Origin and Early Evolutionary History of Primates

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Leakey Foundation Final Report – Origin and Early Evolutionary History of Primates Stephen G. B. Chester, Ph.D. Assistant Professor, Department of Anthropology and Archaeology, Brooklyn College, City University of New York

Brief Summary This research project aimed to improve our understanding of the origin and earliest evolutionary history of primates, and to answer questions related to the systematics and paleobiology of primitive plesiadapiforms. Previously unknown morphology of primitive plesiadapiforms was documented based on recently discovered fossils. These new data, with emphasis on the basal plesiadapiform family Micromomyidae, contribute to our understanding of the taxonomy, phylogeny, and paleobiology of the most primitive primates. Two new species of micromomyids were described (Chester and Beard 2012) and a thorough systematic revision of Micromomyidae was conducted (Chester and Bloch 2013). All fossil specimens of micromomyids were analyzed, including virtually undescribed skeletons of Dryomomys szalayi and Tinimomys graybulliensis, which are currently regarded as the most primitive plesiadapiform skeletons known (Bloch et al. 2007). The first known postcranial fossils (astragali and calcanei) of the oldest and most primitive plesiadapiform, Purgatorius, were also discovered and described throughout the course of this project (Chester et al. 2015). These postcranial specimens were compared to those of other plesiadapiforms, euprimates, basally divergent treeshrews, and colugos to elucidate what separates Primates from the rest of Mammalia (Chester et al. in prep.).

All morphological data were incorporated into three phylogenetic analyses in order to better understand evolutionary relationships among euarchontan mammals (Chester et al. 2015).

Brief Summary of Publications Data generated from this research project have been published in seven peer-reviewed journal articles to date (Chester and Beard 2012, Annals of Carnegie Museum; Chester and Bloch 2013, Journal of Human Evolution; Boyer et al. 2013, Yearbook of Physical Anthropology; Chester et al. 2015, Proceedings of the National Academy of Sciences; Boyer et al. 2015, American Journal of Physical Anthropology; Yapuncich et al. 2015, American Journal of Physical Anthropology; Chester and Sargis Accepted, Phylonyms: A Companion to the PhyloCode) and presented at eight professional conferences (Chester et al. 2010, American Association of Physical Anthropology; Chester and Beard 2010, Society of Vertebrate Paleontology; Chester et al. 2011, SVP; Chester and Bloch 2012, AAPA; Chester et al. 2012, SVP; Chester et al. 2013, AAPA; Chester et al. 2013, SVP; Chester et al. 2015, AAPA).

Additional manuscripts are in preparation on the cranium and postcranial skeleton of micromomyid plesiadapiforms. See References Cited.

Results General results include a thorough systematic revision of the basal plesiadapiform family Micromomyidae, including the description of a new genus and two new species; analysis of the postcranial morphology of the most primitive plesiadapiforms, which resulted in new findings on the positional behavior of the oldest plesiadapiform, Purgatorius; incorporation of these new data into several different phylogenetic analyses in order to resolve relationships among plesiadapiforms and other euarchontan mammals; and a large digital collection of high resolution CT scans of extinct and extant primates and other mammals.

More specifically, two new species of micromomyid plesiadapiforms from the Late Paleocene locality Big Multi Quarry, Washakie Basin, Wyoming, were described. These new

Leakey Foundation Final Report – Origin and Early Evolutionary History of Primates

species are more primitive than previously known congeneric species and extend the known range of their respective genera geographically and or temporally. The co-occurrence of these micromomyid genera at Big Multi Quarry, as well as in the Clarks Fork Basin, Wyoming, suggests that they were sympatric over a sizeable geographic range for at least one million years.

The evolution of different dental specializations in each genus may have been driven by niche separation, as has been documented among living species of sympatric treeshrews. These results were presented at the annual meeting of the Society of Vertebrate Paleontology (Chester and Beard 2010) and were published in the Annals of Carnegie Museum (Chester and Beard 2012).

A systematic revision of the basal plesiadapiform family Micromomyidae was conducted and these new species from Big Multi Quarry, as well as other new specimens of micromomyids, add to our understanding of relationships among these primitive plesiadapiforms. Alpha taxonomy was assessed, and five genera and eleven species of micromomyids were recognized.

The new genus Foxomomys was erected to reflect differences between three Tiffanian North American Land Mammal Age (NALMA) species (‘Micromomys’ fremdi, ‘M.’ vossae, and ‘M.’ gunnelli) and all other micromomyids, including the type species of Micromomys, M. silvercouleei. ‘Micromomys’ millennius and ‘M.’ willwoodensis were attributed to Dryomomys primarily on the basis of having relatively large premolars. Myrmekomomys loomisi was not recognized as a distinct genus or species, and was considered a junior synonym of Tinimomys graybulliensis. The first major cladistic analysis to assess micromomyid interrelationships was performed, and a fairly well resolved strict consensus tree was obtained. Results suggest that the three species of Foxomomys are the most primitive micromomyids known, early Eocene (Wasatchian NALMA) Chalicomomys antelucanus appears to be fairly primitive (which implies a fairly long ghost-lineage), and there is support for the monophyly of Dryomomys and Tinimomys (Figure 1). These results were presented at the annual meeting of the American Association of Physical Anthropologists (Chester and Bloch 2012) and were published in the Journal of Human Evolution (Chester and Bloch 2013).

Body mass was estimated for eight of eleven species of micromomyids based on the area of the lower first molar, and these species generally fall into the 5-40g range. Such small body size suggests that micromomyids were partly insectivorous. Some findings related to the dietary component of the study suggest that the dental morphology of species of Foxomomys likely represent the primitive condition for Micromomyidae, which is fairly insectivorous.

Dryomomys, Chalicomomys, and Micromomys seem to be specialists with great emphasis on their premolars for processing, and Tinimomys has the most bunodont molars with bulbous cusps likely for processing non-leafy plant products (Chester and Bloch 2013). These observations are also part of a broader quantitative study that will be published in the future.

Partial skeletons of micromomyid plesiadapiforms were prepared out of freshwater limestone blocks at the Florida Museum of Natural History, and new postcranial elements were discovered based on clearly documented associations of bones. These associations allowed the assessment of isolated postcranial elements previously attributed to the family Micromomyidae (Beard 1989). Some of these previous attributions were correct, whereas some previously attributed elements did not belong to Micromomyidae (e.g., Manz et al. 2015). Postcranial analyses and comparisons of skeletons indicate and confirm that micromomyids were small, claw-clinging arborealists that were very similar in certain aspects of postcranial morphology to the most basally divergent treeshrew, Ptilocercus lowii, among extant mammals (Bloch et al.

2007, Chester et al. 2015, Chester et al. in prep.).

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Leakey Foundation Final Report – Origin and Early Evolutionary History of Primates

These new partial skeletons of micromomyid plesiadapiforms allowed the search for isolated elements of other primitive plesiadapiforms in museum collections, which ultimately led to the discovery of ankle bones of the oldest known plesiadapiform, Purgatorius. These isolated astragali and calcanei were found during an extensive search through vertebrate fossil collections from the late Puercan NALMA (~65 MYA) Garbani Channel fauna localities in Garfield County, Montana. Astragali and calcanei of Purgatorius were recognized based on size, relative abundance, and diagnostic euarchontan and plesiadapiform features. This taxonomic attribution is further supported by the absence of any other euarchontan fossils from the Garbani Channel fauna. Though recent cladistic analyses have supported a close relationship between Purgatorius and the condylarth Protungulatum (e.g., Goswami et al. 2011), these mammals differ considerably in tarsal morphology, and these differences reflect the use of arboreal compared to terrestrial substrates, respectively. Characteristics of the tarsals of Purgatorius indicate a mobile ankle joint typical of arboreal euarchontan mammals generally, and plesiadapiforms specifically (Figure 2). Among plesiadapiforms, the tarsals of Purgatorius are uniquely similar to those of micromomyids (Figure 3), which is consistent with the similar dental morphology of Purgatorius and primitive micromomyids (e.g., Foxomomys fremdi). These new data, and additional data on different plesiadapiforms and other euarchontan mammals were incorporated into three separate phylogenetic analyses (Figure 4). All of these analyses resulted in plesiadapiforms supported as primates, and results from two of these analyses support Purgatorius as the most basal primate and micromomyids among the most basal primates, which is consistent with the dental and tarsal similarities between these plesiadapiforms. These findings were presented at the annual meetings of the Society of Vertebrate Paleontology (Chester et al. 2012) and the American Association of Physical Anthropologists (Chester et al. 2013), and published in the Proceedings of the National Academy of Sciences (Chester et al. 2015).

Conclusions The objective of this research project was to collect data on extinct and extant primates and other euarchontan mammals in order to elucidate what separates the order Primates from the rest of Mammalia and to improve our understanding of the origin and earliest evolutionary history of primates. More specifically, goals included the systematic revision of the plesiadapiform family Micromomyidae, phylogenetic assessment of interrelationships among euarchontan mammals, and a functional morphological study of micromomyid, other plesiadapiform, and extant euarchontan skeletons to evaluate the positional behaviors and paleobiology of primitive stem primates. New species of micromomyids have been named and described (Chester and Beard 2012), a thorough analysis of micromomyid systematics, as well as the description of a new genus, has been conducted (Chester and Bloch 2013), and a manuscript describing the first known postcrania of the oldest plesiadapiform, Purgatorius, with new phylogenetic analyses supporting all plesiadapiforms as primates, has been published (Chester et al. 2015).

Based on results of this project, the most primitive primates can be differentiated from other euarchontan mammals in having unique dentitions. Many of the dental characteristics of primitive primates have previously been interpreted as being related to a shift from insectivory to more herbivory-frugivory. This might be expected for mammals, such as plesiadapiforms, that have been committed to life in the trees as reflected by many postcranial specializations that are correlated with arboreality in extant mammals. Micromomyid skeletons and the dentition and tarsals of Purgatorius provide further support for this ecological inference. Such dental and

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Leakey Foundation Final Report – Origin and Early Evolutionary History of Primates

postcranial specializations would have allowed these omnivorous, arboreal primates to exploit plant products including fruits, flowers, and associated insect pollinators made available by the major radiation of angiosperms in the earliest Paleocene. The postcranial specializations documented in the ankle of Purgatorius would have been beneficial, as they would have allowed the oldest known primate to access resources that were not directly available to many contemporary terrestrial mammals such as the condylarth Protungulatum.

New fossils of Purgatorius and comparisons among skeletons of micromomyid plesiadapiforms and non-primate euarchontan mammals such as the treeshrew Ptilocercus lowii suggest that the initial divergence of primates from other mammals did not involve major morphological transitions. Instead, our earliest evolutionary history as primates most likely began with minor changes in the craniodental and postcranial skeleton that eventually led to the diversity of diets and positional behaviors that have been documented in the primate fossil record and among extant primates. Additional fossils of early euarchontan mammals and continued comparative analyses that build on this and other studies will further improve our understanding of what separates Primates, the order to which we belong, from the rest of Mammalia.

References Cited Beard, K.C. 1989. Postcranial anatomy, locomotor adaptations, and palaeoecology of Early Cenozoic Plesiadapidae, Paromomyidae, and Micromomyidae (Eutheria, Dermoptera). Ph.D. dissertation, Johns Hopkins University School of Medicine.

Boyer, D. M., Yapuncich, G. S., Chester. S. G. B., Bloch, J. I., Godinot, M. 2013. Hands of early primates. Yearbook of Physical Anthropology 57:33-78.

Bloch, J.I., Silcox, M.T., Boyer, D.M., Sargis, E.J., 2007. New Paleocene skeletons and the relationship of plesiadapiforms to crown-clade primates. Proceedings of the National Academy of Sciences 104, 1159-1164.

Boyer, D. M., Yapuncich, G. S., Butler, J. E., Dunn, R. H., Seiffert, E. R. 2015. Evolution of Postural Diversity in Primates as Reflected by the Size and Shape of the Medial Tibial Facet of the Talus. American Journal of Physical Anthropology 157:134-177.

Chester, S. G. B., Beard, K. C. 2010. Late Paleocene micromomyid plesiadapiforms (Mammalia, Euarchonta) from Big Multi Quarry, Washakie Basin, Wyoming. Journal of Vertebrate Paleontology 30 Supplement: 71A. Chester, S. G. B., Beard, K. C. 2012. New micromomyid plesiadapiforms (Mammalia, Euarchonta) from the late Paleocene of Big Multi Quarry, Washakie Basin, Wyoming. Annals of Carnegie Museum 80:159-172.

Chester, S. G. B., Bloch, J. I. 2012. Systematics of Paleocene-Eocene micromomyid plesiadapiforms. American Journal of Physical Anthropology 147, S54: 114-115.

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Leakey Foundation Final Report – Origin and Early Evolutionary History of Primates

Chester, S. G. B., Bloch, J. I. 2013. Systematics of Paleogene Micromomyidae (Euarchonta, Primates) from North America. Journal of Human Evolution 65:109-142.

Chester, S. G. B., Bloch, J. I., Boyer, D. M., Clemens, W. A. 2015. Oldest known euarchontan postcrania and affinities of Paleocene Purgatorius to Primates. Proceedings of the National Academy of Sciences 112(5):1487-1492.

Chester, S. G. B., Bloch, J. I., Clemens, W. A. 2012. Tarsal morphology of the oldest plesiadapiform Purgatorius indicates arboreality in the earliest primates. Journal of Vertebrate Paleontology, Program and Abstracts, 77.

Chester, S. G. B., Bloch, J. I., Clemens, W. A. 2013. First known tarsals of the earliest primate Purgatorius. American Journal of Physical Anthropology 150, S56: 97-98.

Chester, S. G. B., Bloch, J. I, Sargis, E.J., Silcox, M. T., Williamson, T.E. 2011. Arboreality in palaechthonid plesiadapiforms (Mammalia, Primates): New evidence from a partial skeleton of early Paleocene Torrejonia wilsoni. Journal of Vertebrate Paleontology 31 Supplement: 87A. Chester, S. G. B., Boyer, D. M., Bloch, J. I., Sargis, E. J., Jacobs, R. L., Patel, B. A. 2010.

Hallucal metatarsal of euarchontan mammals. American Journal of Physical Anthropology 141, S50: 80.

Chester, S. G. B., Sargis, E. J. Accepted. Pan-Primates. In K. de Queiroz, P. D. Cantino, J. A. Gauthier (eds.), Phylonyms: A Companion to the PhyloCode, University of California Press: Berkeley.

Chester, S. G. B., Sargis, E. J., Bloch, J. I., Boyer, D.M. 2013. Nearly complete skeleton of early Eocene Tinimomys graybulliensis (Primates, Micromomyidae). Journal of Vertebrate Paleontology, Program and Abstracts, 104.

Chester, S. G. B., Sargis, E. J., Bloch, J. I., Boyer, D.M. 2015. Partial skeleton of early Eocene Tinimomys graybulliensis (Primates, Micromomyidae) from the Clarks Fork Basin, Wyoming.

American Journal of Physical Anthropology Supplement 60:104.

Goswami, A., G. V. R. Prasad, P. Upchurch, D. M. Boyer, E. R. Seiffert, O. Verma, E. Gheerbrant, J. J. Flynn. 2011. A radiation of arboreal basal eutherian mammals beginning in the Late Cretaceous of India. Proceedings of the National Academy of Sciences 108, 16333-16338 (2011).

Manz, C. L., Chester, S. G. B., Bloch, J. I., Silcox, M. T., Sargis, E. J. 2015. New partial skeletons of Palaeocene Nyctitheriidae and evaluation of proposed euarchontan affinities.

Biology Letters 11:20140911.

Silcox, M.T., Bloch, J.I., Boyer, D.M., Houde, P. 2010. Cranial anatomy of Paleocene and Eocene Labidolemur kayi (Mammalia: Apatotheria), and the relationships of the Apatemyidae to other mammals. Zoological Journal of the Linnean Society 160, 773-825.

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Leakey Foundation Final Report – Origin and Early Evolutionary History of Primates

Yapuncich, G. S., Gladman, J. T., Boyer, D. M. In press. Predicting Euarchontan Body Mass: A comparison of Tarsal and Dental variables. the Talus. American Journal of Physical Anthropology DOI: 10.1002/ajpa.22735.

Figure 1. Phylogenetic hypothesis for interrelationships among micromomyid plesiadapiforms placed in a stratigraphic context. Bold lines represent temporal ranges of taxa. Genera abbreviations: F., Foxomomys; M., Micromomys; C., Chalicomomys; T., Tinimomys; D., Dryomomys. Biozone abbreviations: Ti, Tiffanian; Cf, Clarkforkian; Wa, Wasatchian.

Chester and Bloch 2013 JHE.

Leakey Foundation Final Report – Origin and Early Evolutionary History of Primates

Figure 2. Comparison of micro-CT scan images of tarsal bones. Columns illustrate tarsals of condylarth Protungulatum (a), colugo Cynocephalus (b), treeshrew Ptilocercus (c), Purgatorius (d), the micromomyid plesiadapiform Dryomomys (e), and the adapoid euprimate Notharctus (f) right astragali (rows 1–3) and calcanei (rows 4–6) in dorsal (rows 1 and 4), plantar (rows 2 and 5), and distal (rows 3 and 6) views, respectively. Some elements are reversed for clarity. (Scale bars: 1 mm.) aef, astragalar ectal facet; aff, astragalar groove for tendon of musculus flexor fibularis (violet); ah, astragalar head (blue); asf, astragalar sustentacular facet (red); caf, calcaneal fibular facet; cef, calcaneal ectal facet; cf, calcaneocuboid facet (orange); cff, calcaneal groove for tendon of musculus flexor fibularis; csf, calcaneal sustentacular facet (red); ltf, lateral tibial facet (yellow); nav, astragalonavicular facet (red); pt, peroneal tubercle.

Chester et al. 2015 PNAS.

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Leakey Foundation Final Report – Origin and Early Evolutionary History of Primates

Figure 3. Results of principal component analysis of 23 astragalar measurements for 34 species of eutherian mammals (mostly euarchontans) (a) and 25 calcaneal measurements for 33 species of eutherian mammals (mostly euarchontans) (b). Lines connecting data points reflect a minimum-spanning tree computed from a Euclidean distance matrix. Polygons encompass taxa including living strepsirrhine and haplorhine euprimates (red), treeshrews (blue), and colugos (yellow). Gray polygons encompass fossil groups including adapoid and omomyoid euprimates, plesiadapiforms, and earliest Paleocene mammals Protungulatum donnae (Pd) and Procerberus formicarum (Pf). Results support tarsals attributed to Purgatorius (starred) as a plesiadapiform, which, like Protungulatum and Cretaceous Deccanolestes (D. hislopi, Dh; D. robustus, Dr), has tarsal features that may be plesiomorphic (e.g., a large calcaneal peroneal tubercle).

Chester et al. 2015 PNAS.

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Leakey Foundation Final Report – Origin and Early Evolutionary History of Primates

Figure 4. Hypotheses of evolutionary relationships of Purgatorius and other eutherian mammals. (a) Simplified resulting strict consensus cladogram based on data matrix of Goswami et al. (2011), Purgatorius tarsals, and five additional euarchontan taxa (colugo Cynocephalus, the micromomyid plesiadapiforms Foxomomys, Dryomomys, and Tinimomys, and the carpolestid plesiadapiform Carpolestes). Asterisks indicate results also supported by analyses of Goswami et al. (2011) with Laurasiatheria excluding Eulipotyphla and Afrotheria excluding Afrosoricida. (b) Simplified resulting single-most-parsimonious cladogram based on data from Bloch et al.

(2007) and Purgatorius tarsals. (c) Simplified resulting strict consensus cladogram based on data from Silcox et al. (2010) and Purgatorius tarsals. In all cladograms, Sundatheria (Dermoptera + Scandentia) is supported and indicated in green, Primates is supported and indicated in violet, and Purgatorius is supported as a primate and indicated in orange. Chester et al. 2015 PNAS.