A three-dimensional analysis of the morphological evolution and locomotor behaviour of the carnivoran hind limb

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Martín Serra, Alberto ^a   Figueirido, Borja ^a   Palmqvist, Paul ^a  

^a UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

Allometry; Carnivora; Convergence; Hind limb; Locomotion; Phenotypic evolution

Indexed keywords

BIOMECHANICS; BODY SIZE; BONE; CARNIVORE; LOCOMOTION; PHENOTYPIC PLASTICITY; PRINCIPAL COMPONENT ANALYSIS; THREE-DIMENSIONAL MODELING;

CARNIVORA; MAMMALIA;

ADAPTATION; ANIMAL; ARTICLE; BODY SIZE; BONES OF THE ARM AND HAND; BONES OF THE LEG AND FOOT; CARNIVORA; CLASSIFICATION; EVOLUTION; HISTOLOGY; LOCOMOTION; MAMMAL; PHYLOGENY; PHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; BODY SIZE; BONES OF LOWER EXTREMITY; BONES OF UPPER EXTREMITY; CARNIVORA; LOCOMOTION; MAMMALS; PHYLOGENY; PRINCIPAL COMPONENT ANALYSIS;

EID: 84902052930     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-14-129     Document Type: Article

References (81)

1. Ewer RF, The Carnivores Ithaca, NY: Cornell University Press 1973
2. Biewener AA, Animal Locomotion Oxford: Oxford University Press 2003
3. Wilson DE, Mittermeier RA, Handbook of the Mammals of the World Barcelona: Lynx Edicions Carnivores. 2009 1
4. Alexander RM, Principles of Animal Locomotion Princeton: Princeton University Press 2003
5. Walking and running. Hildebrand M, Functional Vertebrate Morphology Cambridge, MA: Harvard University Press, Hildebrand M, Bramble DM, Liem KF, Wake DB, 1985 38 57
6. Functional implications of felid forelimb morphology. Gonyea WJ, Acta Anat 1978 102 111 121 10.1159/000145627 685643 (Pubitemid 8358832)
7. Does metatarsal/femur ratio predict maximal running speed in cursorial mammals? Garland TJ, Janis CM, J Zool 1993 229 133 151 10.1111/j.1469-7998.1993. tb02626.x
8. Inferring locomotor behavior in Paleogene mammals via eigenshape analysis. MacLeod N, Rose KD, Am J Sci 1993 293 300 355 10.2475/ajs.293.A.300 (Pubitemid 23393898)
9. Were there mammalian pursuit predators in the Tertiary? Dances with wolf avatars. Janis CM, Wilhelm PB, J Mammal Evol 1993 1 103 125 10.1007/BF01041590
10. Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. Argot C, J Morphol 2001 247 51 79 10.1002/1097-4687(200101)247:1<51: :AID-JMOR1003>3.0.CO;2-# 11124686 (Pubitemid 32139559)
11. Skeletal indicators of locomotor adaptations in living and extinct rodents. Samuels JX, Van Valkenburgh B, J Morphol 2008 269 1387 1411 10.1002/jmor.10662 18777567
12. Reconstructing the locomotor repertoire of Protopithecus brasiliensis. II. Forelimb morphology. Halenar LB, Anat Rec 2011 294 2048 2063 10.1002/ar.21499
13. Form and function within a phylogenetic framework: locomotory habits of extant predators and some Miocene Sparassodonta (Metatheria). Ercoli MD, Prevosti FJ, Álvarez A, Zool J Linn Soc 2012 165 224 251 10.1111/j.1096-3642.2011.00793.x
14. On their knees: distal femur asymmetry in ungulates and its relationship to body size and locomotion. Janis CM, Shoshitaishvili B, Kambic R, Figueirido B, J Vertebr Paleontol 2012 32 433 445 10.1080/02724634.2012.635737
15. Ontogenesis and morphological diversification. Alberch P, Am Zool 1980 20 653 667
16. Developmental constraints and evolution: a perspective from the Mountain Lake conference on development and evolution. Smith JM, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B, Lande R, Raup D, Wolpert L, Q Rev Biol 1985 60 265 287 10.1086/414425
17. Constraint. Schwenk K, Wagner GP, Key words and concepts in evolutionary developmental biology Cambridge, MA: Harvard University Press, Hall BK, Olson WM, 2003 52 61
18. Body support, scaling and allometry. Alexander RM, Functional Vertebrate Morphology Cambridge, MA: Harvard University Press, Hildebrand M, Bramble DM, Liem KF, Wake DB, 1985 38 57
19. Models and the scaling of energy costs for locomotion. Alexander RM, J Exp Biol 2005 208 1645 1652 10.1242/jeb.01484 15855396 (Pubitemid 40697613)
20. Locomotory stresses in the limb bones of two small mammals: the ground squirrel and chipmunk. Biewener AA, J Exp Biol 1983 103 135 154
21. Biomechanical consequences of scaling. Biewener AA, J Exp Biol 2005 208 1665 1676 10.1242/jeb.01520 15855398 (Pubitemid 40697615)
22. Three-dimensional geometric analysis of felid limb bone allometry. Doube M, Conroy AW, Christiansen P, Hutchinson JR, Shefelbine S, PLoS One 2009 4 4742 10.1371/journal.pone.0004742 19270749
23. Influence of body mass on the shape of forelimb in musteloid carnivorans. Fabre AC, Cornette R, Peigné S, Goswami A, Biol J Linn Soc Lond 2013 110 91 103 10.1111/bij.12103
24. Skeletal indicators of locomotor behavior in living and extinct carnivores. Van Valkenburgh B, J Vertebr Paleontol 1987 7 162 182 10.1080/02724634.1987.10011651
25. Postcranial element shape and function: Assessing locomotor mode in extant and extinct mustelid carnivorans. Schutz H, Guralnick RP, Zool J Linn Soc 2007 150 895 914 10.1111/j.1096-3642.2007.00303.x (Pubitemid 47220959)
26. Humeral epiphyseal shape in the felidae: the influence of phylogeny, allometry, and locomotion. Walmsley A, Elton S, Louys J, Bishop LC, Meloro C, J Morphol 2012 273 1424 1438 10.1002/jmor.20084 23065662
27. Postcranial morphology and the locomotor habits of living and extinct carnivorans. Samuels JX, Meachen JA, Sakay SA, J Morphol 2013 274 121 146 10.1002/jmor.20077 22972188
28. Getting a grip on the evolution of grasping in musteloid carnivorans: a three-dimensional analysis of forelimb shape. Fabre AC, Cornette R, Slater G, Argot C, Peigné S, Goswami A, Pouydebat E, J Evol Biol 2013 26 1521 1535 10.1111/jeb.12161 23662594
29. Locomotor behaviour in Plio-Pleistocene sabre-tooth cats: a biomechanical analysis. Anyonge W, J Zool 1996 238 395 413 10.1111/j.1469-7998.1996.tb05402.x (Pubitemid 126567684)
30. The evolution of cursorial carnivores in the Tertiary: implications of elbow-joint morphology. Andersson K, Werdelin L, Proc R Soc Lond B 2003 270 163 165 10.1098/rsbl.2003.0070
31. Elbow-joint morphology as a guide to forearm function and foraging behaviour in mammalian carnivores. Andersson K, J Zool 2004 142 91 104 (Pubitemid 39252070)
32. Were there pack-hunting canids in the Tertiary, and how can we know? Andersson K, Paleobiology 2005 31 56 72 (Pubitemid 40133963)
33. Forelimb indicators of prey-size preference in the Felidae. Meachen-Samuels JA, Van Valkenburgh B, J Morphol 2009 270 729 744 10.1002/jmor.10712 19123240
34. Radiographs reveal exceptional forelimb strength in the sabertooth cat, Smilodon fatalis. Meachen-Samuels JA, Van Valkenburgh B, PLoS One 2010 5 11412 10.1371/journal.pone.0011412 20625398
35. The predatory behaviour of the thylacine: Tasmanian tiger or marsupial wolf? Figueirido B, Janis CM, Biol Lett 2011 7 937 940 10.1098/rsbl.2011.0364 21543392
36. Morphological convergence of the prey-killing arsenal of sabertooth predators. Meachen-Samuels JA, Paleobiology 2012 38 715 728
37. Updating the evolutionary history of Carnivora (Mammalia): a new species-level supertree complete with divergence time estimates. Nyakatura K, Bininda-Emonds ORP, BMC Biol 2012 10 12 10.1186/1741-7007-10-12 22369503
38. A three-dimensional analysis of morphological evolution and locomotor performance of the carnivoran forelimb. Martin-Serra A, Figueirido B, Palmqvist P, PLoS One 2014 9 85574 10.1371/journal.pone.0085574 24454891
39. Acceleration and balance in trotting dogs. Lee DV, Bertram JE, Todhunter RJ, J Exp Biol 1999 202 3565 3573 10574733 (Pubitemid 30044675)
40. Ground forces applied by galloping dogs. Walter RM, Carrier DR, J Exp Biol 2007 210 208 216 10.1242/jeb.02645 17210958
41. Ecological correlates of hind-limb length in the Carnivora. Harris MA, Steudel K, J Zool 1997 241 381 408 10.1111/j.1469-7998.1997.tb01966.x
42. Exploring the mechanical basis for acceleration: pelvic limb locomotor function during accelerations in racing greyhounds (Canis familiaris). Williams SB, Usherwood JR, Jespers K, Channon AJ, Wilson AM, J Exp Biol 2009 212 550 565 10.1242/jeb.018093 19181903
43. The relationship between forelimb morphology and behaviour in North American carnivores (Carnivora). Iwaniuk AN, Pellis SM, Whishaw IQ, Can J Zool 1999 77 1064 1074 10.1139/z99-082
44. Size and shape in biology. McMahon TA, Science 1973 179 1201 1204 10.1126/science.179.4079.1201 4689015
45. Differential scaling of the long bones in the terrestrial Carnivora and other mammals. Bertram JEA, Biewener AA, J Morphol 1990 204 157 169 10.1002/jmor.1052040205 2348461 (Pubitemid 20234533)
46. Limbs in mammalian evolution. Polly PD, Fins into Limbs: Evolution, Development and Transformation Chicago: University of Chicago Press, Hall BK, 2007 245 268
47. Kardong KV, Vertebrates: comparative anatomy, function, evolution Boston: McGraw-Hill 2006
48. Locomotor adaptations by carnivores. Taylor ME, Carnivore Behaviour, Ecology, and Evolution New York: Cornell University Press, Gittleman JL, 1989 I 382 409
49. Scaling of cursoriality in mammals. Steudel K, Beattie J, J Morphol 1993 217 55 63 10.1002/jmor.1052170105 8411186
50. What is a cursorial mammal? Stein BR, Casinos A, J Zool 1997 242 85 92
51. Functional anatomy of the forelimb in Promegantereon ogygia (Felidae, Machairodontinae, Smilodontini) from the Late Miocene of Spain and the origins of the sabre-toothed felid model. Salesa MJ, Antón M, Turner A, Morales J, J Anat 2010 216 381 396 10.1111/j.1469-7580.2009.01178.x 20039979
52. Three ways to be a saber-toothed cat. Martin LD, Babiarz JP, Naples VL, Hearst J, Naturwissenschaften 2000 87 41 44 10.1007/s001140050007 10663132 (Pubitemid 30058789)
53. Locomotor diversity within past and present guilds of large predatory mammals. Van Valkenburgh B, Paleobiology 1985 11 406 428 (Pubitemid 17248462)
54. Deja vu: the evolution of feeding morphologies in the Carnivora. Van Valkenburgh B, Integr Comp Biol 2007 47 147 163 10.1093/icb/icm016 21672827 (Pubitemid 351176746)
55. Creodonta. Gunnell GF, Evolution of Tertiary mammals of North America: Volume 1, terrestrial carnivores, ungulates, and ungulate like mammals Cambridge: Cambridge University Press, Janis CM, Scott KM, Jacobs LL, 1998 91 109
56. Barone R, Anatomie Compare des Mammifères Domestiques, Ostéologie, Volume 1 Paris: Vigot 1986
57. Homberger DG, Walker WF, Vertebrate dissection Belmont, CA: Brooks Cole 9 2004
58. Evolutionary Morphing. Wiley DF, Amenta N, Alcantara DA, Ghosh D, Kil YJ, Delson E, Harcourt-Smith W, Rohlf FJ, St John K, Hamann B, Proceedings of IEEE Visualization 2005 (VIS'05); Minneapolis 2005 431 438
59. Dryden IL, Mardia K, Statistical Analysis of Shape Chichester, UK: Wiley 1998
60. Klingenberg CP, MorphoJ Manchester: Faculty of Life Sciences, University of Manchester 2011 http://www.flywings.org.uk/MorphoJ-page.htm
61. Maddison WP, Maddison DR, Mesquite: a modular system for evolutionary analysis. Version 2.75 2011 http://mesquiteproject.org
62. Phylogeny of the Procyonidae (Mammalia: Carnivora): molecules, morphology and the great American interchange. Koepfli KP, Gompper ME, Eizirik E, Ho CC, Linden L, Maldonado JE, Wayne RK, Mol Phylogenet Evol 2007 43 1076 1095 10.1016/j.ympev.2006.10.003 17174109 (Pubitemid 46777382)
63. Paleontology and the comparative method: ancestral node reconstructions versus observed node values. Polly PD, Am Nat 2001 157 596 609 10.1086/320622 18707277 (Pubitemid 32546075)
64. Adaptive Zones and the Pinniped Ankle: a 3D Quantitative Analysis of Carnivoran Tarsal Evolution. Polly PD, Mammalian Evolutionary Morphology: A Tribute to Frederick S. Szalay Dordrecht, the Netherlands: Springer, Sargis E, Dagosto M, 2008 65 194
65. Ancestral state reconstruction of body size in the Caniformia (Carnivora, Mammalia): the effects of incorporating data from the fossil record. Finarelli JA, Flynn JJ, Syst Biol 2006 55 301 313 10.1080/10635150500541698 16611601
66. The evolution of body size, Cope's rule and the origin of amniotes. Laurin M, Syst Biol 2004 53 594 622 10.1080/10635150490445706 15371249 (Pubitemid 39290202)
67. Evolution of sexual dimorphism of wing shape in the Drosophila melanogaster subgroup. Gidaszewski NA, Baylac M, Klingenberg CP, BMC Evol Biol 2009 9 110 10.1186/1471-2148-9-110 19457235
68. Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Klingenberg CP, Gidaszewski NA, Syst Biol 2010 59 245 261 10.1093/sysbio/syp106 20525633
69. Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Monteiro LR, Syst Biol 1999 48 192 199 10.1080/106351599260526 12078640 (Pubitemid 129481132)
70. Harvey PH, Pagel MD, The comparative method in evolutionary biology Oxford, UK: Oxford Univ Press 1991
71. Phylogenies and the comparative method. Felsenstein JJ, Am Nat 1985 125 1 15 10.1086/284325 (Pubitemid 16276188)
72. Evolutionary covariation in geometric morphometric data: analyzing integration, modularity, and allometry in a phylogenetic context. Klingenberg CP, Marugán-Lobón J, Syst Biol 2013 62 591 610 10.1093/sysbio/syt025 23589497
73. The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Drake AG, Klingenberg CP, Proc Biol Sci 2008 275 71 76 10.1098/rspb.2007.1169 17956847 (Pubitemid 350146741)
74. A combined morphometric and phylogenetic analysis of an ecomorphological trend: pelagization in Antarctic fishes (Perciformes: Nototheniidae). Klingenberg CP, Ekau W, Biol J Linn Soc Lond 1996 59 143 177 10.1111/j.1095-8312.1996.tb01459.x
75. Geometric morphometrics and phylogeny. Rohlf FJ, Morphology, shape, and phylogeny London: Taylor and Francis, MacLeod N, Forey PL, 2002 175 193
76. Shape at the cross-roads: homoplasy and history in the evolution of the carnivoran skull towards herbivory. Figueirido B, Serrano-Alarcón FJ, Slater GJ, Palmqvist P, J Evol Biol 2010 23 2579 2594 10.1111/j.1420-9101.2010. 02117.x 20942824
77. Developmental plasticity, morphological variation and evolvability: a multilevel analysis of morphometric integration in the shape of compound leaves. Klingenberg CP, Dutke S, Whelan S, Kim M, J Evol Biol 2012 25 115 129 10.1111/j.1420-9101.2011.02410.x 22070353
78. Convergence and divergence in the evolution of cat skulls: temporal and spatial patterns of morphological diversity. Sakamoto M, Ruta M, PLoS One 2012 7 39752 10.1371/journal.pone.0039752 22792186
79. Skull shape evolution in durophagous carnivorans. Figueirido B, Tseng ZJ, Martín-Serra A, Evolution 2013 67 1975 1993 10.1111/evo.12059 23815654
80. Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Mitteroecker P, Bookstein F, Evol Biol 2011 38 100 114 10.1007/s11692-011-9109-8
81. Data from: a three-dimensional analysis of the morphological evolution and locomotor behaviour of the carnivoran hind limb. Martín-Serra A, Figueirido B, Palmqvist P, BMC Evol Biol 2014 doi: 10.5061/dryad.8h6nf