Microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates

Biological Journal of the Linnean Society

Volumn 109, Issue 3, 2013, Pages 644-655

  Quemeneur, Sonia ^a   de Buffrénil, Vivian ^a   Laurin, Michel ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Bone compactness; Habitat; Paleobiology; Paleoecology; Permian; Phylogeny; Temnospondyls

Indexed keywords

ANATOMY; BONE; LIMB; PALEOBIOLOGY; PALEOECOLOGY; PERMIAN; PHYLOGENETICS; PHYLOGENY; TAXONOMY; VERTEBRATE;

AMNIOTA; AVES; LEPIDOSAURIA; MAMMALIA; TESTUDINES; VERTEBRATA;

EID: 84879253714     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/bij.12066     Document Type: Article

References (98)

1. Abramoff MD, Magalhaes PJ, Ram SJ. 2004. Image processing with ImageJ. Biophotonics International 11: 36-42.
2. Ast JC. 2001. Mitochondrial DNA evidence and evolution in Varanoidea (Squamata). Cladistics 17: 211-226.
3. Baker AJ, Pereira SL. 2009a. Ratites and tinamous (Paleognathae. In: Hedges SB, Kumar S, eds. The timetree of life. New York, NY: Oxford University Press, 412-414.
4. Baker AJ, Pereira SL. 2009b. Shorebirds (Charadriiformes. In: Hedges SB, Kumar S, eds. The timetree of life. New York, NY: Oxford University Press, 432-435.
5. Bellairs Ad'A. 1971. Les Reptiles (French edition). Paris: Bordas.
6. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery: a pratical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57: 289-300.
7. Berman DS. 1993. Lower Permian vertebrate localities of New Mexico and their assemblages. New Mexico Museum of Natural History & Science Bulletin 2: 11-21.
8. Biber J-P, Dollinger P, eds. 1995. CITES identification manual, Vol. 3. Reptilia. Geneva: Secretariat of the Convention on International Trade in Endangered Species of Wild Fauna and Flora.
9. Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Greyner R, Price SA, Vos RA, Gittleman JL, Purvis A. 2007. The delayed rise of present-day mammals. Nature 446: 507-512.
10. de Buffrénil V, Canoville A, D'Anastasio R, Doming DP. 2010. Evolution of sirenian pachyosteosclerosis, a model-case for the study of bone structure in aquatic tetrapods. Journal of Mammalian Evolution 17: 101-120.
11. de Buffrénil V, Castanet J. 2000. Age estimation by skeletochronology in the Nile monitor (Varanus niloticus), a highly exploited species. Journal of Herpetology 34: 414-424.
12. de Buffrénil V, Rage J-C. 1993. La 'pachyostose' vertébrale de Simoliophis (Reptilia, Squamata) : données comparatives et considérations fonctionnelles. Annales de Plaéontologie (Vertébrés) 79: 315-335.
13. Canoville A, Laurin M. 2009. Microanatomical diversity of the humerus and lifestyle in lissamphibians. Acta Zoologica 90: 110-122.
14. Canoville A, Laurin M. 2010. Evolution of humeral micronatomy and lifestyle in amniotes, and some comments on palaeobiological inferences. Biological Journal of the Linnean Society 100: 384-406.
15. Carranza S, Arnold EN, Amat F. 2004. DNA phylogeny of Lacerta (Iberolacerta) and other lacertine lizards (Reptilia: Lacertidae): did competition cause long-term montain restriction? Systematics and Biodiversity 2: 57-77.
16. Case EC. 1915. The Permo-Carboniferous red beds of North America and their vertebrate fauna. Publications of the Carnegie Institution of Washington 207: 1-176.
17. Case EC. 1935. Description of a collection of associated skeletons of Trimerorhachis. Contributions from the Museum of Paleontology University of Michigan IV: 227-274.
18. Clack JA, Ahlberg PE, Finney SM, Alonso DP, Robinson JD, Ketcham RA. 2003. A uniquely specialized ear in a very early tetrapod. Nature 425: 65-69.
19. Cope ED. 1877. Descriptions of extinct Vertebrata from the Permian and Triassic formations of the United States. Proceedings of the American Philosophical Society 17: 182-193.
20. Cope ED. 1878. Descriptions of extinct Batrachia and Reptilia from the Permian formation of Texas. Proceedings of the American Philosophical Society 17: 505-530.
21. Cracraft J, Barker F. 2009. Passerine birds (Passeriformes). In: Hedges SB, Kumar S, eds. The timetree of life. New York, NY: Oxford University Press, 423-431.
22. Cubo J, Ponton F, Laurin M, de Margerie E, Castanet J. 2005. Phylogenetic signal in bone microstructure of sauropsids. Systematic Biology 54: 562-574.
23. Del Hoyo J, Elliott A, Christie DA, eds. 2005. Handbook of the birds of the world, Vol. 10. Cuckoo-shrikes to trushes. Barcelona: Lynx Editions.
24. Del Hoyo J, Elliott A, Christie DA, eds. 2006. Handbook of the birds of the world, Vol. 11. Old world flycatchers to old world warblers. Barcelona: Lynx Editions.
25. Del Hoyo J, Elliott A, Christie DA, eds. 2009. Handbook of the birds of the world, Vol. 14. Bush-shrikes to old world sparrows. Barcelona: Lynx Editions.
26. Del Hoyo J, Elliott A, Sargatal J, eds. 1992. Handbook of the birds of the world, Vol. 1. Ostrich to ducks. Barcelona: Lynx Editions.
27. Del Hoyo J, Elliott A, Sargatal J, eds. 1994. Handbook of the birds of the world, Vol. 2. New world vultures to guineafowls. Barcelona: Lynx Editions.
28. Del Hoyo J, Elliott A, Sargatal J, eds. 1996. Handbook of the birds of the world, Vol. 3. Hoatzin to auks. Barcelona: Lynx Editions.
29. Del Hoyo J, Elliott A, Sargatal J, eds. 1999. Handbook of the birds of the world, Vol. 5. Barn owls to hummingbirds. Barcelona: Lynx Editions.
30. Del Hoyo J, Elliott A, Sargatal J, eds. 2001. Handbook of the birds of the world, Vol. 6. Mousebirds to hornbills. Barcelona: Lynx Editions.
31. Del Hoyo J, Elliott A, Sargatal J, eds. 2002. Handbook of the birds of the world, Vol. 7. Jacamars to woodpeckers. Barcelona: Lynx Editions.
32. Dumont ER. 2010. Bone density and the lightweight of skeletons of birds. Proceedings of the Royal Society of London Series B, Biological Sciences 277: 1-6.
33. Dumont M, Laurin M, Jacques F, Pellé E, Dabin W, de Buffrénil V. 2013. Inner architecture of vertebral centra in terrestrial and aquatic mammals: a two-dimensional comparative study. Journal of Morphology doi: 10.1002/jmor.20122
34. Fawcett DW. 1942. The amedullary bones of the Florida manatee (Trichechus latirostris). American Journal of Anatomy 71: 271-309.
35. Fish FE, Stein BR. 1991. Functional correlates of differences in bone density among terrestrial and aquatic genera in the family Mustelidae (Mammalia). Zoomorphology 110: 339-345.
36. Francillon-Vieillot H, de Buffrénil V, Castanet J, Geraudie J, Meunier FJ, Sire J-Y, Zylberberg L, de Ricqlès A. 1990. Microstructures and mineralization of vertebrate skeletal tissues. In: Carter J, ed. Skeletal biomineralizations: patterns, processes and evolutionary trends. New York, NY: Van Nostrand Reinhold, 471-530.
37. Fritz U, Branch WR, Hofmeyr MD, Maran J, Prokop H, Schleicher A, Siroky P, Stuckas H, Vargas-Ramirez M, Vences M, Hundsdorfer AK. 2011. Molecular phylogeny of African hinged and helmeted terrapins (Testudines : Pelomedusidae: Pelusios and Pelomedusa). Zoologica Scipta 40: 115-125.
38. Germain D, Laurin M. 2005. Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zoologica Scripta 34: 335-350.
39. Gimenes Giugliano L, Garcia Collevatti R, Rinaldi Colli G. 2007. Molecular dating and phylogenetic relationships among Teiidae (Squamata) inferred by molecular and morphological data. Molecular Phylogenetics and Evolution 45: 168-179.
40. Girondot M, Laurin M. 2003. Bone Profiler: a tool to quantify, model and statistically compare bone section compactness profiles. Journal of Vertebrate Paleontology 23: 458-461.
41. Grassé PP, ed. 1955. Traité de Zoologie, t. 17 (1-2), Mammifères, les ordres: anatomie, éthologie, systématique. Paris: Masson & Co.
42. Guillon JM, Guéry L, Hulin V, Girondot M. 2012. A large phylogeny of turtles (Testudines) using molecular data. Contributions to Zoology 81: 147-158.
43. Habib MB, Ruff CB. 2008. The effects of locomotion on the structural characteristics of avian long bones. Zoological Journal of the Linnean Society 153: 601-624.
44. Harshman J, Braun EL, Braun MJ, Huddleston CJ, Bowie RCK, Chojnowski JL, Hackett SJ, Han K, Kimball RT, Marks BD, Miglia KJ, Moore WS, Reddy S, Sheldon FH, Steadman DW, Steppan SJ, Witt CC, Yuri T. 2008. Phylogenomic evidence for multiple losses of flight in ratite birds. PNAS 105: 13462-13467.
45. Hassanin A, Douzery EJP. 1999. The tribal radiation of the family Bovidae (Artiodactyla) and the evolution of the mitochondrial cytochrome b gene. Molecular Phylogenetics and Evolution 13: 227-243.
46. Hedges SB, Vidal N. 2009. Lizards, snakes and amphisbaenians (Squamata). In: Hedges SB, Kumar S, eds. The timetree of life. New York, NY: Oxford University Press, 383-389.
47. Houssaye A. 2009. 'Pachyostosis' in aquatic amniotes: a review. Integrative Zoology 4: 325-340.
48. Houssaye A. 2013. Palaeoecological and morphofunctional interpretation of bone mass increase: an example in Late Cretaceous shallow marine squamates. Biological Reviews of the Cambridge Philosophical Society 88: 117-139.
49. Kriloff A, Germain D, Canoville A, Vincent P, Sache M, Laurin M. 2008. Evolution of bone microanatomy of the tetrapod tibia and its use in paleobiological inference. Journal of Evolutionary Biology 21: 1-11.
50. Laurin M. 2004. The evolution of body size, Cope's rule and the origin of amniotes. Systematic Biology 53: 594-622.
51. Laurin M, Canoville A, Germain D. 2011. Bone microanatomy and lifestyle: a descriptive approach. Comptes rendus Palevol 10: 381-402.
52. Laurin M, Canoville A, Quilhac A. 2009. Use of paleontological and molecular data in supertrees for comparative studies: the example of lissamphibian femoral microanatomy. Journal of Anatomy 215: 110-123.
53. Laurin M, Girondot M, Loth M-M. 2004. The evolution of long bone microanatomy and lifestyle in lissamphibians. Paleobiology 30: 589-613.
54. Legendre L, Le Roy N, Martinez-Maza C, Montes L, Laurin M, Cubo J. 2013. Phylogenetic signal in bone histology of amniotes revisited. Zoologica Scripta 42: 44-53.
55. Mac Arthur RH. 1957. On the relative abundance of bird species. Proceedings of the National Academy of Sciences of the United States of America 43: 293-295.
56. Macdonald D, ed. 2001. The new encyclopedia of Mammals. Oxford: Oxford University Press.
57. Madar SI. 2007. The postcranial skeleton of early Eocene pakicetid cetaceans. Journal of Paleontology 8: 176-200.
58. Maddison WP. 2000. Testing character correlation using pairwise comparisons on a phylogeny. Journal of Theoretical Biology 202: 195-204.
59. Maddison WP, Maddison DR. 2011. Mesquite: a molecular system for evolutionary analysis, Version 2.75. Available at: http://mesquiteproject.org
60. de Margerie E, Robin J-P, Verrier D, Cubo J, Groscolas R, Castanet J. 2004. Assessing a relationship between bone microstructure and growth rate: a fluorescent labeling study in the king penguin chick (Aptenodytes patagonicus). Journal of Experimental Biology 207: 869-879.
61. Meredith RW, Janecka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simao TLL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrik A, Westerman M, Ayoub NA, Springer MS, Murphy WJ. 2011. Impacts of the Cretaceous terrestrial revolution and Kpg exinction on mammal diversification. Science 334: 521-524.
62. Nasterlack T, Canoville A, Chinsamy A. 2012. New insights into the biology of the Permian genus Cistecephalus (Therapsida, Dicynodonta). Journal of Vertebrate Paleontology 32: 1396-1410.
63. Okajima Y, Kumazawa Y. 2010. Mitochondrial genomes of acrodont lizards: timing of gene rearrangements and phylogenetic and biogeographic implications. BMC Evolutionary Biology 10: 141.
64. Pawley K. 2007. The postcranial skeleton of Trimerorhachis insignis Cope, 1878 (Temnospondyli: Trimerorhachidae): a plesiomorphic temnospondyl from the Lower Permian of North America. Journal of Paleontology 81: 873-894.
65. Pawley K, Warren A. 2006. The appendicular skeleton of Eryops megacephalus Cope, 1877 (Temnospondyli: Eryopidae) from the Lower Permian of North America. Journal of Paleontology 80: 561-580.
66. Pereira SL, Baker AJ. 2009. Waterfowl and gamefowl (Galloanserae). In: Hedges SB, Kumar S, eds. The timetree of life. New York, NY: Oxford University Press, 415-418.
67. Perrin WF, Würsig B, Thewissen JGM, eds. 2009. Encyclopedia of Marine Mammals, 2nd edn. Amsterdam: Academic Press.
68. Pianka E, King D, eds. 2004. Varanoid lizards of the world. Bloomington, IN: Indiana University Press.
69. Pianka E, Vitt L. 2003. Lizards - window to the evolution of diversity. Berkeley and Los Angeles, CA: University of California press.
70. Polley B, Reisz RR. 2011. A new Lower Permian trematopid (Temnospondyli: Dissorophoidea) from Richards Spur, Oklahoma. Zoological Journal of the Linnean Society 161: 789-815.
71. Quémeneur S, de Buffrénil V, Laurin M. 2013. Data from: microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates. Dryad Digital Repository doi:10.5061/dryad.qd734.
72. Read AF, Nee S. 1995. Inference from binary comparative data. Journal of Theoretical Biology 173: 99-108.
73. de Ricqlès A. 1976. On bone histology of fossil and living reptiles, with comments on its functional and evolutionary significance. In: Bellairs Ad'A, Cox CB, eds. Morphology and biology of reptiles. Linnean Society Symposium, series 3. London: Academic Press, 123-150.
74. de Ricqlès A, de Buffrénil V. 2001. Bone histology, heterochronies and the return of Tetrapods to life in water: w[h]ere are we? In: Mazin J-M, de Buffrénil V, eds. Secondary adaptation of tetrapods to life in water. München: Verlag Dr. FriedrichPfeil, 289-310.
75. de Ricqlès A, Padian K, Horner JR, Francillon-Vieillot H. 2000. Palaeohistology of the bones of pterosaurs (Reptilia: Archosauria) : anatomy, ontogeny and biomechanical implications. Zoological Journal of the Linnean Society 129: 349-385.
76. de Ricqlès A, Padian K, Knoll F, Horner JR. 2008. On the origin of high growth rates in archosaurs and their ancient relatives: complementary histological studies on Triassic archosauriforms and the problem of a 'phylogenetic signal' in bone histology. Annales de Paléontologie 94: 57-76.
77. Ruta M, Coates MI. 2007. Dates, nodes and character conflict: addressing the lissamphibian origin problem. Journal of Systematic Palaeontology 5: 69-122.
78. Sanchez S, Germain D, de Ricqlès A, Abourachid A, Goussard F, Tafforeau P. 2010. Limb-bone histology of temnospondyls: implications for understanding the diversification of palaeoecologies and patterns of locomotion of Permo-Triassic tetrapods. Journal of Evolutionary Biology 23: 2076-2090.
79. Sander M. 1989. Early Permian depositional environments and pound bonebeds in central Archer County, Texas. Paleogeography, Paleoclimatology, Paleoecology 69: 1-21.
80. Scheyer TM, Sander PM. 2007. Shell bone histology indicates terrestrial palaeoecology of basal turtles. Proceedings of the Royal Society of London Series B, Biological Sciences 274: 1885-1893.
81. Schultze H. 1999. The fossil record of the intertidal zone. In: Horn MH, Martin KLM, Chotkowski MH, eds. Intertidal fishes: life in two worlds. London: Academic Press, 373-392.
82. Shaffer HB. 2009. Turtles (Testudines). In: Hedges SB, Kumar S, eds. The Timetree of life. New York, NY: Oxford University Press, 398-401.
83. Shedlock AM, Edwards SV. 2009. Amniotes (Amniota). In: Hedges SB, Kumar S, eds. The timetree of life. New York, NY: Oxford University Press, 398-401.
84. Stein BR. 1989. Bone density and adaptation in semiaquatic mammals. Journal of Mammology 70: 467-476.
85. Stuart-Fox D, Owens IPF. 2003. Species richness in agamid lizards: chance, body size, sexual selection or ecology? Journal of Evolutionary Biology 16: 659-669.
86. Taylor M. 2000. Functional significance of bone ballast in the evolution of buoyancy control strategies by aquatic tetrapods. Historical Biology 14: 15-31.
87. Townsend TM, Larson A, Louis E, Macey JR. 2004. Molecular phylogenetics of Squamata: the position of snakes, amphisbaenians, and dibamids, and the root of the squamate tree. Systematic Biology 53: 735-757.
88. Vallin G, Laurin M. 2004. Cranial morphology and affinities of Microbrachis, and a reappraisal of the phylogeny and lifestyle of the first amphibians. Journal of Vertebrate Paleontology 24: 56-72.
89. Van Tuinen M. 2009a. Birds (Aves). In: Hedges SB, Kumar S, eds. The timetree of life. New York, NY: Oxford University Press, 409-411.
90. Van Tuinen M. 2009b. Advanced birds (Neoaves). In: Hedges SB, Kumar S, eds. The timetree of life. New York, NY: Oxford University Press, 419-422.
91. Vidal N, Hedges SB. 2005. The phylogeny of squamate reptiles (lizards, snakes and amphisbaenians) inferred by nine nuclear protein-coding genes. Comptes-rendus Biologies 328: 1000-1008.
92. Vidal N, Marin J, Sassi J, Battistuzzi FU, Donnellan S, Fitch AJ, Fry BG, Vonk FJ, Vega RCR, Couloux A, Hedges SB. 2012. Molecular evidence for an Asian origin of monitor lizards followed by Tertiary dispersals to Africa and Australasia. Biology Letters 8: 853-855.
93. Wall WP. 1983. The correlation between high limb-bone density and aquatic habits in recent mammals. Journal of Paleontology 57: 197-207.
94. Werneburg R, Lucas SG, Schneider JW, Rinehart LF. 2010. First Pennsylvanian Eryops (Temnospondyli) and its Permian record from New Mexico. New Mexico Museum of Natural History & Science Bulletin 49: 129-136.
95. Wiens JJ, Hollingsworth BD. 2000. War of Iguanas: conflicting molecular and morphological phylogenies and long-branch attraction in Iguanid lizards. Systematic Biology 49: 143-159.
96. Wiens JJ, Kuczynski CA, Arif S, Reeder TW. 2010. Phylogenic relationship of phrynosomatid lizards based on nuclear and mitochondrial data, and a revised phylogeny for Sceloporus. Molecular Phylogenetics and Evolution 54: 150-161.
97. Wiffen J, de Buffrénil V, de Ricqlès A, Mazin J-M. 1995. Ontogenetic evolution of bone structure in Late Cretaceous Plesiosauria from New Zealand. Géobios 28: 625-640.
98. Yu L, Peng D, Liu J, Luan P, Liang L, Lee H, Lee M, Ryder OA, Zhang Y. 2011. On the phylogeny of Mustelidae subfamilies: analysis of the seventeen nuclear non-coding loci and mitochondrial complete genomes. BMC Evolutionary Biology 11: 92.