Abstract
Among Artiodactylamorpha, dichobunoids are some of the oldest fossil species that have been associated with Artiodactyla, the crown clade that includes hippopotamids, camelids, suoids, ruminants, and cetaceans. These important fossil species are known from early Eocene rocks of North America, Europe, and Asia, but their phylogenetic position has yet to be well resolved. Before generating such a phylogeny, it is first critical to document all of the anatomy of known dichobunoid fossils. Here we use CT scans to describe previously undescribed anatomy of the petrosal bone, a complex part of the mammalian skull that contains many variable and phylogenetically informative features. Results show that these extinct species share a number of features that are not documented in modern species including a lateral process of the epitympanic wing constituting the medial border of the piriform fenestra, and a tegmen tympani foramen that may have given passage to the ramus superior of the stapedial artery. Future comprehensive phylogenetic studies may show that many of these characters are plesiomophic for Artiodactylamopha. Some species (Diacodexis, Homacodon and ?Helohyus) exhibit a dorsolateral exposure of the mastoid region of the petrosal on the temporal part of the cranium. This uncommon feature has, to our knowledge, not been reported in another euungulate group.
Similar content being viewed by others
References
Asher RJ, McKenna MC, Emry RJ, Tabrum AR, Kron DG (2002) Morphology and relationships of Apternodus and other extinct zalambdodont placental mammals. Bull Am Mus Nat Hist 273:1-117
Asher RJ, Bennett N, Lehmann T (2009) The new framework for understanding placental mammal evolution. BioEssays 31:853-864
BioChroM’97 (1997) Synthèses et tableaux de corrélations. In: Aguilar J-P, Legendre S, Michaux J (eds) Actes du Congrès BiochroM’97. Mémoires et Travaux de l’Institut Pratique des Hautes-Études, Institut de Montpellier 21, Montpellier, pp. 769-805
Bryant HN, Russell AP (1992) The role of phylogenetic analysis in the inference of unpreserved attributes of extinct taxa. Phil Trans R Soc Lond B Biol Sci 337:405-418
Cifelli RL (1982) The petrosal structure of Hyopsodus with respect to that of some other ungulates, and its phylogenetic implications. J Paleontol 56:795-805
Coombs MC, Coombs WP (1982) Anatomy of the ear region of four Eocene artiodactyls, Gobiohyus, ?Helohyus, Diacodexis and Homacodon. J Vertebr Paleontol 2:219-236
De Queiroz K (2007) Toward an integrated system of clade names. Syst Biol 56:956-974
Dechaseaux C (1969) Moulages endocrâniens d’artiodactyles primitifs, essai sur l’histoire du néopallium. Ann Paléontol (Vertébr) 55:195-248
Dechaseaux C (1974) Artiodactyles primitifs des phosphorites du Quercy. Ann Paléontol (Vertébr) 60:59-100
Gannon PJ, Eden AR, Laitman JT (1988) The subarcuate fossa and cerebellum of extant primates: comparative study of a skull-brain interface. Am J Phys Anthropol 77:143-164
Gatesy J, Geisler JH, Chang J, Buell C, Berta A, Meredith RW (2012) A phylogenetic blueprint for a modern whale. Mol Phylogen Evol 66(2):479-506
Gazin LC (1965) A study of the early Tertiary condylarthran mammal Meniscotherium. Smithsonian Misc Collect 149(4-2):1-98
Geisler JH, Luo ZX (1998) Relationships of Cetacea to terrestrial ungulates and the evolution of cranial vasculature in Cete. In: Thewissen JGM (ed) The Emergence of Whales, Evolutionary Patterns in the Origin of Cetacea. Plenum Press, New York, pp 163- 212
Geisler JH, Theodor JM (2009) Hippopotamus and whale phylogeny. Nature 458(7236):E1-4
Geisler JH, Theodor JM, Uhen MD, Foss SE (2007) Phylogenetic relationships of Cetaceans to Terrestrial Artiodactyls. In: Prothero DR, Foss S (eds) The Evolution of Artiodactyla. John Hopkins University Press, Baltimore, pp 319-31
Giannini NP, Wible JR, Simmons NB (2006) On the cranial osteology of Chiroptera. I. Pteropus (Megachiroptera, Pteropodidae). Bull Am Mus Nat Hist 295:1-134
Gingerich PD (1989) New earliest Wasatchian mammalian fauna from Eocene of northwestern Wyoming, composition and diversity in a rarely sampled highfloodplain assemblage. Univ Mich Pap Paleontol 28:1-97
Hunt RM Jr (1974) The auditory bulla in Carnivora: an anatomical basis for reappraisal of carnivore evolution. J Morphol 143:21-76
Hunt RM Jr (2001) Basicranial anatomy of the living linsangs Prionodon and Poiana (Mammalia, Carnivora, Viverridae), with comments on the early evolution of aeluroid carnivorans. Am Mus Novitates 3330:1-24
Ladevèze S (2007) Petrosal bones of metatherian mammals from the late Paleocene of Itaboraí (Brazil), and a cladistic analysis of petrosal features in metatherians. Zool J Linn Soc 150:85-115
Ladevèze S, Missiaen P, Smith T (2010) First skull of Orthaspidotherium edwardsi (Mammalia, “Condylarthra”) from the late Paleocene of Berru (France) and phylogenetic affinities of the enigmatic European family Pleuraspidotheriidae. J Vertebr Paleontol 30:1559-1578
Luo Z, Gingerich PD (1999) Terrestrial Mesonychia to aquatic Cetacea: transformation of the basicranium and evolution of hearing in whales. Univ Mich Pap Paleontol 31:1-98
MacIntyre GT (1972) The trisulcate petrosal pattern of mammals. In: Dobzhansky T, Hecht M, Steere WC (eds) Evolutionary Biology, Vol. 6. Appleton- Century-Crofts, New York, pp 275–303
MacPhee RDE (1981) Auditory regions of primates and eutherian insectivores: morphology, ontogeny, and character analysis. Contrib Primatol 18:1-282
McDowell SB Jr (1958) The Greater Antillean insectivores. Bull Am Mus Nat Hist 115:117-214
McKenna MC, Bell SK (1997) Classification of Mammals Above the Species Level. Columbia University Press, New York
Mead JG, Fordyce RE (2009) The therian skull: a lexicon with emphasis on the odontocetes. Smithsonian Contrib Zool 627:1-248
O’Leary MA (2010). An anatomical and phylogenetic study of the osteology of the petrosal of extant and extinct artiodactylans (Mammalia) and relatives. Bull Am Mus Nat Hist 335:1-206
O’Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, Giannini NP et al. (2013) The placental mammal ancestor and the Post-K-Pg radiation of placental. Science 339:662-667
O’Leary MA, Gatesy J (2008) Impact of increased character sampling on the phylogeny of Cetartiodactyla (Mammalia): combined analysis including fossils. Cladistics 24:397-442
Orliac MJ (2012) Osteology of the petrosal bone of Suoidea (Artiodactyla, Mammalia). J Syst Palaeontol 11(8):925-945
Orliac MJ, Ducrocq S (2011) Eocene raoellids (Mammalia, Cetartiodactyla) outside the Indian Subcontinent, palaeogeographical implications. Geol Mag 149:80-92
Presley R (1979) The primitive course of the internal carotid artery in mammals. Acta Anat 103:238-244
Rose KD (2006) The Beginning of the Age of Mammals. The John Hopkins University Press, Baltimore
Russell DE, Thewissen JGM, Sigogneau-Russel D (1983) A new dichobunoid artiodactyl (Mammalia) from the Eocene of North-West Pakistan – II Cranial osteology. Proc K Ned Akad B Phys 3:285-300
Sisson S (1911) A text-book of veterinary anatomy. WB Saunders, Philadelphia
Spaulding M, O’Leary MA, Gatesy J (2009) Relationships of Cetacea (Artiodactyla) among mammals: increased taxon sampling alters interpretations of key fossils and character evolution. PloS ONE 4(9):1-14
Theodor JM (2010) Micro-computed tomographic scanning of the ear region of Cainotherium: character analysis and implications. J Vertebr Paleontol 30(1):236-243
Theodor JM, Erfurt J, Métais G (2007) The earliest artiodactyls. In: Prothero DR, Foss S (eds) The Evolution of Artiodactyla. John Hopkins University Press, Baltimore, pp 32-58
Thewissen JGM, Cooper LN, Clementz MT, Bajpai S, Tiwari BN (2007) Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 6343(450):1190-1195
Thewissen JGM, Cooper LN, George JC, Bajpai S (2009) From land to water: the origin of whales, dolphins, and porpoises. Evo Edu Outreach 2:272-288
Wible JR (1986) Transformations in the extracranial course of the internal carotid artery in mammalian phylogeny. J Vertebr Paleontol 6:313-325
Wible JR (2003) On the cranial osteology of the short-tailed opposum Monodelphis brevicaudata (Didelphidae, Marsupialia). Ann Carnegie Mus 72:137-202
Wible JR, Gaudin TJ (2004) On the cranial osteology of the yellow armadillo Euphractus sexcinctus (Dasypodidae, Xenarthra, Placentalia). Ann Carnegie Mus 73:117-196
Wible JR, Rougier GW, Novacek MJ, McKenna MC, Dashzeveg D (1995) A mammalian petrosal from the Early Cretaceous of Mongolia: implications for the evolution of the ear region and mammliamorph interrelationships. Am Mus Novitates 3149:1-19
Wible JR, Rougier GW, Novacek MJ, McKenna (2001) Earliest eutherian ear region: a petrosal referred to Prokennalestes from the Early Cretaceous of Mongolia. Am Mus Novitates 3322:1-44
Witmer LM (1995) The Extant Phylogenetic Bracket and the importance of reconstructing soft tissues in fossils. In: Thomason JJ (ed) Functional Morphology in Vertebrate Paleontology. Cambridge University Press, New York, pp 19-33
Acknowledgement
We thank R. O’Leary (AMNH), Meng Jin (AMNH), C. Argot (MNHN), and B. Marandat (UM2) for access to the collections, J. Thostenson, R. Rudolph, and M. Hill for acquisition of raw CT data at the AMNH, and A-L Charruault and R. Lebrun for acquisition of raw CT scan data at the UM2. We are grateful to J Wible, J Geisler, and one anonymous reviewer for their enriching comments on earlier versions of the manuscript. We also thank the American Museum of Natural History for use of the high resolution CT-scanner (NSF MR1–R2 0959384 to N. Landman, D. Ebel, and D. Frost), and the Montpellier Rio Imaging platform (Montpellier, France) for use of their Skyscan machine. This is ISE-M publication 201X-XX. This research was supported by the ANR funding project Palasiafrica, headed by L. Marivaux.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Fig. S1
Paired stereo images of the petrosal bone of Diacodexis ilicis (AMNH 16141) in A) ventrolateral, B) dorsomedial, C) medioventral, and D) anterior views. Scale = 2 mm. (JPEG 177 kb)
Fig. S2
Paired stereo images of the petrosal bone of Acotherulum saturninum (MNHM Qu 16366) in A) ventrolateral, B) dorsomedial, C) medioventral, and D) anterior views. Scale = 2 mm. (JPEG 198 kb)
Fig. S3
Paired stereo images of the petrosal bone of Dichobune leporina (MNHN Qu 16586) in A) ventrolateral, B) dorsomedial, C) medioventral, and D) anterior views. Scale = 2 mm. (JPEG 178 kb)
Fig. S4
Paired stereo images of the petrosal bone of Homacodon vagans (USNM 482369) in A) ventrolateral, B) dorsomedial, C) medioventral, and D) anterior views. Scale = 5 mm. (JPEG 223 kb)
Fig. S5
Paired stereo images of the petrosal bone of ?Helohyus plicodon (USNM 13079) in A) ventrolateral, B) dorsomedial, C) medioventral, and D) anterior views. Scale = 5 mm. (JPEG 226 kb)
Fig. S6
Paired stereo images of the petrosal bone of Gobiohyus orientalis (USNM 26277) in A) ventrolateral, B) dorsomedial, C) medioventral, and D) anterior views. Scale = 2 mm. (JPEG 195 kb)
Fig. S7
Paired stereo images of the petrosal bone of A) Diacodexis ilicis (AMNH 16141); B) Acotherulum saturninum (MNHM Qu 16366); C) Homacodon vagans (USNM 482369); D) Dichobune leporina (MNHN Qu 16586); E) ?Helohyus plicodon (USNM 13079); and F) Gobiohyus orientalis (USNM 26277) in ventrolateral view. Scale = 2 mm for A, B, D, F and scale = 5 mm for C and E. (JPEG 325 kb)
Fig. S8
Paired stereo images of the petrosal bone of A) Diacodexis ilicis (AMNH 16141); B) Acotherulum saturninum (MNHM Qu 16366); C) Homacodon vagans (USNM 482369); D) Dichobune leporina (MNHN Qu 16586); E) ?Helohyus plicodon (USNM 13079); and F) Gobiohyus orientalis (USNM 26277) in dordomedial view. Scale = 2 mm for A, B, D, F and scale = 5 mm for C and E. (JPEG 343 kb)
Fig. S9
Paired stereo images of the petrosal bone of A) Diacodexis ilicis (AMNH 16141); B) Acotherulum saturninum (MNHM Qu 16366); C) Homacodon vagans (USNM 482369); D) Dichobune leporina (MNHN Qu 16586); E) ?Helohyus plicodon (USNM 13079); and F) Gobiohyus orientalis (USNM 26277) in anterior view. Scale = 2 mm for A, B, D, F and scale = 5 mm for C and E. (JPEG 262 kb)
Fig. S10
Paired stereo images of the petrosal bone of A) Diacodexis ilicis (AMNH 16141); B) Acotherulum saturninum (MNHM Qu 16366); C) Homacodon vagans (USNM 482369); D) Dichobune leporina (MNHN Qu 16586); E) ?Helohyus plicodon (USNM 13079); and F) Gobiohyus orientalis (USNM 26277) in medioventral view. Scale = 2 mm for A, B, D, F and scale = 5 mm for C and E. (JPEG 273 kb)
Fig. S11
Homacodon vagans (USNM 482369) left petrosal in situ, ventral view. Scale = 1 cm. (JPEG 114 kb)
Fig. S12
Gobiohyus orientalis (USNM 26277) right petrosal in situ (reversed to be shown from left side), ventral view. Scale = 1 cm. (JPEG 106 kb)
Fig. S13
?Helohyus plicodon (USNM 13079) right petrosal in situ (reversed to be shown from left side), ventral view. Scale = 1 cm. (JPEG 120 kb)
Fig. S14
3D reconstruction of endocranial features of Homacodon vagans (USNM 482369): endocranial cast in pink, tegmen tympani canal in red. The white dotted line corresponds to the petrosal outlines. Scale = 1 cm. (JPEG 27 kb)
Appendices
Appendix 2
Appendix 1
Rights and permissions
About this article
Cite this article
Orliac, M.J., O’Leary, M.A. Comparative Anatomy of the Petrosal Bone of Dichobunoids, Early Members of Artiodactylamorpha (Mammalia). J Mammal Evol 21, 299–320 (2014). https://doi.org/10.1007/s10914-014-9254-9
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10914-014-9254-9