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Fossoriality and evolutionary development in two Cretaceous mammaliamorphs

Nature volume 592, pages 577–582 (2021)Cite this article

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Abstract

Mammaliamorpha comprises the last common ancestor of Tritylodontidae and Mammalia plus all its descendants1. Tritylodontids are nonmammaliaform herbivorous cynodonts that originated in the Late Triassic epoch, diversified in the Jurassic period2,3,4,5 and survived into the Early Cretaceous epoch6,7. Eutriconodontans have generally been considered to be an extinct mammalian group, although different views exist8. Here we report a newly discovered tritylodontid and eutriconodontan from the Early Cretaceous Jehol Biota of China. Eutriconodontans are common in this biota9, but it was not previously known to contain tritylodontids. The two distantly related species show convergent features that are adapted for fossorial life, and are the first ‘scratch-diggers’ known from this biota. Both species also show an increased number of presacral vertebrae, relative to the ancestral state in synapsids or mammals10,11, that display meristic and homeotic changes. These fossils shed light on the evolutionary development of the axial skeleton in mammaliamorphs, which has been the focus of numerous studies in vertebrate evolution12,13,14,15,16,17 and developmental biology18,19,20,21,22,23,24,25,26,27,28. The phenotypes recorded by these fossils indicate that developmental plasticity in somitogenesis and HOX gene expression in the axial skeleton—similar to that observed in extant mammals—was already in place in stem mammaliamorphs. The interaction of these developmental mechanisms with natural selection may have underpinned the diverse phenotypes of body plan that evolved independently in various clades of mammaliamorph.

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Fig. 1: Holotypes of F. sinensis (JZMP-2107500093) and J. cheni (ZGY0052).
Fig. 2: Dentition and forelimbs of F. sinensis and J. cheni.
Fig. 3: Simplified consensus tree using Bayesian phylogenetic tip-dating analysis.
Fig. 4: Comparison of axial skeletons of selected fossils and extant taxa of mammaliamorph.

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Data availability

In addition to the material presented in the Article and the accessioned specimens, supporting images, graphics and essential phylogenetic data are provided in the Extended Data figures and Supplementary Information. Computed tomography and computed laminography scanning data are available on the Archives of Digital Morphology, Key Laboratory of Vertebrate Evolutionary Systems Science of the Chinese Academy of Sciences (http://www.admorph.org), at https://doi.org/10.12112/M.101 (F. sinensis) and https://doi.org/10.12112/M.102 (J. cheni). Life Science Identifiers for the new genera and species have been registered at Zoobank as: Fossiomanus Mao, Zhang, Liu & Meng, LSIDurn:lsid:zoobank.org:act:C579314D-6330-4D7F-9C71-AF7E8DC9A1DD; Fossiomanus sinensis Mao, Zhang, Liu & Meng, LSIDurn:lsid:zoobank.org:act:3D66E77B-F3A1-4A0D-923B-11121CB934EC; Jueconodon Mao, Zhang, Liu & Meng, LSIDurn:lsid:zoobank.org:act:580A4D81-BFFE-4BE7-BDE9-267ED929CA3A; and Jueconodon cheni Mao, Zhang, Liu & Meng, LSIDurn:lsid:zoobank.org:act:C97D7EF4-68C4-4B09-9E78-BA6F48ADCA09. The data matrix for the phylogenetic analysis is in the Supplementary Information, and has been as deposited in MorphoBank (http://www.morphobank.org; project number 3943).

Code availability

The MrBayes commands for Bayesian analyses are provided in the Supplementary Information.

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Acknowledgements

We thank the Jinzhou Paleontological Museum for providing one of the studied specimens housed in their collections; J. Hooker, P. Brewer and M. Day (Natural History Museum), B. Lindow (Natural History Museum of Denmark), G. Billet and M. Godinot (Museum National d’Histoire Naturelle) for access to specimens under their curatorial care; S.-H. Xie and S.-J. Li (IVPP) for specimen preparation; D. W. Krause (Denver Museum of Nature and Science), S. Hoffmann (New York Institute of Technology) and M. Ruta (University of Lincoln) for data sharing; Y.-M. Hou, P.-F. Yin and P.-H. Wang (IVPP), S.-Y. Hou, M.-J. Han, Y.-Y. Zhang (Yinghua Inspection and Testing) for computed tomography and computed laminography scanning of the specimens; N. Wong (American Museum of Natural History (AMNH)) for drawing the figures; Z.-H. Zhou, X.-L. Wang, J.-Y. Zhang and F. Jin (IVPP) for discussions of localities and the identification of fossil fishes; H.-Y. Liao (Yunnan University) for identification of Eosestheria; and C.-Y. Yu (AMNH) for data transformation. This work was supported by the National Natural Science Foundation of China (41688103 and 42072002); the Strategic Priority Research Program (B) of the CAS (XDB26000000); the Youth Innovation Promotion Association, CAS (2019076); the Kalbfleisch Fellowship, Richard Gilder Graduate School, AMNH; the 100 Young Talents Program of the CAS.

Author information

Authors and Affiliations

  1. Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences (CAS), Beijing, China

    Fangyuan Mao & Chi Zhang

  2. CAS Center for Excellence in Life and Paleoenvironment, Beijing, China

    Fangyuan Mao & Chi Zhang

  3. Division of Paleontology, American Museum of Natural History, New York, NY, USA

    Fangyuan Mao & Jin Meng

  4. Beipiao Pterosaur Museum of China, Beipiao, China

    Cunyu Liu

  5. Earth and Environmental Sciences, Graduate Center, City University of New York, New York, NY, USA

    Jin Meng

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  1. Fangyuan Mao
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  4. Jin Meng
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Contributions

F.M. and J.M. conceived the study and wrote the paper; F.M. conducted the computed tomography scan and rendering work; C.L. collected and curated specimens; C.Z. ran the Bayesian analyses; and all authors edited and approved the manuscript.

Corresponding authors

Correspondence to Fangyuan Mao or Jin Meng.

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The authors declare no competing interests.

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Peer review information Nature thanks Fernando Abdala, P. David Polly, Hans-Dieter Sues and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data figures and tables

Extended Data Fig. 1 Holotype of F. sinensis (JZMP-2107500093).

a, Holotype of F. sinensis, primarily in ventral view. b, Composed computed laminographic image of the holotype. The black box in a and the inset at the bottom left of b indicate fish specimens of Jinanichthys, an index vertebrate fossil for the Jiufotang Formation. The close-up views of caudal vertebrae in a, b correspond to the area outlined in a red-dashed line in a.

Extended Data Fig. 2 Optical and computed tomography-rendered skulls of F. sinensis.

a, c, f, Ventral view of the skull of F. sinensis. b, d, Dorsal view of the skull of F. sinensis. e, One slice of the computed tomography scanning images of the skull of F. sinensis, showing the contrast quality of the image. f, Preserved positions of upper teeth (white) and lower teeth (yellow). There are six upper postcanines that are visible (indicated as ‘upc’ in a) in the specimen, of which the mesial five are fully erupted and functional; PC6 is still erupting and the rest of the tooth crowns are not fully developed within the maxilla (Extended Data Fig. 3a–d). cev, cervical vertebrae; lin, lower incisor; lpc, lower postcanine(s); na, nasal; occ, occipital condyle; pdu, postdentary unit; syd, symphysis (suture) of the dentary; uin, upper incisor; zya, zygomatic arch.

Extended Data Fig. 3 Tooth morphologies of F. sinensis.

a–d, Occlusal (a), buccal (b), lingual (c) and dorsal (root) (d) views of the right upper postcanine dentition. e, Occlusal view of a left upper postcanine. f, g, Occlusal (f) and dorsal (root) (g) views of two left upper postcanines. Teeth shown in e and f are probably PC1 and PC3, respectively, as judged by their wear. h, i, Buccal (h) and lingual (i) views of two left upper postcanines. j–l, Crown (j), distal (k) and lingual (l) views of a left lower postcanine. m, n, Crown (m) and buccal (n) views for two left lower postcanines. o, Buccal view of a loose left lower postcanine. p–r, Lingual (p), buccal (q) and lateral (r) views of the left upper incisor. s, t, Lateral (s) and lingual (t) views of the right upper incisor. u, v, Lateral (u) and lingual (v) views of the left lower incisor. B, buccal cusp (with number) of upper tooth; L, lingual cusp (with number) of upper tooth; M, medial cusp (with number) of upper tooth; b, buccal cusp (with number) of lower tooth; l, lingual cusp (with number) of lower tooth. PC1 to PC5 are functional postcanine teeth with roots developed, and PC6 is erupting and lacks roots.

Extended Data Fig. 4 Limb structures of F. sinensis.

a, b, Optical (a) and computed laminography (b) images of the forelimb. c, d, Optical (c) and computed laminography (d) images of the hindlimb. as, astragalus; ca, calcaneus; cu, cuboid; dc1, distal carpal 1 (trapezium); dc2, distal carpal 2 (trapezoid); dc3, distal carpal 3 (capitate, magnum); ectc, ectocuneiform; entc, entocuneiform; itl, intermedium (lunate); lcl, lateral centrale (unciform, hamate); mc, metacarpal; mcl, medial centrale (centrale); mec, mesocuneiform; mt, metatarsal; na, navicular; phd, distal phalanx (number referring to digit); phi, intermediate phalanx; php, proximal phalanx; ps, pisiform; rad, radiale (scaphoid); uln, ulnare (triquetrum, cuneiform). The tritylodontid terminology for the carpal bones (labelled in the figure) is based on refs. 3,71. The lateral centrale may be interpreted as a fused distal carpal IV and V41. Intermediate phalanx 5 was broken anteriorly.

Extended Data Fig. 5 Holotype of J. cheni (ZGY0052).

a, Holotype of J. cheni in dorsal view (optical photograph). b, Composed computed laminography image of the holotype. The black boxes in a highlight carapaces of the conchostracan Eosestheria, an index invertebrate fossil in the Yixian Formation72. The inset in the bottom right of a shows the structure of Eosestheria. The computed laminography image of the right arm was digitally placed to closer to its original position in b. -l, left side; -r, right side; ac, acetabulum; cp, carpus; mp, metacarpus; na, navicular; nap, nasal anterior process; ph, phalanx; sm, sternum.

Extended Data Fig. 6 Optical and computed tomography-rendered skulls of J. cheni.

a, b, Ventral view of the skull of J. cheni. c, d, Dorsal view of the skull of J. cheni. cop, coronoid process; glf, glenoid fossa; mac, mandibular condyle; nap, nasal projections; ocp, occiput; omc, ossified Meckelian cartilage; ors, orbital socket; pm, promontorium; pop, postorbital process.

Extended Data Fig. 7 Computed tomography-rendered dentition of J. cheni.

a, b, Original preservation of the dentition. c–f, Digitally restored dentition. Arrows point to tooth germs in the dentition.

Extended Data Fig. 8 The forelimbs and hindlimbs of J. cheni.

a, b, Optic (a) and computed laminography (b) images of the left forelimb. c, d, Optic (c) and computed laminography (d) images of the right hindlimb. e, f, Optic (e) and computed laminography (f) images of the right forearm. na, navicular; ph, phalanges; phi, intermediate phalanx (number referring to digit); php, proximal phalanx (number referring to digit). Images in a–d are shown on the same scale.

Extended Data Fig. 9 The consensus tree using Bayesian phylogenetic tip-dating analysis.

In the consensus tree (50% majority rule), the node ages (divergence times) are the median estimates (numbers shown in small font) and node bars (blue) represent the 95% highest posterior density intervals. Fossoriality and meristic or homeotic changes in various taxa and clades are mapped on the tree. Red dots indicate major clades of mammaliamorph. Red bar highlights the paraphyletic eutriconodontans. Extant taxa are not shown (indicated by green arrows); see Extended Data Fig. 10b for trees including extant species.

Extended Data Fig. 10 Strict consensus of most parsimonious trees and result of non-clock Bayesian analysis.

a, Strict consensus of 319 most parsimonious trees obtained in this study. The data matrix consists of 121 generic-level taxa and 551 characters. All characters are unordered and have equal weight. Two characters are parsimony-uninformative (informative for Bayesian analyses). Tree length = 2,864; consistency index = 0.321; retention index = 0.790; rescaled consistency index = 0.254; homoplasy index = 0.679. The two species described in this Article are denoted by black dots. b, Result of nonclock Bayesian analysis using Lewis Mkv model with gamma rate variation across characters (Mkv+Γ). Numbers at selected nodes are posterior clade probabilities. Black bar indicates the position of the taxa described in this Article. Arrow indicates the branch connection. More details are provided in Methods and Supplementary Information.

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This file contains additional supplementary material, including: definition of vertebral region, sources for vertebral formula, sources for fossoriality, meristic-homeotic changes, chronological constraints, character list, references, and results of phylogenetic analyses.

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Mao, F., Zhang, C., Liu, C. et al. Fossoriality and evolutionary development in two Cretaceous mammaliamorphs. Nature 592, 577–582 (2021). https://doi.org/10.1038/s41586-021-03433-2

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