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The Evolution of the Maxillary Canal in Probainognathia (Cynodontia, Synapsida): Reassessment of the Homology of the Infraorbital Foramen in Mammalian Ancestors

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Abstract

In mammals, the infraorbital canal provides a passage for the infraorbital ramus of the maxillary branch of the trigeminal nerve. The infraorbital nerve ensures tactile sensitivity of the upper teeth and face between the eye and upper lip and, more significantly, the innervation of mystacial vibrissae (whiskers). In contrast, most non-mammalian synapsids display a more “reptilian-like” ancestral condition in which a long and ramified maxillary canal completely enclosed the infraorbital nerve along with other branches of the trigeminal nerve. The phylogenetic transition from the ancestral “reptilian-like” to the derived “mammal-like” condition has been hypothesized to occur at the base of the Probainognathia clade. Using μCT and synchrotron scanning, this study aims to document this transition in detail by focusing on a sample of non-mammalian probainognathian cynodonts and early mammaliaforms. We find that the mammalian condition is the result of a gradual shortening of the maxillary canal, which enabled the infraorbital nerve to ramify within the soft tissues of the face. Mobile whiskers became possible only after the mammalian infraorbital nerve had evolved, which suggest that these structures appeared in Probainognathus and more derived cynodonts. Finally a foramen located on the ventral margin of the lacrimal bone, which has been often homologized with the infraorbital foramen of derived Probainognathia and early Mammaliaformes, is most probably homologous to the mammalian zygomaticofacial foramen.

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Acknowledgments

The authors thank Cesar Leandro Schultz, Marina Bento Soares, José Fernando Bonaparte, Bhart-Anjan Bhullar, and Timothy Rowe for access to CT data. Specimen UFRGS-PV-1043-T was scanned at Fachhochschule Aalen with the support of the Alexander von Humboldt Foundation. We acknowledge the European Synchrotron Radiation Facility for provision of synchrotron radiation facilities and we would like to thank Paul Tafforeau for assistance in using beamline ID19. We thank John Wible, Ricardo Araújo, and an anonymous reviewer whose comments helped to improve the manuscript. This research was conducted with financial support from the Claude Leon Foundation; PAST and its scatterlings projects; the NRF African Origins Platform; and the DST-NRF Centre of Excellence in Palaeosciences (CoE in Palaeosciences). Opinions expressed and conclusions arrived at, are those of the authors and are not necessarily to be attributed to the CoE in Paleosciences. The authors declare no competing interest.

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Authors and Affiliations

  1. Evolutionary Studies Institute (ESI) and School of Geosciences, University of the Witwatersrand, PO Wits, Johannesburg, 2050, South Africa

    Julien Benoit & Bruce S. Rubidge

  2. Abteilung Messelforschung und Mammalogie, Senckenberg Forschungsinstitut und Naturmuseum Frankfurt, Senckenberganlage 25, 60325, Frankfurt am Main, Germany

    Irina Ruf

  3. Department of Geology & Geophysics, Yale University, New Haven, CT, USA

    Juri A. Miyamae

  4. European Synchrotron Radiation Facility, Beamline ID19, 71 rue des Martyrs, 38000, Grenoble, France

    Vincent Fernandez

  5. Imaging and Analysis Centre, Natural History Museum, Cromwell Road SW7, London, 5BD, UK

    Vincent Fernandez

  6. Departamento de Paleontologia e Estratigrafia, Institituto de Geociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil

    Pablo Gusmão Rodrigues

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  1. Julien Benoit
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  2. Irina Ruf
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  3. Juri A. Miyamae
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  4. Vincent Fernandez
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  5. Pablo Gusmão Rodrigues
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  6. Bruce S. Rubidge
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Correspondence to Julien Benoit.

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Benoit, J., Ruf, I., Miyamae, J.A. et al. The Evolution of the Maxillary Canal in Probainognathia (Cynodontia, Synapsida): Reassessment of the Homology of the Infraorbital Foramen in Mammalian Ancestors. J Mammal Evol 27, 329–348 (2020). https://doi.org/10.1007/s10914-019-09467-8

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  • DOI: https://doi.org/10.1007/s10914-019-09467-8

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