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Swimmers, Diggers, Climbers and More, a Study of Integration Across the Mustelids’ Locomotor Apparatus (Carnivora: Mustelidae)

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Abstract

Phenotypic integration, defined as the coordinated co-variation of parts of an organism can be an important constraint on phenotypic diversification. Functional factors, by having an heterogeneous impact across the animal body, may reinforce the integration of some parts while causing a perturbation of the integration among other parts. The integration across the locomotor apparatus should thus reflect to a certain extent the locomotor ecology of the animal. Using the mustelids as study group, we track changes in the patterns of co-variation in species belonging to four different locomotor ecologies (terrestrial, semi-arboreal, semi-fossorial, and semi-aquatic). Our results highlight the strong overall integration in mustelid long bones. The main shape changes associated with co-variations between skeletal elements are the bone robustness and proportions of the epiphyses. The pattern of co-variation is, however, only slightly impacted by allometry. Changes in co-variation between species mostly scale with phylogenetic divergence time, except for the (Mustela putorius, M. eversmanni, M. lutreola) clade which, despite a short divergence time, presents strong differences in co-variation. Co-variation patterns differ between locomotor ecologies, but few of these variations match the hypothesis of a reduction of integration due to functional specialization. This may reflect our lack of knowledge on the functional modules in species with locomotor ecologies that differ from terrestrial locomotion rather than invalidate our a priori hypotheses.

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References

  • Adam, P. J. (2002). Hind limb anatomy. In J. H. Steele (Ed.), Encyclopedia of ocean sciences (pp. 214–220). Oxford: Academic Press.

    Google Scholar 

  • Adams, D. C. (2016). Evaluating modularity in morphometric data: Challenges with the RV coefficient and a new test measure. Methods in Ecology and Evolution, 7(5), 565–572. https://doi.org/10.1111/2041-210X.12511.

    Google Scholar 

  • Adams, D. C., & Collyer, M. L. (2016). On the comparison of the strength of morphological integration across morphometric datasets. Evolution. https://doi.org/10.1111/evo.13045.

    Google Scholar 

  • Adams, D. C., & Otárola-Castillo, E. (2013). geomorph: An R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution, 4(4), 393–399.

    Article  Google Scholar 

  • Amson, E., Argot, C., McDonald, H. G., & de Muizon, C. (2015). Osteology and functional morphology of the forelimb of the marine sloth Thalassocnus (Mammalia, Tardigrada). Journal of Mammalian Evolution, 22(2), 169–242.

    Article  Google Scholar 

  • Arias-Martorell, J., Potau, J. M., Bello-Hellegouarch, G., & Pérez-Pérez, A. (2014). Brief communication: Developmental versus functional three-dimensional geometric morphometric-based modularity of the human proximal humerus: Modularity of the Proximal Humerus. American Journal of Physical Anthropology, 154(3), 459–465. https://doi.org/10.1002/ajpa.22520.

    PubMed  Google Scholar 

  • Bodkin, J. L. (2001). Sea Otters. In J. H. Steele (Ed.), Encyclopedia of ocean sciences (pp. 2614–2621). Oxford: Academic Press, https://doi.org/10.1006/rwos.2001.0434.

  • Botton-Divet, L., Cornette, R., Fabre, A.-C., Herrel, A., & Houssaye, A. (2016). Morphological analysis of long bones in semi-aquatic mustelids and their terrestrial relatives. Integrative and Comparative Biology, 56(6), 1298–1309. https://doi.org/10.1093/icb/icw124.

    PubMed  Google Scholar 

  • Bou, J., Casinos, A., & Ocana, J. (1987). Allometry of the Limb Long Bones of Insectivores and Rodents. Journal of Morphology, 192(2), 113–123.

    Article  CAS  PubMed  Google Scholar 

  • Buchholtz, E. A. (2007). Modular evolution of the cetacean vertebral column. Evolution & Development, 9(3), 278–289.

    Article  CAS  Google Scholar 

  • Casinos, A., Quintana, C., & Viladiu, C. (1993). Allometry and adaptation in the long bones of a digging group of rodents (Ctenomyinae). Zoological Journal of the Linnean Society, 107(2), 107–115.

    Article  Google Scholar 

  • Cubo, J. (2004). Pattern and process in constructional morphology. Evolution and Development, 6(3), 131–133.

    Article  PubMed  Google Scholar 

  • Duplaix, N. (1980). Observations on the ecology and behavior of the giant river otter Pteronura brasiliensis in Suriname. Terre Vie, 34, 495–620.

    Google Scholar 

  • Escoufier, Y. (1973). Le traitement des variables vectorielles. Biometrics, 29(4), 751. https://doi.org/10.2307/2529140.

    Google Scholar 

  • Estes, J. A. (1980). Enhydra lutris. Mammalian Species. https://doi.org/10.2307/3503844

    Google Scholar 

  • Fabre, A.-C., Cornette, R., Goswami, A., & Peigné, S. (2015a). Do constraints associated with the locomotor habitat drive the evolution of forelimb shape? A case study in musteloid carnivorans. Journal of Anatomy, 226(6), 596–610. https://doi.org/10.1111/joa.12315.

    PubMed  PubMed Central  Google Scholar 

  • Fabre, A.-C., Cornette, R., Peigné, S., & Goswami, A. (2013a). Influence of body mass on the shape of forelimb in musteloid carnivorans. Biological Journal of the Linnean Society, 110(1), 91–103.

    Article  Google Scholar 

  • Fabre, A.-C., Cornette, R., Slater, G., Argot, C., Peigné, S., Goswami, A., & Pouydebat, E. (2013b). Getting a grip on the evolution of grasping in musteloid carnivorans: A three-dimensional analysis of forelimb shape. Journal of Evolutionary Biology, 26(7), 1521–1535. https://doi.org/10.1111/jeb.12161.

    PubMed  Google Scholar 

  • Fabre, A.-C., Goswami, A., Peigné, S., & Cornette, R. (2014). Morphological integration in the forelimb of musteloid carnivorans. Journal of Anatomy, 225(1), 19–30. https://doi.org/10.1111/joa.12194.

    PubMed  PubMed Central  Google Scholar 

  • Fabre, A.-C., Salesa, M. J., Cornette, R., Antón, M., Morales, J., & Peigné, S. (2015b). Quantitative inferences on the locomotor behaviour of extinct species applied to Simocyon batalleri (Ailuridae, Late Miocene, Spain). The Science of Nature, 102(5–6, 30. https://doi.org/10.1007/s00114-015-1280-9.

    PubMed  Google Scholar 

  • Fischer, M. S., Schilling, N., Schmidt, M., Haarhaus, D., & Witte, H. (2002). Basic limb kinematics of small therian mammals. Journal of Experimental Biology, 205(9), 1315–1338.

    PubMed  Google Scholar 

  • Fish, F. E. (1994). Association of propulsive swimming mode with behavior in river otters (Lutra canadensis). Journal of Mammalogy, 75(4), 989. https://doi.org/10.2307/1382481.

    Google Scholar 

  • Fisher, E. M. (1942). The osteology and myology of the California river otter. Stanford: Stanford University Press.

    Google Scholar 

  • Fujii, J. A., Ralls, K., & Tinker, M. T. (2015). Ecological drivers of variation in tool-use frequency across sea otter populations. Behavioral Ecology, 26(2), 519–526. https://doi.org/10.1093/beheco/aru220.

    Google Scholar 

  • Gasc, J.-P. (2001). Comparative aspects of gait, scaling and mechanics in mammals. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology, 131(1), 121–133.

    Article  CAS  Google Scholar 

  • Goswami, A., & Polly, P. D. (2010). Methods for studying morphological integration, modularity and covariance evolution. Quantitative Methods in Paleobiology. The Paleontological Society Papers Series, 16, 213–243.

    Google Scholar 

  • Goswami, A., Smaers, J. B., Soligo, C., & Polly, P. D. (2014). The macroevolutionary consequences of phenotypic integration: From development to deep time. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1649), 20130254–20130254. https://doi.org/10.1098/rstb.2013.0254.

    CAS  Google Scholar 

  • Gould, S. J., & Lewontin, R. C. (1979). The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proceedings of the Royal Society of London. Series B. Biological Sciences, 205(1161), 581–598.

    Article  CAS  Google Scholar 

  • Gower, J. C. (1975). Generalized procrustes analysis. Psychometrika, 40(1), 33–51.

    Article  Google Scholar 

  • Gunz, P., & Mitteroecker, P. (2013). Semilandmarks: A method for quantifying curves and surfaces. Hystrix, The Italian Journal of Mammalogy, 24(1), 103–109.

    Google Scholar 

  • Hallgrímsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., & Marcucio, R. S. (2009). Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology, 36(4), 355–376. https://doi.org/10.1007/s11692-009-9076-5.

    PubMed  PubMed Central  Google Scholar 

  • Hallgrímsson, B., Willmore, K., & Hall, B. K. (2002). Canalization, developmental stability, and morphological integration in primate limbs. American Journal of Physical Anthropology, 119(S35), 131–158. https://doi.org/10.1002/ajpa.10182.

    Google Scholar 

  • Heinrich, R. E., & Biknevicius, A. R. (1998). Skeletal allometry and interlimb scaling patterns in mustelid carnivorans. Journal of Morphology, 235(2), 121–134.

    Article  CAS  PubMed  Google Scholar 

  • Holmes, T. (1980). Locomotor adaptations in the limb skeletons of North American mustelids. Arcata: Humboldt State University. Retrived 19 Dec, 2014 from http://humboldt-dspace.calstate.edu/handle/2148/1249.

  • Howard, L. D. (1973). Muscular anatomy of the forelimb of the sea otter (Enhydra lutris). Proceedings of the California Academy of Science, 39(20), 411–500.

    Google Scholar 

  • Hunter, L., & Barrett, P. (2011). Carnivores of the World. Princeton: Princeton University Press.

    Google Scholar 

  • Klingenberg, C. P. (2009). Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a priori hypotheses. Evolution and Development, 11(4), 405–421. https://doi.org/10.1111/j.1525-142X.2009.00347.x.

    PubMed  PubMed Central  Google Scholar 

  • Koepfli, K.-P., Deere, K. A., Slater, G. J., Begg, C., Begg, K., Grassman, L., et al. (2008). Multigene phylogeny of the Mustelidae: Resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation. BMC Biology, 6(1), 10. https://doi.org/10.1186/1741-7007-6-10.

    PubMed  PubMed Central  Google Scholar 

  • Larivière, S. (1998). Lontra felina. Mammalian Species, 575, 1–5.

    Google Scholar 

  • Larivière, S. (2001). Aonyx capensis. Mammalian species, 671, 1–6.

    Article  Google Scholar 

  • Larivière, S., & Jennings, A. P. (2009). Mustelidae (weasels and relatives). In D. E. Wilson & R. A. Mittermeier (Eds.), Handbook of the mammals of the world (Vol. 1, Carnivores, pp. 564–656). Barcelona: Lynx.

    Google Scholar 

  • Leach, D. (1977). The descriptive and comparative postcranial osteology of marten (Martes americana Turton) and fisher (Martes pennanti Erxleben): The appendicular skeleton. Canadian Journal of Zoology, 55(1), 199–214.

    Article  CAS  PubMed  Google Scholar 

  • Lodé, T. (1999). Comparative measurements of terrestrial and aquatic locomotion in Mustela lutreola and M. putorius. Zeitschrift fur Saugetierkunde, 64, 110–115.

    Google Scholar 

  • Martín-Serra, A., Figueirido, B., Pérez-Claros, J. A., & Palmqvist, P. (2014). Patterns of morphological integration in the appendicular skeleton of mammalian carnivores. Evolution. https://doi.org/10.1111/evo.12566.

    Google Scholar 

  • Mitteroecker, P., & Bookstein, F. (2007). The conceptual and statistical relationship between modularity and morphological integration. Systematic Biology, 56(5), 818–836. https://doi.org/10.1080/10635150701648029.

    PubMed  Google Scholar 

  • Mitteroecker, P., & Bookstein, F. (2008). The evolutionary role of modularity and integration in the hominoid cranium. Evolution, 62(4), 943–958. https://doi.org/10.1111/j.1558-5646.2008.00321.x.

    PubMed  Google Scholar 

  • Nowak, R. M. (2005). Walker’s carnivores of the world. Baltimore: JHU Press.

    Google Scholar 

  • Pasitschniak-Art, M., & Larivière, S. (1995). Gulo gulo. Mammalian Species, 499, 1–10.

    Google Scholar 

  • Polly, P. D. (2007). Limbs in mammalian evolution. In B. K. Hall (Ed.), Fins into limbs: Evolution, development and transformation (pp. 245–268). Chicago: University of Chicago Press.

    Google Scholar 

  • Polly, P. D. (2008). Adaptive zones and the pinniped ankle: A 3D quantitative analysis of carnivoran tarsal evolution. In E. Sargis & M. Dagosto (Eds.), Mammalian evolutionary morphology: A tribute to Frederick S. Szalay (pp. 167–196). Dordrecht: Springer.

    Chapter  Google Scholar 

  • R Core Team. (2014). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

  • Reid, F., & Helgen, K. M. (2008). Mustela frenata. IUCN. Retrieved December 15, 2015, from http://www.iucnredlist.org/details/41654/0.

  • Riedman, M., & Estes, J. A. (1990). The sea otter (Enhydra lutris): Behavior, ecology, and natural history. Biological Report (USA). no. 90 (14).

  • Rohlf, F. J., & Slice, D. (1990). Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Biology, 39(1), 40–59.

    Google Scholar 

  • Samuels, J. X., Meachen, J. A., & Sakai, S. A. (2013). Postcranial morphology and the locomotor habits of living and extinct carnivorans. Journal of Morphology, 274(2), 121–146. https://doi.org/10.1002/jmor.20077.

    PubMed  Google Scholar 

  • Samuels, J. X., & Van Valkenburgh, B. (2008). Skeletal indicators of locomotor adaptations in living and extinct rodents. Journal of Morphology, 269(11), 1387–1411. https://doi.org/10.1002/jmor.10662.

    PubMed  Google Scholar 

  • Sansalone, G., Colangelo, P., Kotsakis, T., Loy, A., Castiglia, R., Bannikova, A. A., et al. (2017). Influence of evolutionary allometry on rates of morphological evolution and disparity in strictly subterranean moles (Talpinae, Talpidae, Lipotyphla, Mammalia). Journal of Mammalian Evolution. Retrieved January 10, 2017, from http://link.springer.com/10.1007/s10914-016-9370-9.

  • Sato, J. J., Hosoda, T., Wolsan, M., Tsuchiya, K., Yamamoto, M., & Suzuki, H. (2003). Phylogenetic relationships and divergence times among mustelids (Mammalia: Carnivora) based on nucleotide sequences of the nuclear interphotoreceptor retinoid binding protein and mitochondrial cytochrome b genes. Zoological Science, 20(2), 243–264.

    Article  CAS  PubMed  Google Scholar 

  • Schlager, S. (2016). Morpho 2.4. Retrieved August 2, 2016, from https://github.com/zarquon42b/Morpho.

  • Schmidt, M., & Fischer, M. S. (2009). Morphological integration in mammalian limb proportions: Dissociation between function and development. Evolution, 63(3), 749–766.

    Article  PubMed  Google Scholar 

  • Schutz, H., & Guralnick, R. P. (2007). Postcranial element shape and function: Assessing locomotor mode in extant and extinct mustelid carnivorans. Zoological Journal of the Linnean Society, 150(4), 895–914.

    Article  Google Scholar 

  • Slater, G. J., Harmon, L. J., & Alfaro, M. E. (2012). Integrating fossils with molecular phylogenies improves inference of trait evolution. Evolution, 66(12), 3931–3944.

    Article  PubMed  Google Scholar 

  • Stein, B. R. (1988). Morphology and allometry in several genera of semiaquatic rodents (Ondatra, Nectomys, and Oryzomys). Journal of Mammalogy, 69(3), 500–511. https://doi.org/10.2307/1381341.

    Google Scholar 

  • Tarasoff, F., Bisaillon, A., Piérard, J., & Whitt, A. P. (1972). Locomotory patterns and external morphology of the river otter, sea otter, and harp seal (Mammalia). Canadian Journal of Zoology, 50(7), 915–929.

    Article  CAS  PubMed  Google Scholar 

  • Thewissen, J. G. M., Cohn, M. J., Stevens, L. S., Bajpai, S., Heyning, J., & Horton, W. E. (2006). Developmental basis for hind-limb loss in dolphins and origin of the cetacean bodyplan. Proceedings of the National Academy of Sciences, 103(22), 8414–8418.

    Article  CAS  Google Scholar 

  • Thewissen, J. G. M., & Fish, F. E. (1997). Locomotor evolution in the earliest cetaceans: Functional model, modern analogues, and paleontological evidence. Paleobiology, 23(4), 482–490.

    Article  Google Scholar 

  • Van Valkenburgh, B. (1987). Skeletal indicators of locomotor behavior in living and extinct carnivores. Journal of Vertebrate Paleontology, 7(2), 162–182.

    Article  Google Scholar 

  • Wiley, D. F., Amenta, N., Alcantara, D. A., Ghosh, D., Kil, Y. J., Delson, E., et al. (2005). Evolutionary morphing. In Visualization, 2005. VIS 05. IEEE (pp. 431–438). Minneapolis: IEEE. Retrieved November 25, 2017, fromhttp://ieeexplore.ieee.org/xpls/abs_all.jsp?arnumber=1532826.

  • Williams, T. M. (1983a). Locomotion in the North American mink, a semi-aquatic mammal. II. The effect of an elongate body on running energetics and gait patterns. Journal of Experimental Biology, 105(1), 283–295.

    CAS  PubMed  Google Scholar 

  • Williams, T. M. (1983b). Locomotion in the North American mink, a semi-aquatic mammal. I. Swimming energetics and body drag. Journal of Experimental Biology, 103(1), 155–168.

    CAS  PubMed  Google Scholar 

  • Williams, T. M., Ben-David, M., Noren, S., Rutishauser, M., McDonald, K., & Heyward, W. (2002). Running energetics of the North American river otter: Do short legs necessarily reduce efficiency on land? Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology, 133(2), 203–212.

    Article  Google Scholar 

  • Young, N. M., & Hallgrímsson, B. (2005). Serial homology and the evolution of mammalian limb covariation structure. Evolution, 59(12), 2691–2704.

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors want to thank all the collection curators for the loan of the specimens. Suzanne Peurach of the National Museum of Natural History, Washington; Judith Marie Chupasko of the Museum of Comparative Zoology, Harvard; Loïc Costeur of the Naturhistorisches Museum, Basel; Christiane Funk and Frieder Mayer of the Museum für Naturkunde, Berlin; Link E. Olson and Aren Gunderson of the University of the Alaska Museum, Fairbanks; Géraldine Véron, Jacques Cuisin, Julie Villemain, and Céline Bens of the Muséum National d’Histoire Naturelle, Paris; Stefan Merker of the Staatliches Museum für Naturkunde, Stuttgart; Willem Wendelen of the Royal Museum for Central Africa, Tervuren. The authors are grateful to Amandine Blin, Michel Baylac for the access to the MNHN platform for morphometrics (UMS 2700) and for their advices. LB-D thanks the doctoral school ‘Frontières du vivant’ and the Bettencourt Schueller foundation. LB-D, AIH and AnH received financial support from the ANR-13-PDOC-0011. A-CF thanks the Marie-Skłodowska Curie fellowship (EU project 655694 – GETAGRIP) for funding.

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Botton-Divet, L., Houssaye, A., Herrel, A. et al. Swimmers, Diggers, Climbers and More, a Study of Integration Across the Mustelids’ Locomotor Apparatus (Carnivora: Mustelidae). Evol Biol 45, 182–195 (2018). https://doi.org/10.1007/s11692-017-9442-7

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