Skip to main content

Advertisement

SpringerLink
Log in

Evolving Teeth Within a Stable Masticatory Apparatus in Orkney Mice

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Mice from the Orkney archipelago exhibit an important diversity regarding molar shape. While on some islands mice display a usual dental pattern, teeth from other islands display additional cusplets and unusual phenotypes that may constitute case studies for evaluating the potential functional relevance of dental changes. We developed a multifaceted approach combining 2D and 3D geometric morphometrics, dental topography, dental wear, biomechanics, estimations of masticatory muscles force, and in vivo bite force on wild-derived lab descendants exemplifying the two extreme dental morphologies. The two strains differed in the geometry of the upper and lower tooth rows, and in the topography of the upper row only. Surprisingly, the most unusual tooth morphology appeared as the least complex because tooth simplification overwhelmed the signal provided by the occurrence of additional cusplets. No difference in bite force nor muscle force was evidenced, showing that the important change in dental morphology was accommodated without major changes in the rest of the masticatory apparatus. The evolution of unusual dental phenotypes was possibly fueled by drift and inbreeding in small and isolated populations on remote islands of the archipelago. No functional counter-selection impeded this diversification, since the unusual dental phenotypes did not disrupt occlusion and mastication.

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
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Abramoff, M. D., Magalhaes, P. J., & Ram, S. J. (2004). Image processing with imageJ. Biophotonics International, 11(7), 36–42.

    Google Scholar 

  • Anderson, P. S. L., Renaud, S., & Rayfield, E. J. (2014). Adaptive plasticity in the mouse mandible. BMC Evolutionary Biology, 14, 85.

    Article  Google Scholar 

  • Berry, R. J. (1996). Small mammal differentiation on islands. Philosophical Transactions of the Royal Society, London B, 351(1341), 753–764.

    Article  CAS  Google Scholar 

  • Boell, L., & Tautz, D. (2011). Micro-evolutionary divergence pattersn of mandible shapes in wild house mouse (Mus musculus) populations. BMC Evolutionary Biology, 11(306).

    Article  Google Scholar 

  • Bonhomme, V., Picq, S., Gaucherel, C., & Claude, J. (2014). Momocs: Outline analysis using R. Journal of Statistical Software, 56, 1–24.

    Article  Google Scholar 

  • Boyer, D. M. (2008). Relief index of second mandibular molars is a correlate of diet among prosimian primates and other euarchontan mammals. Journal of Human Evolution, 55, 1118–1137.

    Article  Google Scholar 

  • Boyer, D. M., Evans, A. R., & Jernvall, J. (2010). Evidence of dietary differentiation among late Paleocene–early Eocene plesiadapids (Mammalia, primates). American Journal of Physical Anthropology, 142, 194–210. https://doi.org/10.1002/ajpa.21211.

    Article  PubMed  Google Scholar 

  • Boyer, D. M., Puente, J., Gladman, J. T., Glynn, C., Mukherjee, S., Yapuncich, G. S., et al. (2015). A new fully automated approach for aligning and comparing shapes. The Anatomical Record, 298(1), 249–276. http://www2.stat.duke.edu/~sayan/auto3dgm/.

    Article  Google Scholar 

  • Bunn, J. M., Boyer, D. M., Lipman, Y., Clair, E. M. S., Jernvall, J., & Daubechies, I. (2011). Comparing Dirichlet normal surface energy of tooth crowns, a new technique of molar shape quantification for dietary inference, with previous methods in isolation and in combination. American Journal of Physical Anthropology, 145, 247–261. https://doi.org/10.1002/ajpa.21489.

    Article  PubMed  Google Scholar 

  • Champely, S. (2018). pwr: Basic functions for power analysis. R package version 1.2-2.

  • Charles, C., & Viriot, L. (2015). Variations and anomalies in rodent teeth and their importance for testing developmental models. In P. G. Cox & L. Hautier (Eds.), Evolution of the rodents: Advances in phylogeny, functional morphology and development (pp. 405–423). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Crampton, J. S. (1995). Elliptic Fourier shape analysis of fossil bivalves: Some practical considerations. Lethaia, 28, 179–186.

    Article  Google Scholar 

  • de Winter, J. C. F. (2013). Using the student’s t-test with extremely small sample sizes. Practical Assessment, Research and Evaluation, 18(10), 1–12.

    Google Scholar 

  • Dray, S., & Dufour, A.-B. (2007). The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22, 1–20.

    Article  Google Scholar 

  • Evans, A. R., & Jernvall, J. (2009). Patterns and constraints in carnivoran and rodent dental complexity and tooth size. In SVP program and abstracts book. Journal of Vertebrate Paleontology, 29, 92A.

    Google Scholar 

  • Evans, A. R., & Sanson, G. D. (2003). The tooth of perfection: Functional and spatial constraints on mammalian tooth shape. Biological Journal of the Linnean Society, 78, 173–191.

    Article  Google Scholar 

  • Evans, A. R., Wilson, G. P., Fortelius, M., & Jernvall, J. (2007). High-level similarity of dentitions in carnivorans and rodents. Nature, 445(nature05433), 78–81. https://doi.org/10.1038/nature05433.

    Article  CAS  PubMed  Google Scholar 

  • Fabre, P.-H., Herrel, A., Fitriana, Y., Meslin, L., & Hautier, L. (2017). Masticatory muscle architecture in a water-rat from Australasia (Murinae, Hydromys) and its implication for the evolution of carnivory in rodents. Journal of Anatomy, 231(3), 380–397.

    Article  Google Scholar 

  • Godfrey, L. R., Winchester, J. M., King, S. J., Boyer, D. M., & Jernvall, J. (2012). Dental topography indicates ecological contraction of lemur communities. American Journal of Physical Anthropology, 148, 215–227. https://doi.org/10.1002/ajpa.21615.

    Article  PubMed  Google Scholar 

  • Gomes Rodrigues, H., Merceron, G., & Viriot, L. (2009). Dental microwear patterns of extant and extinct Muridae (Rodentia, Mammalia): Ecological implications. Naturwissenschaften, 96, 537–542.

    Article  CAS  Google Scholar 

  • Gunz, P., Mitteroecker, P., & Bookstein, F. L. (2005). Semilandmarks in three dimensions. Modern morphometrics in physical anthropology. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology: Developments in primatology: Progress and prospects (pp. 73–98). New York: Springer.

    Google Scholar 

  • Hammer, Ø, Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological Statistics software package for education and data analysis. Palaeontological Electronica, 4(1), 1–9.

    Google Scholar 

  • Happold, D. C. D. (2013). Mammals of Africa. Volume III: Rodents, hares and rabbits. London: Bloomsbury Publishing.

    Google Scholar 

  • Harmon, L. J., Kolbe, J. J., Cheverud, J. M., & Losos, J. B. (2005). Convergence and the multidimensional niche. Evolution, 59(2), 409–421.

    Article  Google Scholar 

  • Herrel, A., De Smet, A., Aguirre, L. F., & Aerts, P. (2008). Morphological and mechanical determinants of bite force in bats: Do muscles matter? Journal of Experimental Biology, 211, 86–91. https://doi.org/10.1242/jeb.012211.

    Article  PubMed  Google Scholar 

  • Herrel, A., Spithoven, L., Van Damme, R., & De Vree, F. (1999). Sexual dimorphism of head size in Gallotia galloti: Testing the niche divergence hypothesis by functional analyses. Functional Ecology, 13(3), 289–297.

    Article  Google Scholar 

  • Hiiemae, K. M. (1971). The structure and function of the jaw muscles in the rat (Rattus norvegicus L.) III. The mechanics of the muscles. Zoological Journal of the Linnean Society, 50, 111–132.

    Article  Google Scholar 

  • Jacobs, L. L., Flynn, L. J., Downs, W. R., & Barry, J. C. (1990). Quo vadis, Antemus? The Siwalik Muroid record. In E. H. Lindsay (Ed.), European neogene mammal chronology (pp. 573–586). New York: Plenum Press.

    Chapter  Google Scholar 

  • Jamniczky, H. A., & Hallgrímsson, B. (2011). Modularity in the skull and cranial vasculature of laboratory mice: Implications for the evolution of complex phenotypes. Evolution and Development, 13(1), 28–37.

    Article  Google Scholar 

  • Jernvall, J. (2000). Linking develoment with generation of novelty in mammalian teeth. Proceedings of the National Academy of Sciences, USA, 97(6), 2641–2645.

    Article  CAS  Google Scholar 

  • Kan Kouassi, S., Nicolas, V., Aniskine, V., Lalis, A., Cruaud, C., Couloux, A., et al. (2008). Taxonomy and biogeography of the African Pygmy mice, Subgenus Nannomys (Rodentia, Murinae, Mus) in Ivory Coast and Guinea (West Africa). Mammalia, 72, 237–252.

    Google Scholar 

  • Kavanagh, K. D., Evans, A. R., & Jernvall, J. (2007). Predicting evolutionary patterns of mammalian teeth from development. Nature, 449, 427–432.

    Article  CAS  Google Scholar 

  • Kuhl, F. P., & Giardina, C. R. (1982). Elliptic Fourier features of a closed contour. Computer Graphics and Image Processing, 18, 259–278.

    Article  Google Scholar 

  • Langsrud, Ø, & Mevik, B.-H. (2012). ffmanova: Fifty-fifty MANOVA. https://CRAN.R-project.org/package=ffmanova.

  • Lazzari, V., Charles, C., Tafforeau, P., Vianey-Liaud, M., Aguilar, J.-P., Jaeger, J.-J., et al. (2008). Mosaic convergence of rodent dentitions. PLoS ONE, 3, e3607.

    Article  Google Scholar 

  • Ledevin, R., Chevret, P., Ganem, G., Britton-Davidian, J., Hardouin, E. A., Chapuis, J.-L., et al. (2016). Phylogeny and adaptation shape the teeth of insular mice. Proceedings of the Royal Society of London, Biological Sciences (series B), 283, 20152820, https://doi.org/10.1098/rspb.2015.2820.

    Article  CAS  Google Scholar 

  • Miller, G. S. (1912). Catalogue of the mammals of Western Europe (exclusive of Russia) in the collection of the British Museum. London: British Museum (Natural History).

    Google Scholar 

  • Murphy, R. A., & Beardsley, A. C. (1974). Mechanical properties of the cat soleus muscle in situ. American Journal of Physiology, 227(5), 1008–1013.

    CAS  PubMed  Google Scholar 

  • Pampush, J. D., Winchester, J. M., Morse, P. E., Vining, A. Q., Boyer, D. M., & Kay, R. F. (2016). Introducing molaR: A new r package for quantitative topographic analysis of teeth (and other topographic surfaces). Journal of Mammalian Evolution, 161(4), 705–721. https://doi.org/10.1007/s10914-016-9326-0.

    Article  Google Scholar 

  • R-Core-Team (2017). R: A language for environment and statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

    Google Scholar 

  • Renaud, S., Alibert, P., & Auffray, J.-C. (2017). Impact of hybridization on shape, variation and covariation of the mouse molar. Evolutionary Biology, 44(1), 69–81.

    Article  Google Scholar 

  • Renaud, S., & Auffray, J.-C. (2013). The direction of main phenotypic variance as a channel to morphological evolution: Case studies in murine rodents. Hystrix, The Italian Journal of Mammalogy, 24(1), 85–93. https://doi.org/10.4404/hystrix-24.1-6296.

    Article  Google Scholar 

  • Renaud, S., Auffray, J.-C., & de La Porte, S. (2010). Epigenetic effects on the mouse mandible: Common features and discrepancies in remodeling due to muscular dystrophy and response to food consistency. BMC Evolutionary Biology, 10, 28. http://www.biomedcentral.com/1471-2148/10/28.

    Article  Google Scholar 

  • Renaud, S., & Ledevin, R. (2017). Impact of wear and diet on molar row geometry and topography in the house mouse. Archives of Oral Biology, 81, 31–40.

    Article  Google Scholar 

  • Renaud, S., Michaux, J., Jaeger, J.-J., & Auffray, J.-C. (1996). Fourier analysis applied to Stephanomys (Rodentia, Muridae) molars: Nonprogressive evolutionary pattern in a gradual lineage. Paleobiology, 22(2), 255–265.

    Article  Google Scholar 

  • Renaud, S., & Michaux, J. R. (2007). Mandibles and molars of the wood mouse, Apodemus sylvaticus (L.): Integrated latitudinal signal and mosaic insular evolution. Journal of Biogeography, 34(2), 339–355.

    Article  Google Scholar 

  • Renaud, S., Pantalacci, S., & Auffray, J.-C. (2011). Differential evolvability along lines of least resistance of upper and lower molars in island house mice. PLoS One, 6(5), e18951. https://doi.org/10.1371/journal.pone.0018951.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renaud, S., Pantalacci, S., Quéré, J.-P., Laudet, V., & Auffray, J.-C. (2009). Developmental constraints revealed by co-variation within and among molar rows in two murine rodents. Evolution and Development, 11(5), 590–602. https://doi.org/10.1111/j.1525-142X.2009.00365.x.

    Article  PubMed  Google Scholar 

  • Renaud, S., Rodrigues, G., Ledevin, H., Pisanu, R., Chapuis, B., J.-L., & Hardouin, E. A. (2015). Fast morphological response of house mice to anthropogenic disturbances on a Sub-Antarctic island. Biological Journal of the Linnean Society, 114, 513–526.

    Article  Google Scholar 

  • Renvoisé, E., Kavanagh, K. D., Lazzari, V., Häkkinen, T. J., Rice, R., Pantalacci, S., et al. (2017). Mechanical constraint from growing jaw facilitates mammalian dental diversity. Proceedings of the National Academy of Sciences, USA, 114(35), 9403–9408.

    Article  Google Scholar 

  • Rohlf, F. J., & Archie, J. W. (1984). A comparison of Fourier methods for the description of wing shape in Mosquitoes (Diptera: Culicidae). Systematic Zoology, 33(3), 302–317.

    Article  Google Scholar 

  • Salazar-Ciudad, I., & Jernvall, J. (2002). A gene network model accounting for develoment and evolution of mammalian teeth. Proceedings of the National Academy of Sciences, USA, 99(12), 8116–8120.

    Article  CAS  Google Scholar 

  • Santana, S. E., Strait, S., & Dumont, E. R. (2011). The better to eat you with: Functional correlates of tooth structure in bats. Functional Ecology, 25, 839–847.

    Article  Google Scholar 

  • Schlager, S. (2016). mesheR: Meshing operations on triangular meshes. (0.4.160301 ed., pp. R package).

  • Schlager, S. (2017). Morpho and Rvcg: Shape analysis in {R}. In G. Zheng, S. Li, & G. Szekely (Eds.), Statistical shape and deformation analysis (pp. 217–256). Cambridge: Academic Press.

    Chapter  Google Scholar 

  • Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution, 50(5), 1766–1774.

    Article  Google Scholar 

  • Scoville, A. G., & Pfrender, M. E. (2010). Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proceedings of the National Academy of Sciences, USA, 107(9), 4260–4263.

    Article  CAS  Google Scholar 

  • Searle, J. B., Jones, C. S., Gündüz, İ, Scascitelli, M., Jones, E. P., Herman, J. S., et al. (2009). Of mice and (Viking?) men: Phylogeography of British and Irish house mice. Proceedings of the Royal Society of London, Biological Sciences (series B), 276, 201–207. https://doi.org/10.1098/rspb.2008.0958.

    Article  CAS  Google Scholar 

  • Sheets, H. D., Covino, K. M., Panasiewicz, J. M., & Morris, S. R. (2006). Comparison of geometric morphometric outline methods in the discrimination of age-related differences in feather shape. Frontiers in Zoology, 3, 15. https://doi.org/10.1186/1742-9994-3-15.

    Article  PubMed  PubMed Central  Google Scholar 

  • Skinner, M. M., & Gunz, P. (2010). The presence of accessory cusps in chimpanzee lower molars is consistent with a patterning cascade model of development. Journal of Anatomy, 217, 245–253.

    Article  Google Scholar 

  • Stoetzel, E., Denys, C., Michaux, J., & Renaud, S. (2013). Mus in Morocco: A quaternary sequence of intraspecific evolution. Biological Journal of the Linnean Society, 109, 599–621.

    Article  Google Scholar 

  • Ungar, P. S. (2004). Dental topography and diets of Australopithecus afarensis and early Homo. Journal of Human Evolution, 46, 605–622. https://doi.org/10.1016/j.jhevol.2004.03.004.

    Article  PubMed  Google Scholar 

  • West-Eberard, M. J. (1989). Phenotypic plasticity and the origin of diversity. Annual Review of Ecology, Evolution and Systematics, 20, 249–278.

    Article  Google Scholar 

  • Winchester, J. M., Boyer, D. M., Clair, E. M. S., Gosselin-Ildari, A. D., Cooke, S. B., & Ledogar, J. A. (2014). Dental topography of platyrrhines and prosimians: Convergence and contrasts. American Journal of Physical Anthropology, 153(1), 29–44. https://doi.org/10.1002/ajpa.22398.

    Article  PubMed  Google Scholar 

  • Wood, A. E. (1965). Grades and clades among rodents. Evolution, 19, 115–130.

    Article  Google Scholar 

  • Zelditch, M. L., Wood, A. R., Bonett, R. M., & Swiderski, D. L. (2008). Modularity of the rodent mandible: Integrating bones, muscles, and teeth. Evolution and Development, 10(6), 756–766.

    Article  Google Scholar 

Download references

Acknowledgements

We warmly thank the members of the Bigtooth field team: Jean-Christophe Auffray, Pascale Chevret, Annie Orth, and Josette Catalan. We also thank Roohollah Siahsarvie for his investment while breeding the mice, and Laurent Marivaux who kindly gave us access to the stereomicroscopy facility at ISEM. We are indebted to Vincent Bonhomme who implemented the sfourier function in Momocs and was of great help in adapting the method to our data. We acknowledge the contribution of SFR Biosciences (UMS3444/CNRS, US8/Inserm, ENS de Lyon, UCBL) AniRa-ImmOs facility, and we particularly thank Mathilde Bouchet for her kind assistance during the scanning sessions. We also thank two anonymous reviewers for their constructive remarks. This study was supported by the ANR Bigtooth (ANR-11-BSV7-008). This is a publication ISEM 2018-150.

Author information

Author notes

  1. Ronan Ledevin

    Present address: UMR5199 PACEA, Université de Bordeaux, Allée Geoffroy Saint Hilaire (Bat. B8), 33615, Pessac, France

  2. Louise Souquet & Samuel Ginot

    Present address: Institut de Génomique Fonctionnelle de Lyon, UMR 5242, CNRS, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, 46 Allée d’Italie, 69364, Lyon Cedex 07, France

Authors and Affiliations

  1. Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, Université Lyon 1, CNRS, 69100, Villeurbanne Cedex, France

    Sabrina Renaud, Ronan Ledevin & Louise Souquet

  2. 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

    Helder Gomes Rodrigues

  3. Mécanismes adaptatifs et évolution (MECADEV), UMR 7179, CNRS, Funevol team, Muséum National d’Histoire Naturelle, 55 rue Buffon, Bat. Anatomie Comparée, CP 55, 75005, Paris Cedex 5, France

    Helder Gomes Rodrigues & Anthony Herrel

  4. Institut des Sciences de l’Evolution, Université de Montpellier, UMR5554 CNRS, IRD, EPHE, Place Eugène Bataillon, CC65, 34095, Montpellier Cedex, France

    Helder Gomes Rodrigues, Samuel Ginot, Sylvie Agret, Julien Claude & Lionel Hautier

Authors
  1. Sabrina Renaud
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ronan Ledevin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Louise Souquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Helder Gomes Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Samuel Ginot
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sylvie Agret
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Julien Claude
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Anthony Herrel
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lionel Hautier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sabrina Renaud.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Renaud, S., Ledevin, R., Souquet, L. et al. Evolving Teeth Within a Stable Masticatory Apparatus in Orkney Mice. Evol Biol 45, 405–424 (2018). https://doi.org/10.1007/s11692-018-9459-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-018-9459-6

Keywords

Search

Navigation