New Paleocene skeletons and the relationship of plesiadapiforms to crown-clade primates

Abstract

Plesiadapiforms are central to studies of the origin and evolution of primates and other euarchontan mammals (tree shrews and flying lemurs). We report results from a comprehensive cladistic analysis using cranial, postcranial, and dental evidence including data from recently discovered Paleocene plesiadapiform skeletons (Ignacius clarkforkensis sp. nov.; Dryomomys szalayi, gen. et sp. nov.), and the most plesiomorphic extant tree shrew, Ptilocercus lowii. Our results, based on the fossil record, unambiguously place plesiadapiforms with Euprimates and indicate that the divergence of Primates (sensu lato) from other euarchontans likely occurred before or just after the Cretaceous/Tertiary boundary (65 Mya), notably later than logistical model and molecular estimates. Anatomical features associated with specialized pedal grasping (including a nail on the hallux) and a petrosal bulla likely evolved in the common ancestor of Plesiadapoidea and Euprimates (Euprimateformes) by 62 Mya in either Asia or North America. Our results are consistent with those from recent molecular analyses that group Dermoptera with Scandentia. We find no evidence to support the hypothesis that any plesiadapiforms were mitten-gliders or closely related to Dermoptera.

Fig. 1.

Paleocene plesiadapiform skeletons and reconstructions. (A and B) Composite skeleton (A) and reconstruction (B) of paromomyid I. clarkforkensis based on UM specimens 108210 and 82606 (C and D). Skeleton (C) and reconstruction (D) of micromomyid D. szalayi based on UM 41870. Bones not shaded in gray in B and D were not recovered. Documentations of dental–postcranial skeleton associations are outlined in SI Text, Part 1, and its referenced figures.

Fig. 2.

Dentition (Holotype: UM 108210) of I. clarkforkensis. Occlusal (A) view of the rostrum and occlusal (B) and buccal (C) views of the left dentary. (Scale bar: 5 mm.)

Fig. 3.

Dentition of D. szalayi (Holotype: UM 41870). Occlusal (A) view of the rostrum, lingual (B) view of the left premaxilla with I^1–2 and occlusal (C) and buccal (D) views of the left dentary. (Scale bar: 5 mm.)

Fig. 4.

Phylogeny of euarchontans based on a single-most-parsimonious cladogram (tree length = 555, consistency index = 0.548, retention index = 0.523). Divergences of sister taxa are shown schematically, with no implied knowledge of the exact timing of cladogenesis. Node 1 is Euarchonta. Decay indices and bootstrap percentages are as follows (respectively): Node 2 (Primates) = 4, 67%; Node 3 (Euprimateformes) = 3, 30%; Node 4 (Plesiadapoidea) = 2, 52%; Node 5 (Euprimates) = 1, 42%; Scandentia + Dermoptera = 5, 64%. When the analysis is run with all characters unordered, the topology of the resulting single-most-parsimonious cladogram is identical to the one presented here. See SI Text, Part 5, for a list of apomorphies supporting each node. Molecular estimate of primate origins from Springer et al. (31). Logistical model estimate of euprimate origins (D) from Tavaré et al. (32) and probability estimate of euprimate origins (C) from Gingerich and Uhen (33). Molecular divergence estimates (31) as well as the logistical model estimate (32) are notably older than the first occurrences of Euprimates (A) and Primates (B) documented in the fossil record. Results from our analysis suggest that Primates (light tan area) originated in the latest Cretaceous or earliest Paleocene of North America, Euprimateformes originated in the early Paleocene of either Asia or North America, and Euprimates (dark tan rectangle) originated in the Late Paleocene of Asia, Africa, or North America.

Fig. 5.

Hypothesis of character change in euarchontan evolution. Purple: euarchontan features [Node 1: relatively low crowned molars, entotympanic contribution to the auditory bulla (character 83)]; Blue: primate features [Node 2: increased length of M₃ and enlarged M₃ hypoconulid (characters 62, 69); presence of a postprotocingulum on the upper molars (character 71); elongate manual phalanges (character 172)]; yellow: euprimateform features [Node 3: relatively short metatarsals, a nail on the hallux (character 129); a petrosal bulla (character 83)]; red: euprimate features [Node 5: elongate tarsals (characters 134, 137); enlarged peroneal process on first metatarsal (character 159); nails on all digits (character 156); forward-facing orbits with a short snout (character 91)]. A, Eutherian Asioryctes; B, Dermopterans Elpidophorus (teeth: B3) and Cynocephalus (cranium and postcrania: B2, B1); C, Scandentian Ptilocercus; D, Primates Purgatorius (teeth: D3), Ignacius (cranium: D2), and D. szalayi (postcrania: D1); E, Plesiadapoids Chronolestes (teeth: E3) and Carpolestes (cranium and postcrania: E2, E1); F, Euprimates Altanius (teeth: F3) and Notharctus (cranium and postcrania: F2, F1).