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A monotreme-like auditory apparatus in a Middle Jurassic haramiyidan

Abstract

Among extant vertebrates, mammals are distinguished by having a chain of three auditory ossicles (the malleus, incus and stapes) that transduce sound waves and promote an increased range of audible—especially high—frequencies1. By contrast, the homologous bones in early fossil mammals and relatives also functioned in chewing through their bony attachments to the lower jaw2. Recent discoveries of well-preserved Mesozoic mammals have provided glimpses into the transition from the dual (masticatory and auditory) to the single auditory function for the ossicles, which is now widely accepted to have occurred at least three times in mammal evolution3,4,5,6. Here we report a skull and postcranium that we refer to the haramiyidan Vilevolodon diplomylos (dating to the Middle Jurassic epoch (160 million years ago)) and that shows excellent preservation of the malleus, incus and ectotympanic (which supports the tympanic membrane). After comparing this fossil with other Mesozoic and extant mammals, we propose that the overlapping incudomallear articulation found in this and other Mesozoic fossils, in extant monotremes and in early ontogeny in extant marsupials and placentals is a morphology that evolved in several groups of mammals in the transition from the dual to the single function for the ossicles.

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Fig. 1: Three types of middle ear in mammaliaforms.
Fig. 2: Vilevolodon diplomylos (IMMNH-PV01699A).
Fig. 3: The incudomallear articulation across Mammaliaformes.

Data availability

The specimen (IMMNH-PV01699) studied here has been deposited in the Inner Mongolia Museum of Natural History. The data matrix for the phylogenetic analysis is deposited in MorphoBank (project number 3760); computed tomography data are deposited in MorphoSource at https://doi.org/10.17602/M2/M167344.

Code availability

The Batch commands for the Bayesian analysis are included in the Supplementary Information.

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Acknowledgements

We thank P. Bowden for his illustrations; S. Xie for specimen preparation; Z. Yin and T. Stecko for computed tomography scanning; and X. Xu for assistance and discussion. The study was supported by the National Science Foundation of China (41688103,41728003), the Double First-Class joint programme of Yunnan Science and Technology Department and Yunnan University (2018FY001-005), China–Myanmar Joint Laboratory for Ecological and Environmental Conservation and US National Science Foundation grant DEB 1654949.

Author information

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Authors

Contributions

S.B. and J.R.W. conceived the study, undertook comparative and analytical work and wrote the paper; S.L.S. performed Bayesian analyses and edited the manuscript; H.H. contributed to the virtual reconstructions of the skull; and J.W., S.L.S. and B.G. contributed to fossil interpretation and provided feedback on the paper.

Corresponding authors

Correspondence to John R. Wible or Shundong Bi.

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The authors declare no competing interests.

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Peer review information Nature thanks Robin Beck, Simone Hoffmann and Guillermo Rougier for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Fig. 1 Cladograms to illustrate various hypotheses regarding haramiyidan relationships.

The Middle Jurassic Tiaojishan haramyidans are here included in Euharamiyida10 (a junior synonym of Haramiyida66 in our phylogenetic analysis (Supplementary Information)). Clades considered to be close relatives of euharamiyidans are in blue in each tree (simplified from the originals). a, Euharamiyidans are in a monophyletic Haramiyida, positioned outside of Mammalia (parsimony and Bayesian analyses in ref. 4). b, Euharamiyidans are in a monophyletic Haramiyida, positioned within Mammalia in Allotheria with multituberculates; the gondwanatherian Vintana (not shown) is within Trechnotheria (parsimony and Bayesian analyses in ref. 3). c, Haramiyidans are polyphyletic; euharamiyidans fall within Mammalia in Allotheria with multituberculates, and Thomasia and Haramiyavia form a clade with tritylodontids outside Mammaliaformes; gondwanatherians (not shown) are sister to multituberculates (parsimony analysis in ref. 28). d, Haramiyidans are polyphyletic; euharamiyidans fall within Mammalia, and Thomasia and Haramiyavia form a clade with tritylodontids outside Mammaliaformes; the gondwanatherian Vintana (not shown) is within Euharamiyida (tip-dated Bayesian analysis in ref. 67). A, Allotheria; M, Mammalia; Mf, Mammaliaformes; T, Theria.

Extended Data Fig. 2 Dentition of V. diplomylos (IMMNH-PV01699A).

ac, Upper left dentition in buccal (a), occlusal (b) and lingual (c) views. df, Lower left dentition in buccal (d), occlusal (e) and lingual (f) views. Regarding the numbering of the incisors, all haramiyidans for which the dentition is known have one upper and lower incisor (except for Xianshou linglong with two upper incisors10). The distal enlarged incisor was identified as I2 with a tiny I1 mesial to it; the lower incisor was identified as i2 as it occludes with upper I2. DI2, deciduous upper incisor; di2, deciduous lower incisor; I2, upper incisor; i2, lower incisor; M1, upper first molar; m1, lower first molar; M2, upper second molar; m2, lower second molar; P3, upper third premolar; P4, upper fourth premolar; p4, lower fourth premolar.

Extended Data Fig. 3 Reconstruction of the skull of V. diplomylos (IMMNH-PV01699A and B).

a, Skull in lateral view. b, Cranium in dorsal view. ce, Left mandible in occlusal (c), lateral (d) and medial (e) views. an, angular process; cc, coronoid crest; co, mandibular condyle; cp, coronoid process; DI2, deciduous upper incisor; di2, deciduous lower incisor; ethf, ethmoidal foramen; fr, frontal; iof, infraorbital foramen; ju, jugal; lac, lacrimal; m1, lower first molar; m2, lower second molar; maf, masseteric fossa; mas, mandibular symphysis; mef, mental foramen; mf, mandibular foramen; mx, maxilla; na, nasal; P3, upper third premolar; p4, lower fourth premolar; pa, parietal; pmx, premaxilla; ptf, pterygoid fossa; smx, septomaxilla; sq, squamosal; vc, ventral crest.

Extended Data Fig. 4 Reconstructions of auditory apparatus in V. diplomylos on the basis of the holotype versus the referred specimen.

a, Reconstruction on the basis of the Vilevolodon holotype4, which has more-fragmentary auditory elements: the incus is shown with a trochlea and dorsal plate (as in Morganucodon) (Fig. 3a) in a rostrocaudal incudomallear articulation, and the malleus includes ossified Meckel’s cartilage and surangular. b, c, Reconstruction on the basis of the Vilevolodon referred specimen (IMMNH-PV01699A) with well-preserved auditory elements in ventral (b) and dorsal (c) views: the incus is flat and has a dorsoventral incudomallear articulation, and the malleus does not have an ossified Meckel’s cartilage or surangular. Colours for the auditory elements are as in Fig. 1.

Extended Data Fig. 5 Reinterpretation of auditory apparatus of A. allinhopsoni.

ac, e, h, Arboroharamiya allinhopsoni, left auditory apparatus. a, Photograph of the holotype in ventral view (derived from extended data figure 5a of ref. 3). b, c, Reconstruction in ventral (b) and dorsal (c) views (modified from extended data figure 5e, f of ref. 3). e, h, The reconstruction proposed in this Article, in ventral (e) and dorsal (h) views (Supplementary Information). d, g, Ornithorhynchus anatinus (Carnegie Museum 50815), left auditory apparatus rendered from computed tomography scans in ventral (d) and dorsal (g) views. f, i, Vilevolodon diplomylos (IMMNH-PV01699A), left auditory apparatus in ventral (f) and dorsal (i) views. The crus breve of the incus in e and h is based on ref. 17. Colours for the auditory elements are as in Fig. 1; stapes in purple; tympanic membrane (grey) is reconstructed on the ventral views in b, d35,68, f. ac, anterior crus of ectotympanic; al, anterior limb of ectotympanic; apm, anterior process of malleus; asa, anterior process of surangular; cb, crus breve; fv, fenestra vestibuli; gf, glenoid fossa; hy, hyoid element; ic, incus; lp, lenticular process; mab, mallear body; mm, manubrium of malleus; mp, medial process of malleus; oc, occipital condyle; pc, posterior crus of ectotympanic; pf, perilymphatic foramen; pic, stapedial process of incus; pism, process for insertion of stapedius muscle of stapes; pl, posterior limb of ectotympanic; pm, promontorium; ppr, paroccipital process of petrosal; prs, posterior ridge of surangular; pss, posterior surface of surangular; ptp, posttympanic process of squamosal; rl, reflected lamina of ectotympanic; rtm, ridge for attachment for anterior part of tympanic membrane; sa, surangular; sf, stapedius fossa; spg, groove for stapedial artery; st, stapes; tm, transverse part of malleus; ts, tympanic sulcus; ty-d, lateral ectotympanic part presumably equivalent to dorsal part of angular; ty-r, ectotympanic part presumably equivalent to reflected lamina.

Extended Data Fig. 6 Reinterpretation of ectotympanic of Qishou and Arboroharamiya.

ac, Qishou jintzang, the so-called left ectotympanic in ventral (a) and dorsal (b) views, derived from figure 8c, d of ref. 17; interpreted here as the left malleus with broken anterior process and incus in dorsal view (c). d, Arboroharamiya allinhopsoni, the so-called left ectotympanic in ventral view, derived from figure 3 of ref. 17. e, f, Tachyglossus aculeatus (Carnegie Museum 50812), isolated left ectopterygoid bone and the left basicranium in ventral view. g, Arboroharamiya jenkinsi, the so-called left ectotytmpanic in ventral view, derived from figure 7c of ref. 17. h, i, Ornithorhynchus anatinus (Carnegie Museum 50815), isolated left ectopterygoid bone and the left basicranium in ventral view. Colours for the auditory elements are as in Fig. 1. api, anterior prominence of incus; apm(br), anterior process of malleus (broken); arty, anterior edge of ectotympanic; cb, crus breve; cfm, contact area for malleus; ep, ectopterygoid; frt, fracture; mm, manubrium of malleus; prty, posterior edge of ectotympanic; rtm, ridge for attachment of anterior part of tympanic membrane; sp, stapedial process of incus; ty-d, lateral ectotympanic part presumably equivalent to dorsal part of angular; ty-r, ectotympanic part presumably equivalent to reflected lamina.

Extended Data Fig. 7 Simplified strict-consensus parsimony tree, highlighting relationships and relative ages of key mammalian groups.

The full tree is shown in Extended Data Fig. 8. Nodes are not time-calibrated. A, Allotheria; C, Cladotheria; El, Eleutherodontidae; Eu, Eutriconodonta; G, Gondwanatheria; Ha, Haramiyida; M, Mammalia; Mf, Mammaliaformes; Mt, Multituberculata; Sp, Spalacotherioidea; T, Theria; Tr, Trechnotheria.

Extended Data Fig. 8 Full parsimony consensus tree.

The dataset comprises 130 taxa and 509 morphological characters. The strict consensus tree of 30 equally most-parsimonious trees was found in TNT47. Consensus tree length = 2,871; consistency index = 0.300; retention index = 0.784. The simplified version of this consensus tree is presented in Extended Data Fig. 7. The allotherians (Haramiyavia, Cifelliodon, haramiyidans, multituberculates and gondwanatherians) are highlighted in blue. A, Allotheria; Au, Australosphenida; C, Cladotheria; El, Eleutherodontidae; Eu, Eutriconodonta; G, Gondwanatheria; Ha, Haramiyida; M, Mammalia; Mf, Mammaliaformes; Mt, Multituberculata; Sp, Spalacotherioidea; T, Theria; Tr, Trechnotheria.

Extended Data Fig. 9 Bayesian consensus tree.

Fifty-per-cent majority rule consensus tree for Mesozoic mammals from a tip-dated analysis using Bayesian inference in MrBayes64. Tip-dating analysis confirms that mammals originated in the late Triassic (213.82 million years ago (207.98, 221.48 95% highest posterior density intervals)); however, the topology is different from the strict-consensus tree inferred from the parsimony analysis69. Allotherians are in blue.

Extended Data Fig. 10 Ontogeny of auditory ossicles in extant therian mammals.

a, Right malleus, incus and gonial on postnatal days 0, 12 and 30 of the didelphid marsupial Monodelphis domestica in medial view (redrawn from ref. 39), anterior to the left and dorsal to the top. Incus is initially dorsal to the malleus and shifts caudally in later ontogenetic stages. b, Left malleus of the juvenile felid carnivoran Felis pardus (Carnegie Museum of Natural History (CM) 21006) in ventral view, medial to the left and anterior to the top, showing the ossiculum accessorium mallei70 or processus internus praearticularis71. c, Left ear region of newborn golden mole Amblysomus corriae in ventral view, medial to the left and anterior to the top (modified from ref. 72), showing the small, rod-like dermal element medial to the gonial that is posited to be the surangular. Colours for the ossicles are as in Fig. 1.

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Supplementary Information

This file contains a table of contents on extended data figures 1-10 and supplementary information parts A-G, and Supplementary Information Parts A-G.

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Wang, J., Wible, J.R., Guo, B. et al. A monotreme-like auditory apparatus in a Middle Jurassic haramiyidan. Nature 590, 279–283 (2021). https://doi.org/10.1038/s41586-020-03137-z

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