Skip to main content

Advertisement

SpringerLink
Log in

Evolution Towards Fossoriality and Morphological Convergence in the Skull of Spalacidae and Bathyergidae (Rodentia)

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

Rodents show a wide range of anatomical, physiological, and behavioral adaptations to life underground. Cranial and postcranial bone morphologies are deeply impacted by the modes of digging, which can involve either incisors or claws. However, the morphological variation of these elements still needs to be accurately quantified to assess the degree of specializations of the fossorial rodent families in regards to their respective evolution. Here, we focus on the morpho-functional characteristics of the masticatory apparatus in two families of subterranean rodents, the Spalacidae and Bathyergidae. We quantify skull shape in five spalacid genera using geometric morphometric methods, as well as biomechanical estimates for adductor muscles, which are compared with data previously published on bathyergids. We show that skull shape of spalacids has a greater disparity and lower biomechanical estimates than bathyergids, in which the fossorial activity, notably chisel-tooth digging, more significantly impacted the evolution of the skull. Among spalacids, Spalax shows the most extreme specializations to life underground and displays the highest number of morphological convergences with chisel-tooth digging bathyergids, especially regarding its cranial shape and high biomechanical estimate for the temporalis muscle. Fewer morphological convergences were observed between other spalacids and bathyergids. Different evolutionary histories can potentially explain discrepancies observed between the two families, the first bathyergid morphological adaptations to fossorial life being much older than those of spalacids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Adams DC, Collyer M, Kaliontzopoulou A (2020) geomorph: Geometric Morphometric Analyses of 2D/3D Landmark Data. Version 3.2.1. R Package

  • Agrawal VC (1967) Skull adaptations in fossorial rodents. Mammalia 31:300-312

    Article  Google Scholar 

  • Baverstock H, Jeffery NS, Cobb SN (2013) The morphology of the mouse masticatory musculature. J Anat 223:46–60

    Article  PubMed Central  PubMed  Google Scholar 

  • Begall S, Burda H, Schleich CE (2007) Subterranean Rodents: News from Underground. Springer, Berlin Heidelberg New York

    Book  Google Scholar 

  • Bennett NC, Faulkes CG (2000) African Mole-rats: Ecology and Eusociality. Cambridge University Press, Cambridge

    Google Scholar 

  • Bookstein FL (1991) Morphometric Tools for Landmark Data Geometry and Biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Bryja J, Konvičková H, Bryjová A, O. Mikula R, Makundi WN, Chitaukali, Šumbera R (2018) Differentiation underground: range-wide multilocus genetic structure of the silvery mole-rat does not support current taxonomy based on mitochondrial sequences. Mammal Biol 93:82–92. https://doi.org/10.1016/j.mambio.2018.08.006

    Article  Google Scholar 

  • Burda H (2006) Ear and eye in subterranean mole-rats, Fukomys anselli (Bathyergidae) and Spalax ehrenbergi (Spalacidae): progressive specialisation or regressive degeneration? Animal Biol 56:475–486. https://doi.org/10.1163/157075606778967847

    Article  Google Scholar 

  • Casanovas-Vilar I, Van Dam J (2013) Conservatism and adaptability during squirrel radiation: what is mandible shape telling us? PLoS One 8:e61298

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Conover WJ, Iman RL (1981) Rank transformation as a bridge between parametric and nonparametric statistics. Am Stat 35:124–129

    Google Scholar 

  • Cook JA, Lessa EP, Hadly EA (2000) Paleontology, phylogenetic patterns, and macroevolutionary processes in subterranean rodents. In: Lacey EA, Patton JL, Cameron GN (eds) Life Underground: The Biology of Subterranean Rodents. University of Chicago Press, Chicago, pp 332–369

    Google Scholar 

  • Cox PG, Faulkes CG (2014) Digital dissection of the masticatory muscles of the naked mole-rat, Heterocephalus glaber (Mammalia, Rodentia). PeerJ 2:e448.

    Article  PubMed Central  PubMed  Google Scholar 

  • Cox PG, Faulkes CG, Bennett NC (2020) Masticatory musculature of the African mole-rats (Rodentia: Bathyergidae). PeerJ 8:e8847. https://doi.org/10.7717/peerj.8847

    Article  PubMed Central  PubMed  Google Scholar 

  • Cox PG, Jeffery N (2011) Reviewing the morphology of the jaw-closing musculature in squirrels, rats, and guinea pigs with contrast-enhanced microCT. Anat Rec 294:915–928

    Article  Google Scholar 

  • Cox PG, Jeffery N (2015) The muscles of mastication and the function of the medial pterygoid. In: Cox PG, Hautier L (eds) Evolution of the Rodents: Advances in Phylogeny, Functional Morphology and Development. Cambridge University Press, Cambridge, pp 350–372

    Chapter  Google Scholar 

  • de Bruijn H, Bosma AA, Wessels W (2015) Are the Rhizomyinae and the Spalacinae closely related? Contradistinctive conclusions between genetics and palaeontology. Palaeobiodivers Palaeoenviron 95:257–269. https://doi.org/10.1007/s12549-015-0195-y

    Article  Google Scholar 

  • Druzinsky RE (2010) Functional anatomy of incisal biting in Aplodontia rufa and sciuromorph rodents. Part 1: masticatory muscles, skull shape and digging. Cells Tissues Organs 191:510–522

    Article  PubMed Central  PubMed  Google Scholar 

  • Fang X, Nevo E, Han L, Levanon EY., Zhao J, Avivi A, Larkin D, Jiang X, Feranchuk S, Zhu Y, Fishman A (2014) Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax. Nature Commun 5:3966

  • Faulkes CG, Verheyen E, Verheyen W, Jarvis JUM, Bennett NC (2004) Phylogeographical patterns of genetic divergence and speciation in African mole-rats (Family: Bathyergidae). Mol Ecol 13:613–629

    Article  CAS  PubMed  Google Scholar 

  • Flynn LJ (2009) Chapter 4: The antiquity of Rhizomys and independent acquisition of fossorial traits in subterranean muroids. Bull Am Mus Nat Hist 331:128–156

  • Flynn LJ, Jacobs LL, Lindsay EH (1985) Problems in muroid phylogeny. Relationship to other rodents and origin of major groups. In: Luckett WP, Hartenberger J-L (eds) Evolutionary Relationships among Rodents. A Multidisciplinary Analysis. NATO ASI Series A: Life Sciences, Plenum Press, Paris, pp 589–616

  • Ginot S, Herrel A, Claude J, Hautier L (2019) Morphometric models for estimating bite force in Mus and Rattus: mandible shape and size perform better than lever-arm ratios. J Exp Biol 222:jeb204867. https://doi.org/10.1242/jeb.204867

  • Gomes Rodrigues H (2015) The great disparity of dental structures and dynamics in rodents: new insights into their ecological diversity. In: Cox PG, Hautier L (eds) Evolution of the Rodents: Advances in Phylogeny, Functional Morphology and Development. Cambridge University Press, Cambridge, pp 424–447

    Chapter  Google Scholar 

  • Gomes Rodrigues H, Šumbera R, Hautier L (2016) Life in burrows channelled the morphological evolution of the skulls in rodents: the case of African mole-rats (Bathyergidae, Rodentia). J Mammal Evol 23:175–189

    Article  Google Scholar 

  • Hadid Y, Németh A, Snir S, Pavlíček T, Csorba G, Kázmér M, Major Á, Mezhzherin S, Rusin M, Coşkun Y, Nevo E (2012) Is evolution of blind mole rats determined by climate oscillations? PLoS One 7:e30043. https://doi.org/10.1371/journal.pone.0030043

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hautier L, Lebrun R, Cox PG (2012) Patterns of covariation in the masticatory apparatus of hystricognathous rodents: implications for evolution and diversification. J Morphol 273:1319–1337

    Article  PubMed  Google Scholar 

  • Hildebrand M (1985) Digging of quadrupeds. In: Hildebrand M, Bramble DM, Liem KL, Wake DB (eds) Functional Vertebrate Morphology. Harvard University Press, Cambridge, pp 89–109

    Chapter  Google Scholar 

  • He Y, Hu S, Ge D, Yang Q, Connor T, Zhou C (2020) Evolutionary history of Spalacidae inferred from fossil occurrences and molecular phylogeny. Mammal Rev 50:11–24. https://doi.org/10.1111/mam.12170

    Article  Google Scholar 

  • Heth G, Frankenberg E, Raz A, Nevo E (1987) Vibrational communication in subterranean mole rats (Spalax ehrenbergi). Behav Ecol Sociobiol 21:31–33. https://doi.org/10.1007/BF00324432

    Article  Google Scholar 

  • Hiiemae K (1971) The structure and function of the jaw muscles in the rat (Rattus norvegicus L.) III. The mechanics of the muscles. Zool J Linnean Soc 50:111–132

    Article  Google Scholar 

  • Hrouzková E, Dvořáková V, Jedlička P, Šumbera R (2013) Seismic communication in demon African mole rat Tachyoryctes daemon from Tanzania. J Ethol 31:255–259. https://doi.org/10.1007/s10164-013-0374-0

    Article  Google Scholar 

  • Hrouzková E, Šklíba J, Pleštilová L, Hua L, Meheretu Y, Sillero-Zubiri C, Šumbera R (2018) Seismic communication in spalacids: signals in the giant root-rat and Gansu zokor. Hystrix Ital J Mammal 29:243–245. https://doi.org/10.4404/hystrix-00118-2018

    Article  Google Scholar 

  • Jansa SA, Giarla TC, Lim B (2009) The phylogenetic position of the rodent genus Typhlomys and the geographic origin of Muroidea. J Mammal 90:1083–1094

    Article  Google Scholar 

  • Jansa SA, Weksler M (2004) Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Mol Phyl Evol 31:256–276

    Article  CAS  Google Scholar 

  • Jarvis JUM, Sale JB (1971) Burrowing and burrow patterns of East African mole-rats Tachyoryctes, Heliophobius and Heterocephalus. J Zool 163:451–479. https://doi.org/10.1111/j.1469-7998.1971.tb04544.x

    Article  Google Scholar 

  • Kim EB, Fang X, Fushan AA, Huang Z, Lobanov AV, Han L, Marino SM, Sun X, Turanov AA, Yang P, Yim SH (2011) Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Nature 479:223–227

  • Kingdon J (1974) Mole-rats, blesmols, root-rats. In: East African Mammals, vol II, Pt B (Hares and Rodents). Academic Press. London, pp 474–494

    Google Scholar 

  • Kingdon J, Happold D, Butynski T, Hoffmann M, Happold M, Kalina J (2013) Mammals of Africa. Volume III: Rodents, Hares and Rabbits. Bloomsbury Publishing, London

  • Kirby AM, Fairman GD, Pamenter ME (2018) Atypical behavioural, metabolic and thermoregulatory responses to hypoxia in the naked mole rat (Heterocephalus glaber). J Zool 305:106–115. https://doi.org/10.1111/jzo.12542

    Article  Google Scholar 

  • Kock D, Ingram CM, Frabotta LJ, Honeycutt RL, Burda H (2006) On the nomenclature of Bathyergidae and Fukomys n. gen. (Mammalia: Rodentia). Zootaxa 1142:51–55

    Article  Google Scholar 

  • Lacey EA, Patton JL, Cameron GN (2000) Life Underground: The Biology of Subterranean Rodents. University of Chicago Press, Chicago

    Google Scholar 

  • Landry SO Jr (1957) Factors affecting the procumbency of rodent upper incisors. J Mammal 38:223–234. https://doi.org/10.2307/1376314

    Article  Google Scholar 

  • Laville E, Casinos A, Gasc J-P, Renous S, Bou J (1989) The mechanism of digging in Arvicola terrestris and Spalax ehrenbergi: functional and evolutional studies. Anat Anzeiger 169:131–144

    CAS  Google Scholar 

  • Lebrun R, Ponce de León MS, Tafforeau P, Zollikofer CPE (2010) Deep evolutionary roots of strepsirrhine primate labyrinthine morphology. J Anat 216:368–380

    Article  PubMed  Google Scholar 

  • Lin G-H, Wang K, Deng X-G, , Nevo E, Zhao F, Su J-P, Guo S-C, Zhang T-Z, Zhao H (2014) Transcriptome sequencing and phylogenomic resolution within Spalacidae (Rodentia). BMC Genomics 15:32

    Article  PubMed Central  PubMed  Google Scholar 

  • López -Antoñanzas R, Flynn LJ, Knoll F (2013) A comprehensive phylogeny of extinct and extant Rhizomyinae (Rodentia): evidence for multiple intercontinental dispersals. Cladistics 29:247–273

    Article  Google Scholar 

  • López-Antoñanzas R, Knoll F, Wan S, Flynn LJ (2015) Causal evidence between monsoon and evolution of rhizomyine rodents. Sci Rep 5:9008

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Manov I, Hirsh M, Iancu TC, Malik A, Sotnichenko N, Band M, Avivi A, Shams I (2013) Pronounced cancer resistance in a subterranean rodent, the blind mole-rat, Spalax: in vivo and in vitro evidence. BMC Biology 11:91. https://doi.org/10.1186/1741-7007-11-91

    Article  PubMed Central  PubMed  Google Scholar 

  • McIntosh AF, Cox PG (2016a) The impact of digging on craniodental morphology and integration. J Evol Biol 29:2383–2394. https://doi.org/10.1111/jeb.12962

    Article  CAS  PubMed  Google Scholar 

  • McIntosh AF, Cox PG (2016b) Functional implications of craniomandibular morphology in African mole-rats (Rodentia: Bathyergidae). Biol J Linnean Soc 117:447–462. https://doi.org/10.1111/bij.12691

    Article  Google Scholar 

  • McIntosh AF, Cox PG (2019) The impact of digging on the evolution of the rodent mandible. J Morphol 280:176–183. https://doi.org/10.1002/jmor.20929

    Article  PubMed  Google Scholar 

  • Mein P, Pickford M (2008) Early Miocene Rodentia from the northern Sperrgebiet, Namibia. Mem Geol Survey Namibia 20:235–290

    Google Scholar 

  • Morlok WF (1983) Vergleichend- und funktionell-anatomische Untersuchungen an Kopf, Hals und Vorderextremität subterraner Nagetiere (Mammalia, Rodentia). Schweizerbart Science Publishers, Stuttgart

    Google Scholar 

  • Musser GG, Carleton MD (2005) Superfamily Muroidea. In: Wilson DE, Reeder DM ( eds) Mammal Species of the World. A Taxonomic and Geographic Reference. 3rd Ed. Johns Hopkins University Press, Baltimore, pp 894-1531

  • Nevo E (1979) Adaptive convergence and divergence of subterranean mammals. Annu Rev Ecol Evol Syst 10:269–308

    Article  Google Scholar 

  • Nevo E (1999) Mosaic Evolution of Subterranean Mammals: Regression, Progression and Global Convergence. Oxford University Press, Oxford

    Google Scholar 

  • Norris RW (2017) Family Spalacidae. In: Wilson DE, Lacher TE, Mittermeier ME (eds) Handbook of the Mammals of the World, Vol 7, Rodents II. Lynx Edicions, Barcelona, pp 8–142

    Google Scholar 

  • Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528

    Article  CAS  PubMed  Google Scholar 

  • Patterson BD, Upham NS (2014) A newly recognized family from the Horn of Africa, the Heterocephalidae (Rodentia: Ctenohystrica). Zool J Linnean Soc 172:942–963

    Article  Google Scholar 

  • Rado R, Levi N, Hauser H, Witcher J, Alder N, Intrator N, Wollberg Z, Terkel J (1987) Seismic signalling as a means of communication in a subterranean mammal. Anim Behav 35:1249–1251. https://doi.org/10.1016/S0003-3472(87)80183-5

    Article  Google Scholar 

  • Renaud S, Gomes Rodrigues H, Ledevin R, Pisanu B, Chapuis J-L, Hardouin E (2015) Fast evolutionary response of house mice to anthropogenic disturbances on a Sub-Antarctic island. Biol J Linnean Soc 114:513–526

    Article  Google Scholar 

  • Rohlf FJ (1999) Shape statistics: Procrustes superimpositions and tangent spaces. J Classif 16:197–223

    Article  Google Scholar 

  • Sahm A, Bens M, Szafranski K, Holtze S, Groth M, Görlach M, Calkhoven C, Müller C, Schwab M, Kraus J, Kestler HA, Cellerino A, Burda H, Hildebrandt T, Dammann P, Platzer M (2018) Long-lived rodents reveal signatures of positive selection in genes associated with lifespan. PLoS Genetics 14:1–22. https://doi.org/10.1371/journal.pgen.1007272

    Article  CAS  Google Scholar 

  • Sen S (1977) La faune de Rongeurs pliocènes de Çalta (Ankara, Turquie). Bull Mus Natl Hist Nat 465:89–171

    Google Scholar 

  • Sherman PW, Jarvis JUM (2002) Extraordinary life spans of naked mole-rats (Heterocephalus glaber). J Zool 258:307–311

    Article  Google Scholar 

  • Stein BR (2000) Morphology of subterranean rodents. In: Lacey EA, Patton JL, Cameron GN (eds) Life Underground: The Biology of Subterranean Rodents. University of Chicago Press, Chicago, pp 19–61

    Google Scholar 

  • Steppan SJ, Schenk JJ (2017) Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates. PLoS One 12:e0183070. https://doi.org/10.1371/journal.pone.0183070

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Šumbera R, Krásová J, Lavrenchenko LA, Mengistu S, Bekele A, Mikula O, Bryja J (2018) Ethiopian highlands as a cradle of the African fossorial root-rats (genus Tachyoryctes), the genetic evidence. Mol Phyl Evol 126:105–115. https://doi.org/10.1016/j.ympev.2018.04.003

  • Van Daele PAAG, Herrel A, Adriaens D (2009) Biting performance in teeth-digging African mole-rats (Fukomys, Bathyergidae, Rodentia). Physiol Biochem Zool 82:40–50

    Article  PubMed  Google Scholar 

  • Visser JH, Bennett NC, Jansen van Vuuren B (2019) Phylogeny and biogeography of the African Bathyergidae: a review of patterns and processes. PeerJ 7:e7730. https://doi.org/10.7717/peerj.7730

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wood AE (1965) Grades and clades among rodents. Evolution 19: 115–130

    Article  Google Scholar 

Download references

Acknowledgments

We warmly thanks the curators V. Nicolas-Colin, C. Denys (MNHN, Paris), and R. Portela-Miguez (NHM, London) for giving access to the collections of spalacids and bathyergids, respectively. We are grateful to P.-H. Fabre and Q. Martinez (ISEM, Montpellier) for sending us scans of Spalax and Myospalax, and to T. Descamps (MECADEV, MNHN, Paris) for the loan of the microscribe. We thank R. Lebrun (ISEM, Montpellier) who kindly gave us access to Morphotools. We also acknowledge the editor J.R. Wible, and R. Šumbera (University of South Bohemia, Ceske Budejovice) and P. Cox (Hull York Medical School, University of York) for their fruitful comments and suggestions on the manuscript.

Author information

Authors and Affiliations

  1. Centre de Recherche en Paléontologie - Paris (CR2P), UMR CNRS 7207, CP38, Muséum National D’Histoire Naturelle, Sorbonne Université, 8 rue Buffon, 75005, Paris, France

    Morgane Fournier & Helder Gomes Rodrigues

  2. Institut Des Sciences de L’Evolution, cc64, Université de Montpellier, CNRS, IRD, EPHE, 34095, Montpellier, France

    Lionel Hautier

Authors
  1. Morgane Fournier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lionel Hautier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Helder Gomes Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Helder Gomes Rodrigues.

Ethics declarations

Research Involving Human and Animal Participants

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.

Conflict of Interests

The authors declare that they have no conflict of interest.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fournier, M., Hautier, L. & Gomes Rodrigues, H. Evolution Towards Fossoriality and Morphological Convergence in the Skull of Spalacidae and Bathyergidae (Rodentia). J Mammal Evol 28, 979–993 (2021). https://doi.org/10.1007/s10914-021-09550-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-021-09550-z

Keywords

Search

Navigation