Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences

Biological Journal of the Linnean Society

Volumn 100, Issue 2, 2010, Pages 384-406

  Canoville, Aurore ^a   Laurin, Michel ^a  

^a CNRS   (France)

Author keywords

Bone microanatomy; Comparative biology; Habitat; Hypothetical ancestors; Inference models; Palaeobiology; Phylogeny

Indexed keywords

ANATOMY; BONE; DISCRIMINANT ANALYSIS; LIFESTYLE; PALEOBIOLOGY; PHYLOGENY; TAXONOMY; VERTEBRATE;

AMNIOTA; LYSTROSAURUS; MESOSAURUS;

EID: 77954105493     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2010.01431.x     Document Type: Article

References (103)

1. Bartlett MS. The use of transformations. Biometrics 1947, 3:39-52.
2. Battail B. Les genres Dicynodon et Lystrosaurus (Therapsida, Dicynodontia) en Eurasie: une mise au point. GeoBios 1997, 20:39-48.
3. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B (Methodological) 1995, 57:289-300.
4. Benton MJ. Vertebrate Palaeontology 2005, Oxford, Blackwell Publishing
5. Bininda-Emonds ORP. The evolution of supertrees. Trends in Ecology and Evolution 2004, 19:315-322.
6. Bininda-Emonds ORP, Gittleman JL, Kelly CK. Flippers versus feet: comparative trends in aquatic and non-aquatic carnivores. Journal of Animal Ecology 2001, 70:386-400.
7. Bininda-Emonds ORP, Jones KE, Price SA, Grenyer R, Cardillo M, Habib M, Purvis A, Gittleman J. Supertrees are a necessary not-so-evil: a comment on Gatesy et al. Systematic Biology 2003, 52:724-729.
8. Box GEP, Cox DR. An analysis of transformations. Journal of the Royal Statistical Society, Series B 1964, 26:211-252.
9. Boy JA, Sues HD. Branchiosaurs: larvae, metamorphosis and heterochrony in temnospondyls and seymouriamorphs. Amphibian Biology 2000, 1150-1197. Heatwole H, Carroll RL. eds., Chipping Norton, Surrey Beatty & Sons
10. Broom R. On the structure of the shoulder girdle in. Lystrosaurus. Annals of South African Museum 1903, 4:139-141.
11. Canoville A, Laurin M. Microanatomical diversity of the humerus and lifestyle in lissamphibians. Acta Zoologica 2009, 90:110-122.
12. Carroll RL. The earliest reptiles. Zoological Journal of the Linnean Society 1964, 45:61-83.
13. Carroll RL. Origin of reptiles. Morphology A 1969, 1-44. Gans CBellairs AAParsons TS. eds., London, Academic Press
14. Carroll RL. Plesiosaur ancestors from the Upper Permian of Madagascar. Philosophical Transactions of the Royal Society of London, Series B 1981, 293:315-383.
15. Carroll RL. Early evolution of reptiles. Annual Review of Ecology and Systematics 1982, 13:87-109.
16. Carroll RL. Evolutionary constraints in aquatic diapsid reptiles. Palaeontology 1985, 33:145-155.
17. Carroll RL. Vertebrate Paleontology and Evolution 1988, New York, NY, WH Freeman and Company
18. Carroll RL, Gaskill P. The nothosaur Pachypleurosaurus and the origin of plesiosaurs. Philosophical Transactions of the Royal Society of London, Series B 1985, 309:343-393.
19. Casgrain P. Permute! Montreal. 2005, http://www.bio.umontreal.ca/Casgrain/en/labo/permute/index.html, Available from:
20. Castanet J, Cubo J, de Margerie E. Signification de l'histodiversité osseuse: le message de l'os. Biosystema 2001, 19:133-147.
21. Castanet J, Francillon-Vieillot H, Meunier FJ, de Ricqlès A. Bone and individual aging. Bone 1993, 245-283. Hall BK, ed., London, CRC Press
22. Chiappe LM, Chinsamy A. Pterodaustro's true teeth. Nature 1996, 379:211-212.
23. Cluver MA. The cranial morphology of the dicynodont genus Lystrosaurus. Annals of the South African Museum 1971, 56:155-274.
24. Cubo J, de Margerie E, Castanet J. Homoplastic variation of bone vascularization in birds. Journal of Vertebrate Paleontology 2001, 21:43A.
25. Cubo J, Legendre P, de Ricqlès A, Montes L, de Margerie E, Castanet J, Desdevises Y. Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes. Evolution & Development 2008, 10:213-223.
26. Cubo J, Ponton F, Laurin M, de Margerie E, Castanet J. Phylogenetic signal in bone microstructure of sauropsids. Systematic Biology 2005, 54:562-574.
27. Curran-Everett D. Multiple comparisons: philosophies and illustrations. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 2000, 279:1-8.
28. de Buffrénil V, Francillon-Vieillot H. Ontogenic changes in bone compactness in male and female Nile monitors (Varanus niloticus). Journal of Zoology 2001, 253:539-546.
29. de Buffrénil V, Mazin JM. Bone histology of Claudiosaurus germaini (Reptilia, Claudiosauridae) and the problem of pachyostosis in aquatic tetrapods. Historical Biology 1989, 2:311-322.
30. de Buffrénil V, Mazin JM. Contribution de l'histologie osseuse à l'interprétation paléobiologique du genre Placodus Agassiz, 1833 (Reptilia, Placodontia). Revue de Paléobiologie 1992, 11:397-407.
31. de Buffrénil V, Schoevaert D. Données quantitatives et observations histologiques sur la pachyostose du squelette du dugong, Dugong dugon (Müller) (Sirenia, Dugongidae). Canadian Journal of Zoology 1989, 67:2107-2119.
32. de Buffrénil V, Sire JY, Schoevaert D. Comparaison de la structure et du volume squelettiques entre un delphinidé (Delphinus delphis L.) et un mammifère terrestre (Panthera leo L.). Canadian Journal of Zoology 1986, 64:1750-1756.
33. de Lapparent de Broin F, Bocquentin J, Negri FR. Gigantic turtles (Pleurodira, Podocnemididae) from the Late Miocene-Early Pliocene of South Western Amazon. Bulletin de l'Institut Français d'Etudes Andines 1993, 22:657-670.
34. de Margerie E, Sanchez S, Cubo J, Castanet J. Torsional resistance as a principal component of the structural design of long bones: comparative multivariate evidence in birds. Anatomical Record, Part A 2005, 282A:49-66.
35. de Ricqlès A. Recherches paléohistologiques sur les os longs des tétrapodes IV. - Eothériodontes et pélycosaures. Annales de Paléontologie 1974, 60:1-39.
36. de Ricqlès A. Croissance périodique, ontogenèse, phylogenèse et stratégies démographiques: le cas des reptiles captorhinomorphes. Bulletin de la Société Zoologique de France 1980, 105:363-369.
37. de Ricqlès A. Cyclical growth in the long limb bones of a sauropod dinosaur. Acta Palaeontologica Polonica 1983, 28:225-232.
38. de Ricqlès A, de Buffrénil V. Bone histology, heterochronies and the return of tetrapods to life in water: where are we? Secondary Adaptation of Tetrapods to Life in Water 2001, 289-310. Mazin JM, de Buffrénil V. eds., Munich, Dr Friedrich Pfeil
39. Desdevises Y, Legendre P, Azouzi L, Morand S. Quantifying phylogenetically structured environmental variation. Evolution 2003, 57:2467-2652.
40. Domning DP. The earliest known fully quadrupedal sirenian. Nature 2001, 413:625-627.
41. Fawcett DW. The amedullary bones of the Florida manatee (Trichechus latirostris). American Journal of Anatomy 1942, 71:271-309.
42. Felsenstein J. Phylogenies and the comparative method. American Naturalist 1985, 125:1-15.
43. Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, de Sá RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto B, Moler P, Drewes RC, Nussbaum RA, Lynch JD, Green DM, Wheeler WC. The amphibian tree of life. Bulletin of the American Museum of Natural History 2006, 297:1-370.
44. Garland T, Midford PE, Ives AR. An introduction to phylogenetically based methods, with a new method for confidence intervales on ancestral values. American Zoologist 1999, 39:374-388.
45. Germain D, Laurin M. Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zoologica Scripta 2005, 34:335-350.
46. Girondot M, Laurin M. Bone Profiler: a tool to quantify, model and statistically compare bone section compactness profiles. Journal of Vertebrate Paleontology 2003, 23:458-461.
47. Gray NM, Kainec K, Madar S, Tomko L, Wolfe S. Sink or Swim? Bone density as a mechanism for buoyancy control in early cetaceans. Anatomical Record 2007, 290:638-653.
48. Holmes R, Cheng YN, Wu XC. New information on the skull of Keichousaurus hui (Reptilia: Sauropterygia) with comments on sauropterygian interrelationships. Journal of Vertebrate Paleontology 2008, 28:76-84.
49. Hoyle MH. Transformations: an introduction and a bibliography. International Statistical Review 1973, 41:203-223.
50. 2008 IUCN Red List of Threatened Species. 2008, http://www.iucnredlist.org, IUCN, Available at:
51. Josse S, Moreau T, Laurin M. Stratigraphic tools for Mesquite. 2006, http://mesquiteproject.org/packages/stratigraphicTools/, Available from
52. Joyce WG, Gauthier JA. Palaeoecology of Triassic stem turtles sheds new light on turtle origins. Proceedings of the Royal Society of London, Series B, Biological Sciences 2004, 271:1-5.
53. King GM. The aquatic Lystrosaurus: a palaeontological myth. Historical Biology. An International Journal of Paleobiology 1991, 4:285-321.
54. King GM, Cluver MA. The aquatic Lystrosaurus: an alternative lifestyle. Historical Biology. An International Journal of Paleobiology 1991, 4:323-341.
55. King GM, Jenkins I. The dicynodont Lystrosaurus from the Upper Permian of Zambia: evolutionary and stratigraphical implications. Palaeontology 1997, 40:149-156.
56. Kissel RA, Dilkes DW, Reisz RR. Captorhinus magnus, a new captorhinid (Amniota: Eureptilia) from the Lower Permian of Oklahoma, with new evidence on the homology of the astragalus. Canadian Journal of Earth Sciences 2002, 39:1363-1372.
57. Kriloff A, Germain D, Canoville A, Vincent P, Sache M, Laurin M. Evolution of bone microanatomy of the tetrapod tibia and its use in paleobiological inference. Journal of Evolutionary Biology 2008, 21:1-11.
58. Laurin M. Seymouriamorphs. Amphibian Biology 2000, 1064-1080. Heatwole HCarroll RL. eds., Chipping Norton, Surrey Beatty & Sons
59. Laurin M. The evolution of body size, Cope's rule and the origin of amniotes. Systematic Biology 2004, 53:594-622.
60. Laurin M. Systématique, paléontologie et biologie évolutive moderne: l'exemple de la sortie des eaux des vertébrés 2008, Paris, Ellipses
61. Laurin M, Canoville A, Quilhac A. Use of paleontological and molecular data in supertrees for comparative studies: the example of lissamphibian femoral microanatomy. Journal of Anatomy 2009, 215:110-123.
62. Laurin M, Germain D, Steyer JS, Girondot M. Données microanatomiques sur la conquête de l'environnement terrestre par les vertébrés. Comptes Rendus Palevol 2006, 5:603-618.
63. Laurin M, Girondot M, Loth MM. The evolution of long bone microanatomy and lifestyle in lissamphibians. Paleobiology 2004, 30:589-613.
64. Laurin M, Meunier FJ, Germain D, Lemoine M. A microanatomical and histological study of the paired fin skeleton of the Devonian sarcopterygian Eusthenopteron foordi. Journal of Paleontology 2007, 81:143-153.
65. Laurin M, Reisz R. A reevaluation of early amniote phylogeny. Zoological Journal of the Linnean Society 1995, 113:165-223.
66. Lee MSY. Historical burden in systematics and the interrelationships of 'parareptiles'. Biological Reviews of the Cambridge Philosophical Society 1995, 70:459-547.
67. Lee MSY. Pareiasaur phylogeny and the origin of turtles. Zoological Journal of the Linnean Society 1997, 120:197-280.
68. Lee MSY. Molecules, morphology, and the monophyly of diapsid reptiles. Contributions to Zoology 2001, 70:1-18.
69. Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis, Version 2.5. 2008, http://mesquiteproject.org, Available at:
70. Meers MB. Cross-sectional geometric properties of the crocodylian humerus: an exception to Wolff's law? Journal of Zoology 2002, 258:405-418.
71. Midford P, Garland TJ, Maddison WP. PDAP package for Mesquite, Version 1.12. 2008, http://mesquiteproject.org/pdap_mesquite/index.html, Available at
72. Modesto SP. New information on the skull of the Early Permian reptile Captorhinus aguti. PaleoBios 1998, 18:21-35.
73. Modesto SP. The cranial skeleton of the Early Permian aquatic reptile Mesosaurus tenuidens: implications for relationships and palaeobiology. Zoological Journal of the Linnean Society 2006, 146:345-368.
74. Müller J. Early loss and multiple return of the lower temporal arcade in diapsid reptiles. Naturwissenschaften 2003, 90:473-476.
75. Myers P, Espinosa R, Parr CS, Jones T, Hammond GS, Dewey TA. The animal diversity web (online). 2006, http://animaldiversity.org, Available at:
76. Nopcsa FB. Vorläufige Notiz über die Pachyostose und Osteosklerose einiger mariner Wirbeltiere. Anatomischer Anzeiger 1923, 56:353-359.
77. Oelofsen B, Araújo DC. Palaeoecological implications of the distribution of mesosaurid reptiles in the Permian Irati Sea (Paraná Basin), South America. Revista and Brasileira de Geociências 1983, 13:1-6.
78. Olson EC. Fauna of the Vale and Choza: 9-Captorhinomorpha. Fieldiana Geology 1954, 10:211-218.
79. Padian K, de Ricqlès A, Horner JR. Dinosaurian growth rates and bird origins. Nature 2001, 412:405-408.
80. Peabody FE. The origin of the astragalus of reptiles. Evolution 1951, 5:339-344.
81. Peyer B. Geschichte der Tierwelt 1950, Zürich, Büchergilde Gutenberg
82. Piñeiro G. Los mesosaurios y otros fosiles de fines del Paleozoico. Fosiles de Uruguay 2008, 179-205. Perera D. ed., Montevideo, DIRAC
83. Ray S. Functional and evolutionary aspects of the postcranial anatomy of dicynodonts (Synapsida, Therapsida). Palaeontology 2006, 49:1263-1286.
84. Ray S, Chinsamy A, Bandyopadhyay S. Lystrosaurus murrayi (Therapsida, Dicynodontia): bone histology, growth and lifestyle adaptations. Palaeontology 2005, 48:1169-1185.
85. Reisz RR, Laurin M. Owenetta and the origin of turtles. Nature 1991, 349:324-326.
86. Retallack GJ, Smith RMH, Ward PD. Vertebrate extinction across the Permian-Triassic boundary in Karoo Basin, South Africa. GSA Bulletin 2003, 115:1133-1152.
87. Rieppel O. A new pachypleurosaur (Reptilia: Sauropterygia) from the Middle Triassic of Monte San Giorgio, Switzerland. Philosophical Transactions of the Royal Society of London, Series B 1989, 323:1-73.
88. Rieppel O. The genus Placodus: systematics, morphology, paleobiogeography and paleobiology. Fieldiana (Geology), N.S. 1995, 31:1-85.
89. Romer AS. Origin of the amniote egg. Scientific Monthly 1957, 85:57-63.
90. Romer AS. Tetrapods limbs and early tetrapod life. Evolution 1958, 12:365-369.
91. Sander PM. The pachypleurosaurids (Reptilia: Nothosauria) from the Middle Triassic of Monte San Giorgio (Switzerland) with the description of a new species. Philosophical Transactions of the Royal Society of London, Series B 1989, 325:561-670.
92. Scheyer TM, Sánchez-Villagra MR. Carapace bone histology in the giant pleurodiran turtle Stupendemys geographicus: Phylogeny and function. Acta Palaeontologica Polonica 2007, 52:137-154.
93. Scheyer TM, Sander PM. Shell bone histology indicates terrestrial palaeoecology of basal turtles. Proceedings of the Royal Society of London, Series B, Biological Sciences 2007, 274:1885-1893.
94. Scheyer TM, Sander PM. Bone microstructures and mode of skeletogenesis in osteoderms of three pareiasaur taxa from the Permian of South Africa. Journal of Evolutionary Biology 2009, 22:1153-1162.
95. Schmidt S. Paleoecology of nothosaurs. Third Symposium on Mesozoic Ecosystems, short papers 1984, 215-218. Reif WF. ed., Tübingen, Attempto Verlag
96. Shedlock AM, Edwards SV. Amniotes (Amniota). The timetree of life 2009, 375-379. Hedges SB, Kumar S. eds., Oxford, Oxford University Press
97. STATISTICA, Version 6. 2003, http://www.statsoft.com, StatSoft France,
98. Steyer JS, Laurin M, Castanet J, de Ricqlès A. First histological and skeletochronological data on temnospondyl growth; palaeoecological and palaeoclimatological implications. Palaeogeography, Palaeoclimatology, Palaeoecology 2004, 206:193-201.
99. Storrs GW. Function and phylogeny in sauropterygian (Diapsida) evolution. American Journal of Science 1993, 293A:63-90.
100. Sues HD. On the skull of Placodus gigas and the relationships of the Placodontia. Journal of Vertebrate Paleontology 1987, 7:138-144.
101. Sullivan C, Reisz RR. First record of Seymouria (Vertebrata: Seymouriamorpha) from Early Permian fissure fills at Richards Spur, Oklahoma. Canadian Journal of Earth Sciences 1999, 36:1257-1266.
102. Vallin G, Laurin M. Cranial morphology and affinities of Microbrachis, and a reappraisal of the phylogeny and lifestyle of the first amphibians. Journal of Vertebrate Paleontology 2004, 24:56-72.
103. Werneburg I, Sánchez-Villagra MR. Timing of organogenesis support basal position of turtles in the amniote tree of life. BMC Evolutionary Biology 2009, 9:1-9.