Geometric morphometrics shows differences and similarities in skull shape between the red and giant pandas

Journal of Zoology

Volumn 286, Issue 4, 2012, Pages 293-302

  Figueirido, B ^a,b   Serrano Alarcon F J ^a   Palmqvist, P ^a  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b BROWN UNIVERSITY   (United States)

Author keywords

Ailuropoda melanoleuca; Aiulurus fulgens; Biomechanical constraints; Convergent evolution; Landmark based morphometrics; Skull morphology

Indexed keywords

ADAPTATION; BEAR; BIOMARKER; BIOMETRY; CARNIVORE; CONVERGENT EVOLUTION; FOSSIL RECORD; HOMOLOGY; MORPHOLOGY; MORPHOMETRY; NATURAL SELECTION; PHYLOGENETICS; SHAPE; SKULL; SPECIALIST; TAXONOMY;

AILURIDAE; AILUROPODA; AILUROPODA MELANOLEUCA; AILURUS FULGENS; PROCYONIDAE; URSIDAE;

EID: 84859214157     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/j.1469-7998.2011.00879.x     Document Type: Article

References (75)

1. Abouheif, E. (2008). Parallelism as the pattern and process of mesoevolution. Evol. Dev. 10, 3-5.
2. Adams, D.C., Rohlf, F.J. & Slice, D. (2004). Geometric morphometrics: ten years of progress following the 'revolution'. Ital. J. Zool. 71, 5-16.
3. Antón, M., Salesa, M.J., Pastor, J.F., 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.
4. Arendt, J. & Reznick, D. (2008). Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23, 26-32.
5. Bardenfleth, K.S. (1913). On the systematic position of Aeluropus melanoleucusfMindeskr. Japetus Steenstrup. 17, 1-15.
6. Beddard, F.E. (1902). Cambridge natural history, 10: Mammalia. London: Macmillan.
7. Bininda-Emonds, O.R., Gittleman, J.L. & Purvis, A. (1999). Building large trees by combining phylogenetic information: a complete phylogeny of extant Carnivora (Mammalia). Biol. Rev. 74, 143-175.
8. Bookstein, F.L. (1991). Morphometric tools for landmarks data: geometry and biology. London: Cambridge University Press.
9. Brakefield, P.M. (2006). Evo-devo and constraints on selection. Trends Ecol. Evol. 21, 362-368.
10. Chorn, J. & Hoffmann, R.S. (1978). Ailuropoda melanoleuca Mamm. Spec. 110, 1-6.
11. Christiansen, P. & Wroe, S. (2007). Bite forces and evolutionary adaptations to feeding ecology in carnivores. Ecology 88, 347-358.
12. Davis, D.D. (1964). The giant panda: a morphological study on evolutionary mechanisms. Fieldiana, Geol. 3, 1-339.
13. Delisle, I. & Strobeck, C. (2005). A phylogeny of the Caniformia (order Carnivora) based on 12 complete protein-coding mitochondrial genes. Mol. Phylogenet. Evol. 37, 192-201.
14. Desutter-Grandcolas, L., Lengendre, F., Grandcolas, P., Robillard, T. & Murienne, J. (2005). Convergence and parallelism: is a new life ahead of old concepts? Cladistics 21, 51-61.
15. Dierenfeld, E.S., Hintz, H.F., Robertson, J.B., Van Soest, P.J. & Oftedal, O.T. (1982). Utilization of bamboo by the giant panda. J. Nutr. 112, 636-641.
16. Dryden, I.L. & Mardia, K.V. (1998). Statistical Shape Analysis. Chichester: John Wiley & Sons.
17. Edwards, M.S., Zhong, G., Wei, R. & Liu, X. (2006). Nutrition and dietary husbandry. In Giant pandas: biology, veterinary medicine and management: 101-158. Wildt, D.E., Zhang, A., Janssen, D.L. & Ellis, S. (Eds). Cambridge: Cambridge University Press.
18. Endo, H., Hama, N., Niizawa, N., Kimura, J., Itou, T., Koie, H. & Sakai, T. (2008). Three-dimensional imaging of the manipulating apparatus in the lesser panda and the giant panda. In Anatomical imaging: towards a new morphology: 61-66. Endo, H. & Frey, R. (Eds). Tokyo: Springer.
19. Endo, H., Makita, T., Sasaki, M., Arishima, K., Yamamoto, M. & Hayashi, Y. (1999). Comparative anatomy of the radial sesamoid bone in the polar bear (Ursus maritirnus), the brown bear (Ursus arctos) and the giant panda (Ailuropoda melanoleuca). J. Vet. Med. Sci. 61, 903-907.
20. Endo, H., Sasaki, M., Hayashi, Y., Koie, H., Yamaya, Y. & Kimura, J. (2001a). Carpal bone movements in gripping action of the giant panda (Ailuropoda melanoleuca). J. Anat. 198, 243-246.
21. Endo, H., Sasaki, M., Kogiku, H., Yamamoto, M. & Arishima, K. (2001b). Radial sesamoid bone as a part of the manipulation system in the lesser panda (Ailurus fulgens). Ann. Anat. 183, 181-184.
22. Endo, H., Sasaki, N., Yamagiwa, D., Uetake, Y., Kurohmaru, M. & Hayashi, Y. (1996). Functional anatomy of the radial sesamoid bone in the giant panda (Ailuropoda melanoleuca). J. Anat. 189, 587-592.
23. Figueirido, B., MacLeod, N., Krieger, J., De Renzi, M., Pérez-Claros, J.A. & Palmqvist, P. (2011b). Constraint and adaptation in the evolution of carnivoran skull shape. Paleobiology 37, 490-518.
24. Figueirido, B., Palmqvist, P. & Pérez-Claros, J.A. (2009). Ecomorphological correlates of craniodental variation in bears and paleobiological implications for extinct taxa: an approach based on geometric morphometrics. J. Zool. (Lond.) 277, 70-80.
25. Figueirido, B., Palmqvist, P., Pérez-Claros, J.A. & Dong, W. (2011a). Cranial shape transformation in the evolution of the giant panda (Ailuropoda melanoleuca). Naturwissenschaften 98, 107-116.
26. Figueirido, B., Serrano-Alarcón, F.J., Slater, G.J. & Palmqvist, P. (2010). Shape at the cross-roads: homoplasy and history in the evolution of the carnivoran skull towards herbivory. J. Evol. Biol. 23, 2579-2594.
27. Flower, W.H. & Lydekker, R. (1891). An introduction to the study of mammals living and extinct. London: Adam and Charles Black.
28. Flynn, J.J., Finarelli, J.A., Zehr, S., Hsu, J. & Nedbal, M. (2005). Molecular phylogeny of the Carnivora (Mammalia): assessing the impact of increased sampling on resolving enigmatic relationships. Syst. Biol. 54, 317-337.
29. Flynn, J.J. & Nedbal, M. (1998). Phylogeny of the Carnivora (Mammalia): congruence vs. incompatibility among multiple data sets. Mol. Phylogenet. Evol. 9, 414-426.
30. Flynn, J.J., Nedbal, M., Dragoo, J. & Honeycutt, L. (2000). Whence the red panda? Mol. Phylogenet. Evol. 17, 190-199.
31. Flynn, J.J., Neff, N.A. & Tedford, R.H. (1988). Phylogeny of the Carnivora. In The phylogeny and classification of the tetrapods. Vol. 2, Mammals: 73-116. Benton, M. (Ed.). Oxford: Clarendon.
32. Ginsburg, L. (1982). Sur la position systématique du petit panda, Ailurus fulgens (Carnivora, Mammalia). Geobios (Mem. Spec.) 6, 247-258.
33. Ginsburg, L. (1999). Order Carnivora. In The Miocene land mammals of Europe: 109-148. Rössner, G. & Heissig, K. (Eds). Munich: Pfeil.
34. Gittleman, J.L. (1994). Are the pandas successful specialists or evolutionary failures? BioScience 44, 456-464.
35. Goldman, D., Giri, P.R. & O'Brien, S.J. (1989). Molecular genetic-distance estimates among the Ursidae as indicated by one- and two-dimensional protein electrophoresis. Evolution 43, 282-295.
36. Goswami, A., Milne, N. & Wroe, S. (2011). Biting through constraints: cranial morphology, disparity and convergence across living and fossil carnivorous mammals. Proc. Roy. Soc. B Biol. Sci. 278, 1831-1839.
37. Gould, S.J. (1978). The panda's peculiar thumb. Nat. Hist. 87, 20-30.
38. Gould, S.J. (2002). The structure of evolutionary theory. Cambridge: Harvard University Press.
39. Gregory, W.K. (1936). On the phylogenetic relationships of the giant panda (Ailuropoda) to other arctoid carnivora. Am. Mus. Novit. 878, 1-29.
40. Hall, B.K. (2007). Homoplasy and homology: dichotomy or continuum? J. Hum. Evol. 52, 473-479.
41. Hunt, R.M. (1974). The auditory bulla in Carnivora: an anatomical basis for reappraisal of carnivore evolution. J. Morphol. 143, 21-76.
42. Jin, C., Ciochon, R.L., Dong, W., Hunt, R.M., Liu, J., Jaeger, M. & Zhu, Q. (2007). The first skull of the earliest giant panda. Proc. Natl. Acad. Sci. U.S.A. 104, 10932-10937.
43. Klingenberg, C.P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Mol. Ecol. Resour 11, 353-357.
44. Klingenberg, C.P., Duttke, S., Whelan, S. & Kim, M. (2012). Developmental plasticity, morphological variation and evolvability: a multilevel analysis of morphometric integration in the shape of compound leaves. Journal of Evolutionary Biology (Online DOI: 10.1111/j.1420-9101.2011.02410.x)
45. Lankester, E.R. & Lydeker, R. (1901). On the affinities of Aeluropus melanoleucus Trans. Soc. Lond. 8, 163-171.
46. Leander, B.S. (2008). Different modes of convergent evolution reflects phylogenetic distances: a reply to Arendt and Reznick. Trends Ecol. Evol. 23, 481-482.
47. Ledje, C. & Arnason, U. (1996). Phylogenetic analyses of complete cytochromeb genes of the order Carnivora with particular emphasis on the Caniformia. J. Mol. Evol. 42, 135-144.
48. Li, Y. (Ed.) (1986). Morphology of the giant panda: systematic anatomy and organ-histology. Beijing: Science Press.
49. Madsen, O., Scally, M., Douady, C.J., Kao, D.J., DeBry, R.W., Adkins, R., Amrine, H.M., Stanhope, M.J., de Jong, W.W. & Springer, M.S. (2001). Parallel adaptive radiations in two major clades of placental mammals. Nature 409, 610-614.
50. Marugán-Lobón, J. & Buscalioni, A.D. (2004). Geometric morphometrics in macroevolution: morphological diversity of the skull in modern avian form in contrast to some theropod dinosaurs. In Morphometrics: applications in biology and paleontology: 157-171. Elewa, A.M.T. (Ed.). New York: Springer.
51. Marugán-Lobón, J. & Buscalioni, A.D. (2006). Avian skull morphological evolution: exploring exo- and endocranial covariation with two-block partial least squares. Zoology 109, 217-230.
52. McLellan, B. & Reiner, D.C. (1994). A review of bear evolution. Int. Conf. Bear Res. Manage. 9, 85-96.
53. Meyer, A. (1999). Homology and homoplasy: the retention of genetic programmes. In homology: 141-157. Bock, G. (Ed.). Chichester: Wiley & Son.
54. Mivart, G. (1885). On the anatomy, classification, and distribution of the Arctoidea. Proc. Zool. Soc. Lond. 1885, 340-404.
55. Nevo, E. (2001). Evolution of genome-phenome diversity under environmental stress. Proc. N.Y. Acad. Sci. 98, 623-6240.
56. Pradhan, S., Saha, G.K. & Khan, J.A. (2001). Ecology of the red panda Ailurus fulgens in the Singhalila National Park, Darjeeling, India. Biol. Conserv. 98, 11-18.
57. Radinsky, L.A. (1984). Basicranial axis length v. skull length in analysis of carnivore skull shape. Biol. J. Linn. Soc. 22, 31-41.
58. Raven, H.C. (1936). Notes on the anatomy on the viscera of the giant panda (Ailuropoda melanoleuca). Am. Mus. Novit. 877, 1-223.
59. Roberts, M.S. & Gittleman, J.L. (1984). Ailurus fulgens Mamm. Spec. 222, 1-8.
60. Rohlf, F.J. (2008). TpsDig, ver. 2.11 Digitize landmarks and outlines. Department of Ecology and Evolution, State University of New York at Stony Brook [computer program and documentation].
61. Salesa, M.J., Antón, M., Peigné, S. & Morales, J. (2006b). Evidence of a false thumb in a fossil carnivore clarifies the evolution of pandas. Proc. Natl. Acad. Sci. U.S.A. 109, 379-382.
62. Salesa, M.J., Siliceo, G., Antón, M., Abella, J., Montoya, P. & Morales, J. (2006a). Anatomy of the 'false thumb' of Tremarctos ornatus (Carnivora, Ursidae, Tremarctinae): phylogenetic and functional implications. Estud. Geol. 62, 389-394.
63. Schaller, G.B. (1993). The last panda. Chicago: University of Chicago Press.
64. Schaller, G.B., Qitao, T., Johnson, K.G., Wang, X., Shen, H. & Hu, J. (1989). The feeding ecology of giant pandas and Asiatic black bears in the Tangjiahe Reserve, China. In Carnivore behaviour, ecology, and evolution, Vol. 1: 212-241. Gittleman, J.L. (Ed.). Ithaca: Cornell University Press.
65. Segall, W. (1943). The auditory region of the arctoid carnivores. Fieldiana, Zool. 29, 33-59.
66. Simpson, G.G. (1945). The principles of classification and classification of mammals. Bull. Am. Mus. Nat. Hist. 85, 1-350.
67. Sims, J.A., Parsons, J.L., Bissell, H.A., Ouellette, J.R. & Rude, B.J. (2007). Determination of bamboo-diet digestibility and fecal output by giant pandas. Ursus 18, 38-45.
68. Tagle, D.A., Miyamoto, M.M., Goodman, M., Hofmann, O., Braunitzer, G., Göltenboth, R. & Jalanka, H. (1986). Hemoglobin of pandas: phylogenetic relationships of carnivores as ascertained with protein sequence data. Naturwissenschaften 73, 512-514.
69. Wayne, R.K., Benveniste, R.E., Janczewski, D.N. & O'Brien, S.J. (1989). Molecular and biochemical evolution of the Carnivora. In Carnivore behaviour, ecology, and evolution, Vol. 1: 465-494. Gittleman, J.L. (Ed.). Ithaca: Cornell University Press.
70. de Winter, W. & Oxnard, C.E. (2001). Evolutionary radiations and convergences in the structural organization of mammalian brains. Nature 409, 710-714.
71. Wozencraft, W.C. (1989). The phylogeny of the recent Carnivora. In Carnivore behaviour, ecology, and evolution, Vol. 1: 495-535. Gittleman, J.L. (Ed.). Ithaca: Cornell University Press.
72. Wroe, S. & Milne, N. (2007). Convergence and remarkably consistent constraint in the evolution of carnivore skull shape Evolution 61, 1251-1260.
73. Wyss, A.R. & Flynn, J.J. (1993). A phylogenetic analysis and definition of the Carnivora. In Mammal phylogeny: placentals: 32-52. Szalay, F., Novacek, M. & McKenna, M. (Eds). New York: Springer-Verlag.
74. Zhang, S., Pan, R., Li, M., Oxnard, C. & Wei, F. (2007). Mandible of the giant panda (Ailuropoda melanoleuca) compared with other Chinese carnivores: functional adaptation. Biol. J. Linn. Soc. 92, 449-456.
75. Zhu, L., Wua, Q., Dai, J., Zhang, S. & Wei, F. (2011). Evidence of cellulose metabolism by the giant panda gut microbiome. Proc. Natl. Acad. Sci. U.S.A. (Online DOI:10.1073/pnas.1017956108)