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Life in Burrows Channelled the Morphological Evolution of the Skull in Rodents: the Case of African Mole-Rats (Bathyergidae, Rodentia)

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Abstract

African mole-rats are fossorial rodents that consist of five chisel-tooth digging genera (Heterocephalus, Heliophobius, Georychus, Fukomys, and Cryptomys) and one scratch digger (Bathyergus). They are characterized by striking physiological, morphological, and behavioral adaptations intimately related to their subterranean life. The influence of their mode of life in shaping the cranial morphology has yet to be evaluated in comparison to other Ctenohystrica, especially fossorial genera, which include the subterranean genera Spalacopus and Ctenomys. In our study, we seek to determine to what extent subterranean life affects the morpho-functional properties of the skull among fossorial ctenohystricans. 3D geometric morphometric analyses were performed on 277 skulls, encompassing 63 genera of Ctenohystrica, and complemented by biomechanical studies. African mole-rats and other subterranean Ctenohystrica, especially chisel-tooth diggers, have a short snout, a wide cranium with enlarged zygomatic arches, and a strongly hystricognathous mandible. Even if convergences are also manifest between most fossorial Ctenohystrica, subterranean rodents departed from the main ctenohystrican allometric trends in having a skull shape less size-dependent, but under stronger directional selection with intense digging activity as a major constraint. African mole-rats, notably chisel-tooth diggers, show important mechanical advantage for the temporalis muscles favoring higher forces at the bite point, while mechanical advantage of the superficial masseter muscles is lower compared to other Ctenohystrica. If subterranean species can be clearly discriminated based on their skull morphology, the intrinsic mosaic of anatomical characters of each genus (e.g., skull, teeth, and muscles) can be understood only in the light of their ecology and evolutionary history.

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Acknowledgments

We are grateful to R. Portela Miguez from the National History Museum of London, and to P. Mein from the Université Lyon 1 for providing access to their collections of rodents. We thank R. Lebrun (Institut des Sciences de l’Evolution de Montpellier) who kindly gave us access to MeshTools and Morphotools, and for his help during analyses, and to P.-H. Fabre (Institut des Sciences de l’Evolution de Montpellier) who allowed us to use his phylogenetic data on Ctenohystrica for PIC analyses. We also acknowledge P. Cox and A. McIntosh (Hull York Medical School) for fruitful discussions on African mole-rats and associated musculatures. Thanks to C. Charles (Institut de Génomique Fonctionnelle de Lyon, Structure Fédératrice de Recherche BioSciences UMS3444/US8, Gerland - Lyon Sud) for giving access to facilities associated with X-ray microtomography. The manuscript benefited from the constructive comments of two anonymous reviewers, and of the editor-in-chief, John Wible. This work was supported by La Fondation des Treilles (www.les-treilles.com, grant to H.G.R.), and by the Grant Agency of Czech Republic, n. 41-14-36098G (R.S.).

Compliance with Ethical Standards

The authors declare that they have no conflict of interest. This article does not contain any studies with human participants or animals performed by any of the authors. Informed consent was obtained from all individual participants included in the study.

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  1. Helder Gomes Rodrigues

    Present address: Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements (CR2P), UMR CNRS 7207, CP38, Muséum national d’Histoire naturelle, Univ Paris 6, 8 rue Buffon, 75005, Paris, France

Authors and Affiliations

  1. Department of Zoology, Faculty of Science, University of South Bohemia, Branišovská 31, České Budějovice, 37005, Czech Republic

    Radim Šumbera

  2. Laboratoire de Paléontologie, Institut des Sciences de l’Évolution de Montpellier (CNRS, UM, IRD, EPHE), c.c. 064, Université Montpellier, Place Eugène Bataillon, 34095, Montpellier Cedex 05, France

    Lionel Hautier

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Correspondence to Helder Gomes Rodrigues.

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Gomes Rodrigues, H., Šumbera, R. & Hautier, L. Life in Burrows Channelled the Morphological Evolution of the Skull in Rodents: the Case of African Mole-Rats (Bathyergidae, Rodentia). J Mammal Evol 23, 175–189 (2016). https://doi.org/10.1007/s10914-015-9305-x

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