Getting a grip on the evolution of grasping in musteloid carnivorans: A three-dimensional analysis of forelimb shape

Journal of Evolutionary Biology

Volumn 26, Issue 7, 2013, Pages 1521-1535

  Fabre, A C ^a,b,c   Cornette, R ^d   Slater, G ^e   Argot, C ^a   Peigne S ^a   Goswami, A ^c   Pouydebat, E ^d  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^e SMITHSONIAN INSTITUTION   (United States)

Author keywords

Ecomorphology; Geometric morphometrics; Grasping; Musteloids

Indexed keywords

ADAPTATION; BEHAVIORAL ECOLOGY; BIPEDALISM; CARNIVORE; HUMAN EVOLUTION; LIFESTYLE; MAMMAL; SPECIES DIVERSITY;

ADAPTATION; ANIMAL; ARTICLE; CARNIVORY; ECOMORPHOLOGY; EVOLUTION; FORELIMB; GEOMETRIC MORPHOMETRICS; GRASPING; HAND STRENGTH; HISTOLOGY; LOCOMOTION; MUSTELIDAE; MUSTELOIDS; PHYSIOLOGY; RADIUS; ULNA;

ECOMORPHOLOGY; GEOMETRIC MORPHOMETRICS; GRASPING; MUSTELOIDS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; CARNIVORY; FORELIMB; HAND STRENGTH; LOCOMOTION; MUSTELIDAE; RADIUS; ULNA;

MAMMALIA;

EID: 84880701008     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12161     Document Type: Article

References (61)

1. Andersson, K. 2003. Locomotor Evolution in the Carnivora (Mammalia): Evidence From the Elbow Joint. University of Uppsala, Sweden.
2. Andersson, K. 2004. Elbow-joint morphology as a guide to forearm function and foraging behaviour in mammalian carnivores. Zool. J. Linn. Soc. 142: 91-104.
3. Andersson, K. 2005. Were there pack-hunting canids in the Tertiary, and how can we know? Paleobiology 31: 56-72.
4. Antón, M., Salesa, M.J., Pastor, J., Peigné, S. & Morales, J. 2006. Implications of the functional anatomy of the hand and forearm of Ailurus fulgens (Carnivora, Ailuridae) for the evolution of the "false-thumb" in pandas. J. Anat. 209: 757-764.
5. Argot, C. 2001. Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. J. Morphol. 247: 51-79.
6. Baylac, M. 2012. Rmorph: a R geometric and multivariate morphometrics library. Available from the author: baylac@mnhn.fr.
7. Bookstein, F.L. 1997. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med. Image Anal. 1: 225-243.
8. Bookstein, F.L. & Green, W.D.K. 2002. User's Manual, EWSH3.19. URL http://brainmap.stat.washington.edu/edgewarp.
9. Brácha, V., Zhuravin, I.A. & Bures, J. 1990. The reaching reaction in the rat: a part of the digging pattern? Behav. Brain Res. 36: 53-64.
10. Byrne, R.W., Corp, N. & Byrne, J.M. 2001. Manual dexterity in the gorilla: bimanual and digit role differentiation in a natural task. Anim. Cogn. 4: 347-361.
11. Candela, A.M. & Picasso, M.B.J. 2008. Functional anatomy of the limbs of Erethizontidae (Rodentia, Caviomorpha): Indicators of locomotor behavior in Miocene porcupines. J. Morphol. 269: 552-593.
12. Christel, M. 1993. Grasping techniques and hand preference in Hominoidea. In: Hands of Primates (H. Preuschoft, D.J. Chivers, eds), pp. 91-108. Springer, Wien, New York.
13. Corp, N. & Byrne, R.W. 2002. The Ontogeny of manual skill in wild chimpanzees: evidence from feeding on the fruit of Saba Florida. Behaviour 139: 137-168.
14. Crast, J., Fragaszy, D., Hayashi, M. & Matsuzawa, T. 2009. Dynamic in-hand movements in adult and young juvenile chimpanzees (Pan troglodytes). Am. J. Phys. Anthropol. 138: 274-285.
15. Eizirik, E., Murphy, W.J., Koepfli, K.-P., Johnson, W.E., Dragoo, J.W., Wayne, R.K. et al. 2010. Pattern and timing of diversification of the mammalian order Carnivora inferred from multiple nuclear gene sequences. Mol. Phylogenet. Evol. 56: 49-63.
16. Endo, H., Hama, N., Niizawa, N., Kimura, J. & Itou, T. 2007. Three-dimensional analysis of the manipulation system in the lesser panda. Mammal Study 32: 99-103.
17. Ewer, R.F. 1973. The Carnivores. Cornell University Press, Ithaca, New York.
18. Felsenstein, J. 1985. Phylogenies and the comparative method. Amer. Nat. 125: 1-15.
19. Flores, D.A. & Díaz, M.M. 2009. Postcranial skeleton of Glironia venusta (Didelphimorphia, Didelphidae, Caluromyinae): Description and Functional Morphology. Zoosyst. Evol. 85: 311-339.
20. Garland, T., Dickerman, A.W., Janis, C.M. & Jones, J.A. 1993. Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42: 265-292.
21. Godinot, M. 1991. Approche fonctionnelle des mains des primates paléogènes. Geobios 24: 161-173.
22. Godinot, M. 2007. Primate origins: a reappraisal of historical data favoring tupaiid affinities. In: Primate Origins: Adaptations and Evolution (M.J. Ravosa, M. Dagosto, eds), pp. 83-133. Springer Press, New York.
23. Gonyea, W.J. 1978. Functional implications of felid forelimb morphology. Acta Anat. 102: 111-121.
24. Gray, L.A., O'Reilly, J.C. & Nishikawa, K.C. 1997. Evolution of forelimb movement patterns for prey manipulation in anurans. J. Exp. Zool. 277: 417-424.
25. Grillner, S. & Wallén, P. 1985. Central pattern generators for locomotion, with special reference to vertebrates. Annu. Rev. Neurosci. 8: 233-261.
26. Grzimek, B. 1990. Grzimek's Encyclopedia of Mammals. McGraw-Hill Publishing Company, New York.
27. Gunz, P., Mitteroecker, P. & Bookstein, F.L. 2005 Semilandmarks in three dimensions. In: Modern Morphometrics in Physical Anthropology (D.E. Slice, ed.), pp. 73-98. Kluwer Academic/Plenum Publishers, New York.
28. Halenar, L.B. 2011. Reconstructing the locomotor repertoire of Protopithecus brasiliensis. II. Forelimb morphology. Anat. Rec. 294: 2048-2063.
29. Harmon, L.J., Weir, J.T., Brock, C.D., Glor, R.E. & Challenger, W. 2008. GEIGER: investigating evolutionary radiations. Bioinformatics 24: 129-131.
30. Harvey, P.H. & Pagel, M.D. 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford, UK.
31. Ivanco, T.L., Pellis, S.M. & Whishaw, I.Q. 1996. Skilled forelimb movements in prey catching and in reaching by rats (Rattus norvegicus) and opossums (Monodelphis domestica): relations to anatomical differences in motor systems. Behav. Brain Res. 79: 163-181.
32. Iwaniuk, A.N. & Whishaw, I.Q. 1999. How skilled are the skilled limb movements of the raccoon (Procyon lotor)? Behav. Brain Res. 99: 35-44.
33. Iwaniuk, A.N. & Whishaw, I.Q. 2000. On the origin of skilled forelimb movements. Trends Neurosci. 23: 372-376.
34. Iwaniuk, A.N., Pellis, S.M. & Whishaw, I.Q. 1999. The relationship between forelimb morphology and behaviour in North American carnivores (Carnivora). Can. J. Zool. 77: 1064-1074.
35. Iwaniuk, A.N., Pellis, S.M. & Whishaw, I.Q. 2000. The relative importance of body size, phylogeny, locomotion, and diet in the evolution of forelimb dexterity in fissiped carnivores (Carnivora). Can. J. Zool. 78: 1110-1125.
36. Lanyon, L.E. 1980. The influence of function on the development of bone curvature. An experimental study on the tibia rat. J. Zool. 198: 457-466.
37. MacLeod, N. & Rose, K.D. 1993. Inferring locomotor behavior in paleogene mammals via eigenshape analysis. Am. J. Sci. 293-A: 300-355.
38. Maddison, W.P. & Maddison, D.R. 2011. Mesquite: a modular system for evolutionary analysis. Version 2.75. URL http://mesquiteproject.org.
39. Manzano, A.S., Abdala, V. & Herrel, A. 2008. Morphology and function of the forelimb in arboreal frogs: specializations for grasping ability? J. Anat. 213: 296-307.
40. Nowak, R.M. 2005. Walker's Carnivores of the World. The Johns Hopkins University Press, Baltimore.
41. Parr, W.C.H., Wroe, S., Chamoli, U., Richards, H.S., McCurry, M.R., Clausen, P.D. et al. 2012. Toward integration of geometric morphometrics and computational biomechanics: new methods for 3D virtual reconstruction and quantitative analysis of Finite Element Models. J. Theor. Biol. 301: 1-14.
42. Pouydebat, E., Laurin, M., Gorce, P. & Bels, V. 2008. Evolution of grasping among anthropoids. J. Evol. Biol. 21: 1732-1743.
43. Pouydebat, E., Gorce, P., Coppens, Y. & Bels, V. 2009. Biomechanical study of grasping according to the volume of the object: human versus non-human primates. J. Biomech. 42: 266-272.
44. Pouydebat, E., Reghem, E., Borel, A. & Gorce, P. 2011. Diversity of grip in adults and young humans and chimpanzees (Pan troglodytes). Behav. Brain Res. 218: 21-28.
45. R Development Core Team 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna: R Foundation for Statistical Computing, ISBN 3-900051-07-0. URL http://www.R-project.org.
46. Reghem, E., Tia, B., Bels, V. & Pouydebat, E. 2011. Food prehension and manipulation in Microcebus murinus (Prosimii, Cheirogaleidae). Folia Primatol. 82: 177-188.
47. Reghem, E., Byron, C., Bels, V. & Pouydebat, E. 2012. Hand posture in the grey mouse lemur during arboreal locomotion on narrow branches. J. Zool. 288: 76-81.
48. Revell, L.J. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3: 217-223.
49. Rohlf, F.J. & Slice, D. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Zool. 39: 40-59.
50. Rose, M.D. 1993. Functional anatomy of the elbow and forearm in primates. In: Postcranial Adaptations in non-Human Primates (D.L. Gebo, ed.), pp. 70-95. Northern Illinois Univ Press, DeKalb.
51. Sacrey, L.-A.R., Alaverdashvili, M. & Whishaw, I.Q. 2009. Similar hand shaping in reaching-for-food (skilled reaching) in rats and humans provides evidence of homology in release, collection, and manipulation movements. Behav. Brain Res. 204: 153-161.
52. Salesa, M.J., Antón, M., Peigné, S. & Morales, J. 2006. Evidence of a false thumb in a fossil carnivore clarifies the evolution of pandas. Proc. Natl. Acad. Sci. 103: 379-382.
53. Sargis, E.J. 2002. Functional morphology of the forelimb of tupaiids (Mammalia, Scandentia) and its phylogenetic implications. J. Morphol. 253: 10-42.
54. Sato, J.J., Wolsan, M., Minami, S., Hosoda, T., Sinaga, M.H., Hiyama, K. et al. 2009. Deciphering and dating the red panda's ancestry and early adaptive radiation of Musteloidea. Mol. Phylogenet. Evol. 53: 907-922.
55. Sato, J.J., Wolsan, M., Prevosti, F.J., D'Elía, G., Begg, C., Begg, K. et al. 2012. Evolutionary and biogeographic history of weasel-like carnivorans (Musteloidea). Mol. Phylogenet. Evol. 63: 745-757.
56. Schutz, H. & Guralnick, R.P. 2007. Postcranial element shape and function: assessing locomotor mode in extant and extinct mustelid carnivorans. Zool. J. Linn. Soc. 150: 895-914.
57. Slater, G.J., Harmon, L.J. & Alfaro, M.E. 2012. Integrating fossils with molecular phylogenies improves inference of trait evolution. Evolution 66: 3931-3944.
58. Sustaita, D., Pouydebat, E., Manzano, A., Abdala, V., Hertel, F. & Herrel, A. 2013. Getting a grip on tetrapod grasping: form, function, and evolution. Biol. Rev. Camb. Philos. Soc. 88: 380-405.
59. Szalay, F.S. & Sargis, E.J. 2001. Model-based analysis of postcranial osteology of marsupials from the Palaeocene of Itaboraí (Brazil) and the phylogenetics and biogeography of Metatheria. Geodiversitas 23: 139-302.
60. Wiley, D.F., Amenta, N., Alcantara, D.A., Ghosh, D., Kil, Y.J., Delson, E. et al. 2005. Evolutionary morphing. In: Proceedings of IEEE Visualization 2005 (VIS'05), 23-28 October 2005, pp. 431-438. Minneapolis, MN, USA.
61. Wilson, D.E. & Mittermeier, R.A. 2009. In: Handbook of the Mammals of the World (D.E. Wilson & R.A. Mittermeier, eds), pp. 1-728. Lynx Edicions, Barcelona.