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Fossils document evolutionary changes of jaw joint to mammalian middle ear

Nature volume 628, pages 576–581 (2024)Cite this article

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Abstract

The dual jaw joint of Morganucodon1,2 consists of the dentary–squamosal joint laterally and the articular–quadrate one medially. The articular–quadrate joint and its associated post-dentary bones constitute the precursor of the mammalian middle ear. Fossils documenting the transition from such a precursor to the mammalian middle ear are poor, resulting in inconsistent interpretations of this hallmark apparatus in the earliest stage of mammaliaform evolution1,2,3,4,5. Here we report mandibular middle ears from two Jurassic mammaliaforms: a new morganucodontan-like species and a pseudotribosphenic shuotheriid species6. The morganucodontan-like species shows many previously unknown post-dentary bone morphologies1,2 and exhibits features that suggest a loss of load-bearing function in its articular–quadrate joint. The middle ear of the shuotheriid approaches the mammalian condition in that it has features that are suitable for an exclusively auditory function, although the post-dentary bones are still attached to the dentary. With size reduction of the jaw-joint bones, the quadrate shifts medially at different degrees in relation to the articular in the two mammaliaforms. These changes provide evidence of a gradual loss of load-bearing function in the articular–quadrate jaw joint—a prerequisite for the detachment of the post-dentary bones from the dentary7,8,9,10,11,12 and the eventual breakdown of the Meckel’s cartilage13,14,15 during the evolution of mammaliaforms.

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Fig. 1: CT images of the holotype of Dianoconodon youngi (IVPP V4257).
Fig. 2: Lower jaw and mandibular middle ear of Dianoconodon youngi (IVPP V4257).
Fig. 3: Mandibular middle ear of the shuotheriid docodontiform Feredocodon chowi.
Fig. 4: Mandibular middle ears and transformation of the articular–quadrate joints in mammaliaforms.

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Data availability

All material related to the data for phylogenetic analyses is presented in this Article and its Supplementary Information. Life science identifiers for the new genera and species have been registered at Zoobank as Dianoconodon (LSIDurn:lsid:zoobank.org:act:81F7A97D-4CF1-4803-900C-55D8D63F41C4) and Dianoconodon youngi (LSIDurn:lsid:zoobank.org:act:E5077547−6D55-472D-875A-3012831C33AC). The character list and data matrix for the phylogenetic analysis can be found in ref. 6 and have been deposited in MorphoBank (https://morphobank.org/; project number 5075).

Code availability

The PAUP commands for parsimony-based analyses and the MrBayes commands for Bayesian analyses have been deposited in Zenodo (https://doi.org/10.5281/zenodo.10597270; see also ref. 6).

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Acknowledgements

We thank Z. Li and Z. Liu for access to the specimens reported in this study; H. You for discussions about localities and stratigraphy; M. Chase, A. Smith, Y. Hou, P. Yin and J. Wang for CT scanning of the specimens; A. Shi and Y. Xu for help with drawings; and N. Wong for CT reconstruction. F.M. was supported by the National Natural Science Foundation of China (42122010, 42288201 and 42072002) and the Youth Innovation Promotion Association of the Chinese Academy of Sciences (2019076).

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Author notes

  1. Deceased: Fakui Zhang

Authors and Affiliations

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

    Fangyuan Mao, Chi Zhang, Jicheng Ren & Fakui Zhang

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

    Fangyuan Mao & Jin Meng

  3. Bureau of Land and Resources of Lufeng County, Lufeng, China

    Tao Wang

  4. Fossil Research Center of Chuxiong Prefecture, Chuxiong, China

    Guofu Wang

  5. Museums Victoria, Melbourne, Victoria, Australia

    Thomas Rich & Patricia Vickers-Rich

  6. School of Earth, Atmosphere and Environment, Monash University, Melbourne, Victoria, Australia

    Thomas Rich & Patricia Vickers-Rich

  7. School of Earth and Planetary Science, Curtin University, Perth, Western Australia, Australia

    Patricia Vickers-Rich

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

    Jin Meng

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Contributions

F.M. and J.M. conceived the study and wrote the paper. F.M. performed the CT scanning and rendering work. C.Z. ran the Bayesian analyses. J.R. rendered the CT data. T.W. and G.W. participated in the fieldwork and provided stratigraphic data. F.Z. participated in early discussions of the work. T.R. and P.V.-R. provided discussions and manuscript edits. All authors edited and approved the manuscript.

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Correspondence to Fangyuan Mao or Jin Meng.

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Extended data figures and tables

Extended Data Fig. 1 CT reconstruction of the skull and mandibles of Dianoconodon youngi (IVPP V4257, holotype).

a,b, Right (a) and left (b) view of the skull with partial associated skeleton. c–h, Dorsal (c), ventral (d), left (e), right (f), posterior (g), and anterior (h) views of the cranium. i, Dorsal view of the two mandibles as preserved (see Extended Data Fig. 4 for other aspects of the mandible). Abbreviations: anp, angular process of the dentary; C (c), upper (lower) canine; cop, coronoid process; dec, dentary condyle; fr, frontal; glf, glenoid fossa of the squamosal; I (i), upper (lower) incisor; inf, infraorbital foramen; ju, jugal; M (m), upper (lower) molar; max, maxilla; na, nasal; occ, occipital condyles; P(p), upper (lower) premolar; pa, parietal; pod, post-dentary bones; pmx, premaxilla; prm, promontorium of the petrosal; qua, quadrate; qun, quadrate notch; squ, squamosal; st, stapes; vet, vertebrae.

Extended Data Fig. 2 CT reconstruction of the upper dentitions of Dianoconodon youngi (IVPP V4257, holotype).

a–c, Left upper dentition in labial (a), occlusal (b) and lingual (c) views. d–f, Right upper dentition in lingual (d), occlusal (e) and labial (f) views. See also Extended Data Fig. 1.

Extended Data Fig. 3 CT reconstruction of the lower dentitions of Dianoconodon youngi (IVPP V4257, holotype).

a–c, Left lower dentition in labial (a), occlusal (b) and lingual (c) views. d–f, Right lower dentition in lingual (d), occlusal (e) and labial (f) views.

Extended Data Fig. 4 Comparison of the mandible and post-dentary trough, and reconstruction of the mandibular middle ears in Morganucodon and Dianoconodon youngi.

a–d, Reconstructed lower jaw of Morganucodon in labial (a), lingual (b, with the post-dentary bones; c, without the post-dentary bones) and posterior views. e–h, CT-rendered lower jaw of Dianoconodon in labial (e), lingual (f, with the post-dentary bones and quadrate; g, without the post-dentary bones and quadrate), and posterior (h) views. i–k, Drawings of the post-dentary trough (i, j) and ventral aspect (k) of the mandible of Morganucodon. l–o, Medial (l, without post-dentary bones; m, with postdentary bones) and posteromedial (n, without post-dentary bones; o, with postdentary bones) views of the posterior mandible showing the post-dentary trough and attached post-dentary bones, the quadrate, and quadratojugal. p,q, Ventral (p) and dorsal (q) views of the posterior portion of the dentary and post-dentary bones and quadrate. r–v, Comparison of Dianoconodon (V) with various versions of the reconstructed MdME of Morganucodon. Abbreviations: apd, angular process of the dentary; arf, articular fossa; dec, dentary condyle; mcg, Meckelian groove; mdf, mandibular foramen; mdr, medial ridge; pdt, post-dentary trough; pod, post-dentary bones. A-Q with the same scale. Some images have been reversed for convenience of comparison. Drawings are modified from the following sources: a–d and i–k (adapted from figures 7, 14 and 20A of ref. 1), r (redrawn from figure 8 of ref. 52), s (redrawn from figure 9A of ref. 59), t (redrawn from plate 3-11 of ref. 16) and u (redrawn from figure 28.7G of ref. 17). Red arrows in d and h indicate difference in the relationship of the post-dentary bones with the dentary and the joint condition (single or dual) in each form. Blue shaded oval areas highlight various interpretations of the Morganucodon middle ear; in particular note the reflected lamina, the retroarticular process and the quadrate–articular joint in different shapes and positions. See Supplementary Information for additional details.

Extended Data Fig. 5 The stapes, quadrate and quadratojugal of Dianoconodon youngi in comparison with the corresponding bones of Morganucodon.

a, The right middle ear of Dianoconodon (a1, medial view; a2, posterior view with the petrosal; a3, posterior view without the petrosal) b, The left quadrate and quadratojugal (partial) in roughly dorsal (b1), ventral (b2), medial (b3), posterior (b4), and lateral (b5) views. c, The right quadrate in anterior (c1), posterior (c2), lateral (c3), dorsal (c4), ventral (c5), and medial (c6) views. d, The right stapes in medial (d1), ventral (d2), and dorsal (d3) views. e, The left stapes of Morganucodon in medial (e1), anterior (e2), and dorsal (e3) views. f, The left quadratojugal of Dianoconodon in lateral (f1), medial (f2), and posterior (f3) views. g, The left quadrate of Morganucodon in anterior (g, posterior (g2), lateral (g3), dorsal (g4), ventral (g5), and medial (g6) views (corresponding to C1−6). Abbreviations: acs, anterior crus of the stapes; ang, angular bone (ectotympanic); apd, angular process of the dentary; art, articular (malleus); asq, articulation for the squamosal; cob, coronoid bone; cop, coronoid process; dec, dentary condyle; dop, dorsal plate of the quadrate; fps, footplate of the stapes; fqu, facet for the quadrate; glf, glenoid fossa; ju, jugal; omc, ossified Meckel’s cartilage; pcs, posterior crus of the stapes; pef, perilymphatic foramen; pet, petrosal; pstm?, posterior process for the stapedial muscle?; qua, quadrate; quj, quadratojugal; qun, quadrate notch; rla, reflected lamina of the angular bone (ventral limb of the ectotympanic); squ, squamosal; st, stapes; stp, stapedial process of the quadrate; tro, trochlea of the quadrate. e and g are adapted from figures 85 and 86 of ref. 2.

Extended Data Fig. 6 The post-dentary bones, angular, and articular complex of Dianoconodon youngi in comparison with the corresponding bones of Morganucodon.

a, The mandibles with the middle-ear bones in ventral view. b, The middle-ear bones in medial (left side, upper) and lateral (right side, lower) views. c–e, Right angular in medial (c), lateral (d), and dorsal (e) views. f–g, Left angular bone in lateral (f) and medial (g) views. h–j, Left articular complex in dorsal (h), lateral (i), and medial (j) views. k,l, Right articular complex in posterior views (slightly different in angle in k and l). m, Posterior view of the articular complex of Morganucodon. n,o, Close-up medial (n) and dorsal (o) views of the posterior end of the right articular complex of Dianoconodon, showing the facet for trochlea of the quadrate. p,q, Articular complex of Morganucodon in medial (p) and dorsal (q) views. Abbreviations: ang, angular (ectotympanic); apa, anterior process of the angular (anterior limb of the ectotympanic); apm, anterior process of the articular; aps?, articular-prearticular suture?; art, articular (malleus); asur, anterior process of the surangular; dap, dorsal articular process; den, dentary; dpa, dorsal process of the angular; ftq, facet for trochlea of quadrate; omc, ossified Meckel’s cartilage; pod, post-dentary bones; ppa, posterior process of the angular; pra, prearticular (anterior process of the malleus); qua, quadrate; quj, quadratojugal; rar, retroarticular process of the articular (base of the manubrium of the malleus in mammals); rla, reflected lamina of the angular bone (ventral limb of the ectotympanic); sas?, surangular-articular suture?; st, stapes; sur, surangular. m is adapted from figure 88A(v) of ref. 2 and p and q are adapted from figure 33 of ref. 1.

Extended Data Fig. 7 Comparison of the mandible and post-dentary trough, and reconstruction of the mandibular middle ears in shuotheriid Feredocodon and docodontans.

a, The reconstructed mandible and middle ear in medial view. b, Lateral view of the reconstructed dentary. c,d, CT-rendered left (c) and right (d, reversed) posterior portions of the mandible with the middle-ear bones, showing their relative sizes with the reconstructed mandibles. e,f, CT-rendered mandibles of the paratype of Feredocodon chowi (IMMNH-PV01925, Mao et al., Feredocodon) in medial (e) and lateral (f) views. g–j, Medial views of the mandible of Docodon (g, adapted from figure 5a of ref. 43), Borealestes (h, adapted from figure 7A1 of ref. 48), Agilodocodon (i, adapted from figure 2i of ref. 5) and Microdocodon (j, adapted from figure S2J of ref. 42). k–n, Medial (slightly dorsal, k), medial (slightly ventral, l), dorsal (m), and ventral (n) views of the posterior portion of the left dentary of Feredocodon chowi (IMMNH-PV01925), showing the structure of the post-dentary trough. Abbreviations: ang, angular (ectotympanic); apd, angular process of the dentary; art, articular (malleus); cop, coronoid process; cor, coronoid; dec, dentary condyle; ean, efflected angular process; mde, middle ear; mdf, mandibular foramen; mdr, medial ridge; mrp, medial ridge protuberance43; omc, ossified Meckel’s cartilage; pdt, post-dentary trough; qua, quadrate (incus).

Extended Data Fig. 8 CT reconstruction of the middle-ear bones of Feredocodon chowi (IMMNH-PV01925, paratype) in relation to the surrounding structures.

a,b, Ventral (a) and ventrolateral (b) views of the basicranial region, showing the relationship of the middle-ear bones with the promontorium and dentary. c, Posterior (nearly) view. d–f, Various angles of primarily ventral views (d shows the ventral view of the dentary, same as in Extended Data Fig. 7n). g,h, Posterodorsal (g) and posteroventral (h) views. i–k, Posterodorsal views at different angles. Abbreviations: afq, articular facet for the quadrate; ang, angular (ectotympanic) art, articular (malleus); asur, anterior process of the surangular; cri, crista interfenestralis; dec, dentary condyle; den, dentary; ean, efflected angular process; juf, jugular foramen; mrp, medial ridge protuberance43,48; occ, occipital condyles; omc, ossified Meckel’s cartilage; pef, perilymphatic foramen; pmp, promontorium of the petrosal; pra, prearticular (anterior process of the malleus); qua, quadrate (incus); rar, retroarticular process (base of the manubrium); rla, reflected lamina of the angular (ventral limb of the ectotympanic); squ, squamosal; st, stapes; stp, stapedial process of the quadrate; sub?, surangular boss?; sur, surangular.

Extended Data Fig. 9 Middle-ear bones of the shuotheriid Feredocodon in comparison with those of docodontans and Sinoconodon.

a, Lateral (a1) and medial (a2) views of the middle-ear bones. b, The stapes in lateral view. c, The quadrate (incus) in medial (c1), lateral (c2), dorsal (c3), and anterior (c4) views. c, The articular complex in medial (d1), lateral (d2), and posterior (d3) views. e, Medial (e1) and lateral (e2) views of the angular (ectotympanic). A-E are from the left middle ear. f, Lateral (f1) and medial (f2) views of the right middle ears. g, Partial stapes of Haldanodon in lateral (g1) and medial (g2) views (adapted from figure 12A-B of ref. 3. h–j, Reconstructed middle ears of Agilodocodon, Castorocauda, and Sinoconodon. k, Sinoconodon quadrate (incus) in anterior and posterior views. l, Agilodocodon quadrate (incus) in anterior and posterior views. Drawlings of h–l are adapted from figure S5 of ref. 5. Abbreviations: acs, anterior crus of the stapes; afa, articular facet for the articular; afq, articular facet for the quadrate; ang, angular bone (ectotympanic); apa, anterior process of the angular (anterior limb of ectotympanic); aps?, articular-surangular suture?; art, articular (malleus); asur, anterior process of the surangular; crs, crus of the stapes; dop, dorsal plate of the quadrate; fps, footplate of the stapes; omc, ossified Meckel’s cartilage; pcs, posterior crus of the stapes; ppa, posterior process of the angular (dorsal limb of the ectotympanic); pra, prearticular (anterior process of the malleus); qua, quadrate (incus); rar, retroarticular process (base of the manubrium but not the manubrium); rla, reflected lamina of the angular (ventral limb of the ectotympanic); st, stapes; stp, stapedial process of the quadrate; sub?, surangular boss?; sur, surangular; tro, trochlea of the quadrate.

Extended Data Table 1 Measurements of Dianoconodon
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Supplementary information

Supplementary Information

The Supplementary Information provides information about the systematic palaeontology of the study, including the taxonomy and a detailed description of the new genus and species, Dianoconodon youngi, with the focus on the mandibular middle ear. It also provides a detailed description of the mandibular middle ear of the Middle Jurassic shuotheriid Feredocodon chowi. A brief introduction about the phylogenetic analyses is also included. The data matrix and results from PAUP and from the Bayesian tip-dating analyses are presented. The related character list and dataset are presented in MorphoBank (http://www.morphobank.org; project number 5075), and the related detailed settings and logs of these analyses are deposited in Zenodo (https://doi.org/10.5281/zenodo.10597270; ref. 6); see also Methods in the main text). The subjects treated and presented in the Supplementary Information are listed at the start of the Supplementary file.

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Mao, F., Zhang, C., Ren, J. et al. Fossils document evolutionary changes of jaw joint to mammalian middle ear. Nature 628, 576–581 (2024). https://doi.org/10.1038/s41586-024-07235-0

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