Rooting Around the Eutherian Family Tree: the Origin and Relations of the Taeniodonta
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- Rook, D.L. & Hunter, J.P. J Mammal Evol (2014) 21: 75. doi:10.1007/s10914-013-9230-9
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Placing early groups into the overall phylogeny of eutherian mammals can be challenging, particularly when the group does not have extant members. We investigated the relationships of the Taeniodonta, an extinct group from the Late Cretaceous through Paleogene of North America. This group has a few purported close relatives, including Cimolestes, Procerberus, and Alveugena, that may form a sequence of ancestors and descendants. The leading hypothesis is that Procerberus gave rise to taeniodonts through Alveugena. We test this hypothesis and analyze relations to known stem and crown Eutheria to determine the place of taeniodonts in eutherian phylogeny. Cladistic analyses were performed using previously published characters and datasets, namely a taeniodont/cimolestid specific dataset and a reanalysis of Wible and colleagues (2009), with added taxa for both. Our studies suggest that taeniodonts arose from Cimolestes through Alveugena, that Procerberus is more distantly related to taeniodonts, and that taeniodonts and their relatives are stem eutherians. We diagnose the Taeniodonta based on these analyses. Other Paleogene groups, especially those allied with Cimolestes such as tillodonts and pantolestans, merit further study. Our findings indicate that stem eutherians such as the Taeniodonta, in addition to crown eutherians, continued to diversify during the Paleogene.
Taeniodonts are especially intriguing eutherian mammals. They are a classic example of rapid evolution, having been one of the first mammalian lineages to reach large body size (Patterson 1949). Their ecology as a group ranging from small insectivores to large, digging herbivores and the morphologies associated is quite distinct. The taeniodonts are a strictly North American group, allowing their biogeographical distribution to be easily gleaned from resources such as the Paleobiology Database and their history of dispersal and radiation inferred (Weinstein, unpublished thesis). Finally, their temporal range from the Late Cretaceous (Fox and Naylor 2003) through the middle Eocene (Turnbull 2004) makes them part of the great diversification of mammals following the mass extinction at the end of the Cretaceous (Fox and Naylor 2003; Rose 2006).
Taeniodonts are one of twenty or so orders of extinct eutherians known only from fossils whose relationships to the living and other extinct groups is unknown (Kielan-Jaworowska et al. 2004; Rose 2006). Determining whether an extinct eutherian order is part of the crown or stem group has been difficult, both because few characters distinguish crown and stem eutherians and because the ancestral condition of the crown group for many characters is unknown. Extinct group placement is further complicated by molecular sequence analyses (e.g., Springer et al. 2004) that leave out any group without some living representatives. Progress in the emergence of a stable tree for extant eutherian mammals has realigned relationships among living orders but unfortunately resulted in a large number of orphaned extinct lineages, whose relationships to the extant orders and even membership in the crown group remain uncertain. Taeniodont placement within Eutheria is further hampered by their highly modified morphology, obscuring potential synapomorphies that might be shared with other groups.
The origin of Taeniodonta has been under debate for over a century. Though the group was originally allied with rodents (Cope 1888) and edentates (Wortman 1896, 1897; Matthew 1937), more recent hypotheses agree that taeniodonts are one of the many lineages descended from Cimolestes, an early, primitive eutherian mammal known from the Late Cretaceous and early Paleocene of North America (Lillegraven 1969; McKenna 1969). Procerberus, another purported descendant of Cimolestes, has been consistently suggested as the link between Cimolestes and the taeniodonts (Lillegraven 1969; McKenna 1969). The early species P. formicarum and the larger P. grandis, which has taeniodont-like tooth wear, have been suggested as the lineage that gave rise to the taeniodonts (Eberle 1999). Alveugena, a relatively recent find, has been well supported as the bridge between Procerberus and the taeniodonts (Eberle 1999; Rook et al. 2010).
Whether any given extinct eutherian taxon is part of the stem or crown group helps to constrain the time of appearance of the crown group, which further allows molecular phylogeneticists to estimate divergence times (e.g., Springer et al. 2003) and paleontologists to test those estimates (Foote et al. 1999; Hunter and Janis 2006). Differences in crown and stem members of the Paleogene diversification help resolve how the Cretaceous/Paleogene extinction event impacted the evolution of the Eutheria, a topic of ongoing discussion and debate (Savage and Russell 1983; Alroy 1999; Novacek 1999; Archibald and Deuthschmann 2001; Rose and Archibald 2005; Rose 2006; Bininda-Edmonds et al. 2007; Wible et al. 2007, 2009; Meredith et al. 2011; O’Leary et al. 2013).
Here, using cladistic analysis, we test the hypotheses that Cimolestes, Procerberus, and Alveugena are sister taxa to the taeniodonts and that the taeniodonts are monophyletic. We also test the hypothesis that taeniodonts are members of the crown group of Eutheria. In order to accomplish these goals, we adapted character sets already used to explore the relationships among taeniodonts and their presumed close relatives (Schoch 1986; Eberle 1999; Rook et al. 2010; Rook and Hunter 2011) and the best dataset available at the present time for testing crown or stem group status of extinct eutherians (Wible et al. 2007, 2009).
Materials and Methods
We performed a heuristic branch-swapping cladistic analysis using NONA (Goloboff 1999) and WinClada (Nixon 2002). NONA was used to find the most parsimonious tree(s), calculate branch length, and calculate Bremer support values, which show how many steps longer a tree would need to be before the clade in question is lost (Wenzel 2002). WinClada was used to calculate homoplasy indicators based on the NONA trees: consistency index (CI), based on the number of additional unnecessary evolutionary steps taken in a character; and retention index (RI), determined by how different the character evolution is from the maximum possible number of steps (Wenzel 2002).
Taeniodont Relations to Basal Cimolestans
Literature used for character coding
Schoch and Lucas (1981a)
Van Valen (1966)
Schoch and Lucas (1981b)
Bloch et al. (2004)
Sloan and Van Valen (1965)
Middleton and Dewar (2004)
Krause and Gingerich (1983)
Lucas and Williamson (1993)
Fox and Naylor (2003)
Stem Versus Crown Eutheria
For investigation into the stem or crown group membership of the Taeniodonta, we used the published character matrix of Wible et al. (2009). Schowalteria, the most basal taeniodont (according to Rook et al. 2010; Rook and Hunter 2011) and Alveugena, the purported sister taxon (Eberle 1999; Rook et al. 2010) were added (see Appendix 2 for character definitions and codes of added taxa).
Taeniodont Relations to Basal Cimolestans
Stem Versus Crown Eutheria
The monophyly of the Taeniodonta has recently been called into question by the discovery of an ancient taeniodont from the Late Cretaceous of Canada, Schowalteria. Fox and Naylor (2003) speculated that Schowalteria was a stylinodontid, the younger family of taeniodonts, based on certain characters but not on a cladistic analysis. They argued that its early appearance caused Taeniodonta to be a para- or even polyphyletic grouping. This concern has been disputed recently, but is still likely a cause for debate (Rook and Hunter 2011).
Here, the monophyly of Taeniodonta is supported by a Bremer support of 3 (Fig. 1). Schowalteria is the sister group to the rest of the taeniodonts (as also in Rook and Hunter 2011), no longer contradicting its early appearance in the fossil record. There are also no autapomorphic characters in this analysis precluding Schowalteria from being the ancestral taeniodont (Rook and Hunter 2011). Accordingly, we rediagnose the monophyletic Taeniodonta in the final section of this paper to include Schowalteria and all other taeniodonts.
Taeniodont Relations to Basal Cimolestans
The basal cimolestan tree reported here differs from the phylogenies of Eberle (1999) and Rook et al. (2010). Although Alveugena is still the sister taxon to the taeniodonts (Eberle 1999; Rook et al. 2010), Cimolestes is the sister taxon to Alveugena + Taeniodonta, not Procerberus. The Procerberus species do not appear as a lineage leading to Alveugena and the taeniodonts, contrary to Eberle (1999) and Rook et al. (2010), but are a monophyletic clade (see also Rook et al. 2010). Alveugena as a sister taxon to the taeniodonts is again supported (Eberle 1999; Rook et al. 2010), with a Bremer support value of 3.
The original placement of Cimolestes as basal to Procerberus and Alveugena was likely due to its use as an outgroup in those earlier studies (Eberle 1999; Rook et al. 2010). Cimolestes is only slightly more primitive in character than Alveugena, and using it as an outgroup may have failed to fully polarize characters in the earlier analyses. Protictis as the outgroup in this study, chosen because it is completely removed from the problem, allowed Cimolestes to fall closer to the taeniodonts than Procerberus. In the earlier studies of Eberle (1999) and Rook et al. (2010), Cimolestes was constrained to the base of the tree. Although this study agrees with Eberle (1999) and Rook et al. (2010) in supporting the hypothesis of a cimolestid origin of the taeniodonts, it disagrees over which cimolestid (Cimolestes or Procerberus) is more closely related.
Another pattern that emerges is the paraphyly of McKenna and Bell's (1997) Cimolestidae, which includes Cimolestes and Procerberus as well as Didelphodus and Acmeodon. The latter two taxa are here allied with the widely recognized palaeoryctids, Aaptoryctes and Palaeoryctes. These two "cimolestid" taxa are disputed in their familial placement. Though the paraphyly of the cimolestids is apparent in this analysis, other inferences about the palaeoryctid and cimolestid taxa are beyond the scope of the current study. As for the taeniodonts, they are still more closely related to the cimolestids, particularly Cimolestes, than to the palaeoryctids.
Stem Versus Crown Eutheria
The main result of our large-scale analysis is that the taeniodonts unite with the Cimolestidae, placing them among stem Eutheria. This study is the first time a taeniodont has been identified as a stem or crown member of the Eutheria, and this analysis places them with the former, along with Alveugena. This placement is supported by Bremer supports of 4 for Alveugena + Schowalteria, and does not change the original Bremer support values of the Wible et al. (2009) Cimolestidae clade. The basal taeniodont is separated from the other cimolestids in this analysis by a number of features: two greatly enlarged lower incisors; a one-tooth-root-width diastema between p1 and p2; double-rooted P4; p5 talonid width equal to the trigonid; lower molars with vestigial paraconids, protoconids subequal in height to the para- and/or metaconids, and m3 smaller than m2; anterior mental foramen below p2, masseteric fossa extending anteriorly onto the dentary body, and a mandibular symphysis extending to p1 or more anteriorly.
The characters listed below emerge as potentially diagnostic for crown Eutheria. Though this study did not explicitly seek out such characters, this list could be a jumping-off point for future research and placement of eutherian groups. The vast majority of the characters separating the stem and crown eutherians in this analysis were dental. Several were molar characters, only three were cranial, and one was a premolar character— a diastema present between the first and second lower premolars. The characters of the upper molars included a strongly reduced or absent ectoflexus, a metacone and paracone that are subequal with bases separated, and weak or absent postmetacrista. The characters of the lower molars were trigonids less than twice or subequal in height and subequal or narrower in width than talonids, and possessing a protoconid that is subequal to the paraconid and/or metaconid. Finally, the cranial characters, all from the dentary, were the absence of a condyloid crest, a condylar process lacking a posteriorly directed peduncle, and a condyle that lies above the tooth row by more than a molar length. These characters show once again that the taeniodonts belong with the stem eutherian mammals and not with any later-appearing clade. This list also gives researchers specific characters that may be used to distinguish extinct stem from crown eutherians in the future. Character states that place the taeniodonts among the stem eutherians are best seen in the oldest, most basal members of the group. More derived, later taeniodonts appear to converge on some crown eutherian states, such as reduced upper molar stylar shelves and nearly equal lower molar trigonid and talonid heights. This distribution of character states hints at possible future avenues of study involving the parallel and convergent evolution of some traits in crown and stem eutherians in the Paleogene.
It has been suggested that taeniodont origins lie within the basal cimolestids (including Cimolestes) (McKenna 1975). In these analyses, it is evident that Alveugena is the sister group of taeniodonts, but Cimolestes may be more closely related to the taeniodonts than Procerberus, as opposed to Procerberus being more closely related to taeniodonts in the studies of Eberle (1999) and Rook et al. (2010). Cimolestes and Alveugena are the closest sister groups to the taeniodonts, and quite possibly form an ancestral sequence. No other cimolestan genus included is more closely related. Taeniodonta to all evidence is also monophyletic (Rook and Hunter 2011; Rook et al. 2010), and we present a revised diagnosis of the clade in the following section.
Taeniodonts and Alveugena are placed as stem eutherians along with Cimolestes. Their placement as stem eutherians and use in the current analysis have helped to determine several characters that could be used to distinguish stem from crown eutherians in the future. These analyses show once again that crown and stem eutherians were diversifying together through the Paleogene.
MAMMALIA Linnaeus, 1758
EUTHERIA Gill, 1872
Taeniodonta Cope, 1876
Included Genera. Onychodectes Cope, 1888, Wortmania Hay, 1899, Conoryctes Cope, 1881, Conoryctella Gazin, 1939, Huerfanodon Schoch and Lucas, 1981a, Psittacotherium Cope, 1882, Ectoganus Cope, 1874, Stylinodon Marsh, 1874, Schochia Lucas and Williamson, 1993 (now Robertschochia Lucas, 2011), and Schowalteria Fox and Naylor, 2003.
Distribution. Lancian (Late Cretaceous) to Uintan (middle Eocene) of western North America, Tiffanian (middle to late Paleocene) and Uintan of Texas, and Tiffanian of South Carolina.
Diagnosis. Larger than cimolestids and differs from Cimolestes and Alveugena in the following ways: upper and lower canines moderate to large, stout, and recurved; P1/p1 single rooted, P2/p2 double rooted, P4 triangular, p4 premolariform, P5 with well-developed paracone and protocone, lacking a metacone, with cuspate stylar shelf, and p5 nonmolariform with a well-developed talonid heel, more so than the cimolestids; upper molars molariform with small, lingually placed protocone and conules, paracone and metacone moderate and placed far labial, small stylar shelf, no pre- or post-cingula, ectocingula present and well developed; lower molars with variable relative trigonid/talonid widths, trigonid/talonid heights generally subequal and where different never as different as with the cimolestids, protoconids and metaconids subequal with smaller paraconid placed more labial than the metaconid, and lacking the accessory talonid notch cusp and expanded m3 talonid of Cimolestes and Alveugena; hypsodonty found in all cheek teeth, with early animals showing more crown hypsodonty and later showing more root hypsodonty to hypselodonty; and the wear pattern generally over entire surface of cheek teeth and often deep enough to expose pulp cavity.
Comments on Diagnosis. We numbered premolars assuming an ancestral count of five of which the third upper and lower premolars are lost in crown eutherians and some stem eutherians (e.g., Wible et al. 2009). Although the Taeniodonta has not been formally diagnosed, Schoch (1986) provided a detailed list of taeniodont characteristics. The diagnosis above has been modified from Schoch’s (1986) list. Premolar, canine, and wear characters were added, and also lower molar paraconid characters. Characters removed or modified include subequal talonid and trigonid on the lower molars and decreasing molar size posteriorly.
Discussion. Taeniodonta is here referred to as a monophyletic clade as demonstrated above in the phylogenetic analysis. The new discovery of Schowalteria has modified the diagnosis the most, as it is the earliest and most basal taeniodont, whereas Onychodectes had been claimed as most basal at the time of Schoch (1986). Although the monophyly of this group has been debated, these parsimony analyses, the first undertaken of the entire group along with non-taeniodonts among both crown and stem eutherians, show that the Taeniodonta is a monophyletic stem eutherian group.
This work was submitted by D. Rook, formerly D. Weinstein, in partial fulfillment of the degree Master of Science at The Ohio State University under the supervision of J. P. Hunter. We thank J. W. Wenzel for help on cladistic analyses. We also thank J. Galkin of the American Museum of Natural History and M. Brett-Surman of the National Museum of Natural History for access to collections. We thank R. Asher and especially J. Wible for extensive discussion of their character matrix and cladistic analyses. We thank two anonymous reviewers for their comments on our manuscript. The Ohio State University, Department of Evolution, Ecology and Organismal Biology, supported this work through a University Fellowship and a Graduate Teaching Assistantship.