iid Pe ang iri ae ta er da B uri ida e ur d a e Vo ram e m yi b Ph at dae a ida Ta sco e rs lar i A ped ctid cr ob ida ae M a e ac tid ro ae po di da e

ARGYROLAGIDAE AND MARSUPIAL PHYLOGENY

491

Form of i2 not globular/i2 procumbent

globular cranium/i2 procumbent

alisphenoid/petrosal

just alisphenoid alisphenoid/squamosal

uncertain

equivocal

basisphenoid

basisphenoid/basioccipital suture

uncertain

absent

ant. and lat. to cartoid foramen

numerous, in pterygoid fossa

uncertain

Figure 5. Mapping of added anatomical characters onto the phylogeny presented in Fig. 3 using MacClade (Maddison & Maddison, 1992). (A) Form of braincase; (B) Foramen ovale location; (C) Carotid foramen location; (D) Transverse canal location.

492

´ NCHEZ-VILLAGRA M. R. SA

Bernstein, I. Horovitz, J. A. W. Kirsch, M. C. Maas, R. H. Madden, W. Maier, A. van Nievelt, G. R. Rougier, B. Williams, and specially R. Asher. Two anonymous reviewers provided useful comments that helped to improve the manuscript. I thank the following individuals for permission and assistance with the use of collections under their care: G. W. Rougier and R. Tedford (AMNH, Paleontology), F. Brady, B. Mader, D. Lunde, and R. D. E. MacPhee (AMNH, Mammalogy), F. Iwen, J. A. W. Kirsch, and E. Pillaert (Madison), L. Gordon and D. Schmidt (USNM); B. Stanley and B. Patterson (Chicago), F. Anaya (La Paz), E. Weber (Tu¨bingen), M. Ade, R. Angermann, S. Frahnert, A. Mess, and U. Zeller (Berlin). Research on argyrolagids was conducted in the context of a joint project between Duke University, the University of Florida, and the Museo Nacional de Historia Natural de La Paz. This work would not have been possible without the assistance and collaboration of F. Anaya, R. H. Madden and B. J. MacFadden. I thank F. Anaya for the loan of the specimen and R. F. Kay for making it possible. The fossil was skillfully prepared by A. van Nievelt. I thank M. Hohloch for photographic work and R. Britz for facilitating equipment for this purpose. This research was financially supported by the German Academic Exchange Program (DAAD), a Collection Study Grant of the AMNH, the Department of Biological Anthropology and Anatomy and the Graduate School at Duke University, and NSF grants to K. K. Smith, and to R. F. Kay and R. H. Madden. This work was completed at the Lehrstuhl fu¨r Spezielle Zoologie, at the Universita¨t Tu¨bingen. I thank Wolfgang Maier for his support.

REFERENCES Ameghino F. 1897. Mammife`res cre´tace´s de l’Argentine (deuxie`me contribution a` la connaissance de la faune mammalogique des couches a` Pyrotherium). Boletı´n del Instituto Geolo´gico Argentino 18: 1–117. Aplin KP. 1987. Basicranial anatomy of the early Miocene diprotodontian Wynyardia bassiana (Marsupialia: Wynyardiida) and its implications for wynyardiid phylogeny and classification. In Archer M, ed. Possums and Opossums. Studies in Evolution. Sydney: Surrey Beatty & Sons and the Royal Zoological Society of New South Wales, 369–391. Aplin K. 1990. Basicranial regions of diprotodontian marsupials: anatomy, ontogeny and phylogeny. Unpublished Doctoral Thesis, School of Biological Sciences, University of New South Wales. Aplin KP, Archer M. 1987. Recent advances in marsupial systematics with a new syncretic classification. In: Archer M, ed. Possums and Opossums. Studies in evolution. Sydney: Surrey Beatty & Sons and the Royal Zoological Society of New South Wales, xv–lxxii. Archer M. 1976. The basicranial region of marsupicarnivores

(Marsupialia), interrelationships of carnivorous marsupials, and affinities of the insectivorous marsupial peramelids. Zoological Journal of the Linnean Society 59: 217–322. Archer M. 1981. Revision of the dasyurid marsupial genus Sminthopsis Thomas. Bulletin of the American Museum of Natural History 168: 63–223. Archer M. 1982. A review of Miocene thylacinids (Thylacinidae, Marsupialia), the phylogenetic position of the Thylacinidae and the problem of apriorisms in character analysis. In: Archer M, ed. Carnivorous Marsupials. New South Wales: Royal Zoological Society of New South Wales, vol. II, 445–476. Archer M. 1984. Origins and early radiations of marsupials. In: Archer M, Clayton G, eds. Vertebrate Zoogeography and Evolution in Australasia. Perth: Hesperian Press, 585– 624. Archer M, Hand S, Godthelp H. 1988. A new order of Tertiary zalambdodont marsupials. Science 239: 1528– 1531. Asher R. 1999. A morphological basis for assessing the phylogeny of the ‘Tenrecoidea’ (Mammalia, Lipotyphla). Cladistics 15: 231–252. Beer GR de. 1937. The Development of the Vertebrate Skull. Oxford: Clarendon Press. Reprint. University of Chicago Press, 1985. Bown TM, Fleagle JG. 1993. Systematics, biostratigraphy, and dental evolution of the Palaeothentidae, later Oligocene to early-middle Miocene (Deseadan-Santacrucian) caenolestoid marsupials of South America. Journal of Paleontology 67: 1–76. Bremer K. 1988. The limits of amino-acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42: 795–803. Bremer K. 1994. Branch support and tree stability. Cladistics 10: 295–304. Bublitz J. 1987. Untersuchungen zur Systematik der Rezenten Caenolestidae Trouessart, 1898. Bonner Zoologische Monographien, Nr. 23, 1–96. Carpenter JM. 1988. Choosing among equally parsimonious cladograms. Cladistics 4: 291–296. Clemens WA, Richardson BJ, Baverstock P. 1989. Biogeography and phylogeny of the Metatheria. In: Walton DW, Dyne GR, eds. Fauna of Australia. Canberra: Australian Government Publishing Service, vol. 1B, Mammalia, 527– 548. Crompton AW. 1971. The origin of the tribosphenic molar. In: Kermack DM, Kermack KA, eds. Early Mammals. Zoological Journal of the Linnean Society 50: 65–87. Queiroz K de, Gauthier J. 1992. Phylogenetic taxonomy. Annual Review of Ecology and Systematics 23: 449–480. Farris JS. 1969. A successive approximations approach to character weighting. Systematic Zoology 18: 374–385. Farris JS. 1989. The retention index and the rescaled consistency index. Cladistics 5: 417–419. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791. Gaudin TJ, Wible JR, Hopson JA, Turnbull WD. 1996.

ARGYROLAGIDAE AND MARSUPIAL PHYLOGENY Reexamination of the morphological evidence for the Cohort Epitheria (Mammalia, Eutheria). Journal of Mammalian Evolution 3: 31–79. Goloboff PA. 1998. Principios Ba´sicos de Cladı´stica. Buenos Aires: Sociedad Argentina de Bota´nica. Gregory WK. 1910. The orders of mammals. Bulletin of the American Museum of Natural History 27: 1–524. Groves CP, Flannery T. 1990. Revision of the families and genera of bandicoots. In: Seebeck JH, Wallis RL, Brown PR, Kemper CM, eds. Bandicoots and Bilbies. Sydney: Surrey Beatty & Sons, 1–11. Hennig W. 1968. Elementos de una Sistema´tica Filogene´tica. Buenos Aires: Editorial Universitaria de Buenos Aires. Hennig W. 1983. Stammesgeschichte der Chordaten. Hamburg: Paul Parey. Hoffstetter R. 1968. Un gisement de mammife`res de´se´ade´ans (Oligoce`ne infe´rieur) en Bolivie. Comptes rendus de l’Acade´mie des sciences, Paris, se´rie D 269: 434–437. Jollie M. 1968. The head skeleton of a new-born Manis javanica with comments on the ontogeny and phylogeny of the mammal head skeleton. Acta Zoologica, Stockholm 49: 227–305. Kay RF, MacFadden BJ, Madden RH, Sandeman H, Anaya F. 1998. Revised age of the Salla beds, Bolivia, and its bearing on the age of the Deseadan South American Land Mammal ‘Age’. Journal of Vertebrate Paleontology 18: 189–199. Kay RF, Williams BA. 1994. Dental evidence for anthropoid origins. In: Fleagle JG, Kay RF, eds. Anthropoid Origins. New York: Plenum Press, 361–445. Kirsch JAW. 1977a. The classification of marsupials with special reference to karyotypes and serum proteins. In: Hunsaker D, ed. The Biology of Marsupials. New York: Academic Press, 1–50. Kirsch JAW. 1977b. The comparative serology of Marsupialia, and a classification of marsupials. Australian Journal of Zoology supplementary series 52: 1–152. Kirsch JAW, Archer M. 1982. Polythetic cladistics, or, when parsimony’s not enough: The relationships of carnivorous marsupials. In: Archer M, ed. Carnivorous Marsupials. New South Wales: Royal Zoological Society of New South Wales, vol. II, 595–619. Kirsch JAW, Dickerman AW, Reig OA, Springer MS. 1991. DNA hybridization evidence for the Australian affinity of the American marsupial Dromiciops australis. Proceedings of the National Academy of Sciences, USA 88: 10465–10469. Kirsch JAW, Lapointe F-J, Springer MS. 1997. DNAhybridisation studies of marsupials and their implications for metatherian classification. Australian Journal of Zoology 45: 211–280. Lee MSY. 1998. Similarity, parsimony and conjectures of homology: the chelonian shoulder girdle revisited. Journal of Evolutionary Biology 11: 379–387. Luckett WP. 1993. An ontogenetic assessment of dental homologies in therian mammals. In: Szalay FS, Novacek MJ, McKenna MC, eds. Mammal Phylogeny. Mesozoic Differentiation. Multituberculates, Monotremes, Early Therians and Marsupials. New York: Springer-Verlag, 182–204.

493

Luckett WP. 1994. Suprafamilial relationships within Marsupialia: resolution and discordance from multidisciplinary data. Journal of Mammalian Evolution 2: 255–283. Maddison DR. 1991. The discovery and importance of multiple islands of most-parsimonious trees. Systematic Zoology 40: 315–328. Maddison WP, Maddison DR. 1992. MacClade version 3. Sunderland, Massachusetts: Sinauer Associates. Mares MA. 1993. Heteromyids and their ecological counterparts: A pandesertic view of rodent ecology and evolution. In: Genoways HH, Brown JH, eds. Biology of Heteromyidae. Special Publication of the American Society of Mammalogists, 652–715. Marshall LG. 1977a. Cladistic analysis of borhyaenoid, dasyuroid, didelphoid, and thylacinid (Marsupialia: Mammalia) affinity. Systematic Zoology 26: 410–425. Marshall LG. 1977b. A new species of Lycopsis (Borhyaenidae: Marsupialia) from the La Venta fauna (late Miocene) of Colombia, South America. Journal of Paleontology 51: 633–642. Marshall LG. 1980. Systematics of the South American marsupial Family Caenolestidae. Fieldiana Geology 5: 1– 145. Marshall LG. 1987. Systematics of Itaboraian (middle Paleocene) age ‘opossum-like’ marsupials from the limestone quarry at Sa˜o Jose´ de Itaboraı´, Brazil. In: Archer M, ed. Possums and Opossums: Studies in Evolution. Sydney: Surrey Beatty and Sons Pty Ltd, 91–160. Marshall LG, Case JA, Woodburne MO. 1990. Phylogenetic relationships of the families of marsupials. In: Genoways HH, ed. Current Mammalogy. New York: Plenum Press, vol. 2, 433–502. Marshall LG, Muizon C de. 1995. Part II: The Skull. In: Muizon C de, ed. Pucadelphys andinus (Marsupialia, Mammalia) from the early Paleocene of Bolivia. Paris: Me´moires du Museum National d’Histoire Naturelle, vol. 165, 21–90. McBride SL, Clark AH, Farrar E, Archibald DA. 1987. Delimitation of a cryptic Eocene tectono-thermal domain in the eastern Cordillera of the Bolivian Andes through KAr dating and 39Ar/40Ar step heating. Journal of the Geological Society, London 144: 243–255. McKenna MC. 1980. Early history and biogeography of South America’s extinct land mammals. In: Ciochon RL, Chiarelli AB, eds. Evolutionary Biology of the New World Monkeys and Continental Drift. New York: Plenum Press, 43–77. Meacham CA. 1984. The role of hypothesized direction of characters in the estimation of evolutionary history. Taxon 33: 26–38. Muizon C de. 1994. A new carnivorous marsupial from the Palaeocene of Bolivia and the problem of marsupial monophyly. Nature 370: 208–211. Muizon C de. 1998. Mayulestes ferox, a borhyaenoid (Metatheria, Mammalia) from the early Palaeocene of Bolivia. Phylogenetic and palaeobiologic implications. Geodiversitas 20: 19–142. Murray P, Wells R, Plane M. 1987. The cranium of the

494

´ NCHEZ-VILLAGRA M. R. SA

Miocene thylacoleonid, Wakaleo vanderleuri: Click go the shears – a fresh bite at thylacoleonid systematics. In: Archer M, ed. Possums and Opossums. Studies in Evolution. Sydney: Surrey Beatty & Sons and the Royal Zoological Society of New South Wales, 433–466. Nowak RM. 1991. Walker’s Mammals of the World. Baltimore: The Johns Hopkins University Press. Pascual R, Goin FJ, Carlini AA. 1994. New data on the Groeberiidae: Unique late Eocene-early Oligocene South American marsupials. Journal of Vertebrate Paleontology 14: 247–259. Redford KH, Eisenberg JF. 1992. Mammals of the Neotropics: Volume 2, The Southern Cone, Chile, Argentina, Uruguay, Paraguay. Chicago: University of Chicago Press. Reig OA. 1981. Teorı´a del origen y desarrollo de la fauna de mamı´feros de Ame´rica del Sur. Monographie Naturae, Publicaciones del Museo Municipal de Ciencias Naturales ‘ Lorenzo Scaglia’’, 1–162. Reig OA, Kirsch JAW, Marshall LG. 1987. Systematic relationships of the living and the neocenozoic American ‘‘opossum-like’’ marsupials (Suborder Didelphiomorphia), with comments on the classification of these and of the Cretaceous and Paleogene New World and European metatherians. In: Archer M, ed. Possums and Opossums: Studies in Evolution. Sydney: Surrey Beatty & Sons and the Royal Zoological Society of New South Wales, 1–89. Retief JD, Krajewski C, Westerman M, Winfkein RJ, Dixon GH. 1995. Molecular phylogeny and evolution of marsupial protamine P1 genes. Proceedings of the Royal Society of London, Series B 259: 7–14. Ride WDL. 1962. On the evolution of Australian marsupials. In: Leeper GW, ed. The Evolution of Living Organisms. Melbourne: Melbourne University Press, 281–306. Ride WDL. 1964. A review of Australian fossil marsupials. Journal and Proceedings of the Royal Society of Western Australia 47: 97–131. Ross C, Williams BA, Kay RF. 1998. Phylogenetic analysis of anthropoid relationships. Journal of Human Evolution 35: 221–306. Rougier GW, Wible JR, Novacek MJ. 1998. Implications of Deltatheridium specimens for early marsupial history. Nature 396: 459–463. Sa´nchez-Villagra MR. 1998. Patterns of morphological change in the ontogeny and phylogeny of the marsupial skull. Unpublished Ph.D. Thesis, Duke University. Sa´nchez-Villagra MR, Kay RF. 1996. Do phalangeriforms (Marsupialia: Diprotodontia) have a hypocone? Australian Journal of Zoology 44: 461–467. Sa´nchez-Villagra MR, Kay RF. 1997. A skull of Proargyrolagus, the oldest argyrolagid (Late Oligocene Salla Beds, Bolivia), with brief comments concerning its paleobiology. Journal of Vertebrate Paleontology 17: 717– 724. Sa´nchez-Villagra MR, Kay RF, Anaya-Daza F. 2000. Cranial anatomy and paleobiology of the Miocene marsupial Hondalagus altiplanensis and a phylogeny of argyrolagids. Palaeontology 43: 287–301.

Sanderson MJ. 1995. Objections to bootstrapping phylogenies: A critique. Systematic Biology 44: 299–320. Segall W. 1969a. The auditory ossicles (malleus, incus) and their relationships to the tympanic: in marsupials. Acta Anatomica 73: 176–191. Segall W. 1969b. The middle ear region of Dromiciops. Acta Anatomica 72: 489–501. Segall W. 1970. Morphological parallelisms of the bulla and auditory ossicles in some insectivores and marsupials. Fieldiana Zoology 51: 169–205. Sempere TL, He´rail G, Oller J, Bonhomme MG. 1990. Late Oligocene–early Miocene major tectonic crisis and related basins in Bolivia. Geology 18: 946–949. Simmons NB. 1993. The importance of methods. Archontan phylogeny and cladistic analysis of morphological data. In: MacPhee RDE, ed. Primates and their Relatives in Phylogenetic Perspective. New York: Plenum Press, 1–61. Simpson GG. 1970. The Argyrolagidae, extinct South American marsupials. Bulletin of the Museum of Comparative Zoology 139: 1–86. Springer MS, Kirsch JAW, Case JA. 1997. The chronicle of marsupial evolution. In: Givnish TJ, Sytsma KJ, eds. Molecular Evolution and Adaptive Radiation. New York: Cambridge University Press, 129–161. Springer MS, Westerman M, Kavanagh JR, Burk A, Woodburne MO, Kao DJ, Krajewski C. 1998. The origin of the Australasian marsupial fauna and the phylogenetic affinities of the enigmatic monito del monte and marsupial mole. Proceedings of the Royal Society of London, series B 265: 2381–2386. Springer MS, Westerman M, Kirsch JAW. 1994. Relationships among orders and families of marsupials based on 12S ribosomal DNA sequences and the timing of the marsupial radiation. Journal of Mammalian Evolution 2: 85–115. Springer MS, Woodburne MO. 1989. The distribution of some basicranial characters within the Marsupialia and a phylogeny of the Phalangeriformes. Journal of Vertebrate Paleontology 9: 210–221. Swofford DL. 1993. PAUP – Phylogenetic Analysis Using Parsimony, Version 3.1.1. Washington, DC; Laboratory of Molecular Systematics, Smithsonian Institution. Swofford DL. 1999. PAUP∗ Phylogenetic Analysis Using Parsimony (∗and other methods) version 4. Sunderland, Massachusetts; Sinauer Associates. Swofford DL, Maddison WP. 1992. Parsimony, characterstate reconstructions, and evolutionary inferences. In: Mayden RL, ed. Systematics, Historical Ecology, and North American Freshwater Fishes. Stanford, CA: Stanford University Press, 186–223. Szalay FS. 1982. A new appraisal of marsupial phylogeny and classification. In: Archer M, ed. Carnivorous Marsupials. New South Wales: Royal Zoological Society of New South Wales, vol. II, 621–640. Szalay FS. 1994. Evolutionary History of the Marsupials and an Analysis of Osteological Characters. New York: Cambridge University Press. Tedford RH, Woodburne MO. 1987. The Ilariidae, a new

ARGYROLAGIDAE AND MARSUPIAL PHYLOGENY family of vombatiform marsupials from the Miocene strata of South Australia and an evaluation of the homology of molar cusps in the Diprotodontia. In: Archer M, ed. Possums and Opossums: Studies in Evolution. Sydney: Surrey Beatty and Sons and the Royal Zoological Society of New South Wales, 401–418. Tedford RH, Woodburne MO. 1998. The diprotodontian ‘hypocone’ revisited. Australian Journal of Zoology 46: 249–250. Villarroel C, Marshall LG. 1982. Geology of the Deseadan (early Oligocene) age Estratos Salla in the Salla-Luribay Basin, Bolivia, with descriptions of new Marsupialia. Ge´obios Me´moire Spe´cial 6: 201–211. Wa¨gele JW. 1994. Review of methodological problems of ‘Computer cladistics’ exemplified with a case study on isopod phylogeny (Crustacea: Isopoda). Zeitschrift fu¨r zoologische Systematik und Evolutionsforschung 32: 81–107. Wheeler WC. 1995. Sequence alignment, parameter sensitivity, and the phylogenetic analysis of molecular data. Systematic Biology 44: 321–331.

495

Wible JR. 1986. Transformations in the extracranial course of the internal carotid artery in mammalian phylogeny. Journal of Vertebrate Paleontology 6: 313–325. Wilkinson M. 1992. Ordered versus unordered characters. Cladistics 8: 375–385. Wincza H. 1896. Ueber einige Entwickungsveraenderungen in der Gegend des Scha¨delgrundes bei den Sa¨ugetieren. Bulletin international de l’Academie Polonaise de Sciences et des Lettres, Cracovie 8: 326–337. Wolff RG. 1984. A new early Oligocene argyrolagid (Mammalia: Marsupialia) from Salla, Bolivia. Journal of Vertebrate Paleontology 4: 108–113. Wortman JL. 1901. Studies of Eocene Mammalia in the Marsh Collection, Peabody Museum. American Journal of Science 11: 334–348. Wroe S. 1997. A reexamination of proposed morphologybased synapomorphies of the families of Dasyuromorphia (Marsupialia). I. Dasyuridae. Journal of Mammalian Evolution 4: 19–52.

496

´ NCHEZ-VILLAGRA M. R. SA APPENDIX

Marsupial data set (Springer et al., 1997) modified and expanded, with Argyrolagidae added. Letters represent represent polymorphic characters: A=(0,1); B=(1,2). See text for explanation concerning two possible codings for character 10.

Didelphidae Caenolestidae Microbiotheriidae Peramelidae Thylacomyidae Myrmecobiidae Notoryctidae Dasyuridae Phascolarctidae Vombatidae Macropodidae Phalangeridae Burramyidae Pseudocheiridae Petauridae Acrobatidae Tarsipedidae Ancestor Argyrolagidae

Didelphidae Caenolestidae Microbiotheriidae Peramelidae Thylacomyidae Myrmecobiidae Notoryctidae Dasyuridae Phascolarctidae Vombatidae Macropodidae Phalangeridae Burramyidae Pseudocheiridae Petauridae Acrobatidae Tarsipedidae Ancestor Argyrolagidae

10 (+10∗)

20

30

40

50

00010021000 10?11210110 00010110000 01010021210 01011021210 1112022??00 21?1000?000 11010021000 23211111111 33211210011 23011210?11 22111200111 22211200211 22211111111 22211210211 22?01210211 43??2?????? 00010010000 11?11210100

0110000011 0222100011 0221000010 0221000010 0221200010 0112000?00 000000002? 0000000010 1112211001 011220001? 0112200010 0112210201 0221210?00 1122221201 0212210101 0212200?01 ?????????? 0000000000 011110001?

0031100001 1131200012 1131000011 0021100011 0021100011 0230100001 2???0?0001 0021000001 0032222201 2?0012220? 1?21120010 0?33101112 0231111111 0011111012 0?31201110 1?10000010 ????122202 0021100001 1121000012

0000000000 000001?000 0000010000 0000001000 0000001000 00000?0000 0000101000 0000000000 0111002210 0010102220 1010100210 1111100100 011001?100 0111001110 0110101101 0010111101 0010???201 0000000000 000000?010

0000000000 ?000000000 ?001000000 0001000000 0010100000 1000001000 ?00000100? 1000000000 0010101111 0010100110 0100000011 0100000011 0000010000 0010000000 0001000000 0000010000 0000001000 0000000000 ?00???000?

60

70

80

90

100

0201222222 0202012221 0010211101 0211022222 0233022222 0002212122 000001220? 0201012121 1201210101 1202220?21 0102111122 0111211120 0201022221 0201221221 0201212221 0201011100 0021222122 0001001011 ?2?21?2?2?

0000000000 0100000000 0100000000 0101000000 0101000000 0101000000 0100000000 0101000000 1110000010 1022000001 1202000020 1202111121 1202111121 1202111121 1202111121 1002111121 1101211121 0000000000 ?200?0?0??

0000000000 00000000?0 0001121011 0000011000 100????0?? 1000010000 10001??0?? 1000010000 10011?121? 1001111210 1101121211 1111121211 10111??2?? 11111??21? 11111??21? 11011??1?? 101????1?? 0000000000 ?0000??0??

0010000001 0000?00??? 0120?0???? 1120000110 1120000??? 0121?00??? 0120?00??? 0121000001 1100111??0 1100111110 1120011110 1120011110 1120??1??? 1120011110 1120011??0 11200?1??1 11000?1??? 0000000000 0000??????

1100?10001 ??0??????? ??00?11??? 010010?010 ??0??????? ??0??????? ??0??????? 1100111010 ??11001100 0?11?01100 1?00111001 1000111001 ??00111001 ??00111001 1?00111001 ??00111001 ??00111010 000000?000 ??????????

0100001 ?111001 000010A 10000A1 ?000001 ?000001 ?000??? 1000001 0000111 0000202 0000112 00001AB 0000?0A 0000101 000010B 0000A?1 1000??0 0000000 ??1100B