Evolution of bone compactness in extant and extinct moles (Talpidae): Exploring humeral microstructure in small fossorial mammals

BMC Evolutionary Biology

Volumn 13, Issue 1, 2013, Pages

  Meier, Patricia S ^a   Bickelmann, Constanze ^a,b   Scheyer, Torsten M ^a   Koyabu, Daisuke ^a   Sánchez Villagra, Marcelo R ^a  

^a PALÄONTOLOGISCHES INSTITUT UND MUSEUM   (Switzerland)

^b LEIBNIZ INSTITUTE FOR EVOLUTION AND BIODIVERSITY SCIENCE   (Germany)

Author keywords

Paleohistology; Phylogeny; Placentalia; Size; Wolffs law

Indexed keywords

ANATOMY; BIOMECHANICS; BONE; CLADISTICS; EXTINCTION; HISTOLOGY; MICROSTRUCTURE; MORPHOLOGY; PHYLOGENY; SMALL MAMMAL; SPECIALIZATION; TAXONOMY;

EUTHERIA; INSECTIVORA; MAMMALIA; TALPIDAE; TALPINI;

ANIMAL; ARTICLE; CLASSIFICATION; ECOSYSTEM; EVOLUTION; FOSSIL; GENETICS; HISTOLOGY; HUMERUS; MOLE (INSECTIVORA); PHYLOGENY; SPECIES EXTINCTION;

ANIMALS; BIOLOGICAL EVOLUTION; ECOSYSTEM; EXTINCTION, BIOLOGICAL; FOSSILS; HUMERUS; MOLES; PHYLOGENY;

MLCS; MLOWN;

EID: 84874212146     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-13-55     Document Type: Article

References (49)

1. Gorman ML, Stone DR, The natural history of moles New York: Cornell University Press 1990 138
2. Mc Kenna MC, Bell SK, Classification of mammals above the species level New York: Columbia University Press 1997
3. A comprehensive morphological analysis of talpid moles (Mammalia) phylogenetic relationships. Sánchez-Villagra MR, Horovitz I, Motokawa M, Cladistics 2006 22 59 88 10.1111/j.1096-0031.2006.00087.x
4. Molecular phylogenetic relationships of moles, shrew moles, and desmans from the New and Old worlds. Shinohara A, Campbell KL, Suzuki H, Mol Phylogenet Evol 2003 27 247 258 10.1016/S1055-7903(02)00416-5 12695089
5. Evolution and biogeography of talpid moles from continental East Asia and the Japanese Islands inferred from mitochondrial and nuclear gene sequences. Shinohara A, Suzuki H, Tsuchiya K, Zhang Y-P, Luo J, Jiang X-L, Wang Y-X, Campbell KL, Zoolog Sci 2004 21 1177 1185 10.2108/zsj.21.1177 15613798
6. The holes of moles: Osteological correlates of the trigeminal nerve in Talpidae. Crumpton N, Thompson R, J Mamm Evol 2012 10.1007/s10914-012-9213-2
7. Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals. Koyabu D, Endo H, Mitgutsch C, Suwa G, Catania KC, Zollikofer CP, Oda S-I, Koyasu K, Ando M, Sánchez-Villagra MR, EvoDevo 2011 2 21 10.1186/2041-9139-2-21 22040374
8. Testing convergent and parallel adaptations in talpids humeral mechanical performance by means of Geometric Morphometrics and Finite Element Analysis. Piras P, Sansalone G, Teresi L, Kotsakis T, Colangelo P, Loy A, J Morphol 2012 273 696 711 10.1002/jmor.20015 22419178
9. Patterns of evolutionary transformation in the humerus of moles (Talpidae, Mammalia): a character analysis. Sánchez-Villagra MR, Menke PR, Geisler JH, Nat Hist 2004 170 163 170
10. Comparative myology of moles and the phylogeny of the Talpidae (Mammalia, Lipotyphla). Whidden HP, Am Mus Novit 2000 3294 1 53
11. The anatomy of the shoulder and upper arm of the mole (Talpa europaea). Freeman R, Journal of Anatomy and Physiology 1886 20 201 219
12. Locomotion and appendicular anatomy in three soricoid insectivores. Reed CA, Am Midl Nat 1951 45 513 671 10.2307/2421996
13. The anatomy of mole locomotion. Yalden DW, J Zool 1966 149 55 64
14. Cinefluorographical study of the burrowing movements in the common mole, Talpa europaea (Lipotyphla, Talpidae). Gambaryan PP, Gasc J-P, Renous S, Russian J Theriol 2002 1 91 109
15. Functional interpretations of the radiographic anatomy of the femora of Myotis lucifugus, Pipistrellus subflavus, and Blarina brevicauda. Dawson DL, Am J Anat 1980 157 1 15 10.1002/aja.1001570102 7405858
16. Bone density and adaptation in semiaquatic mammals. Stein BR, J Mammal 1989 70 467 476 10.2307/1381418
17. Microstructure and mineralization of vertebrate skeletal tissues. Francillon-Vieillot H, De Buffrénil V, Castanet J, Géraudie J, Meunier FJ, Sire J-Y, Zylberberg L, De Ricqlès AJ, Skeletal biomineralization: Patterns, processes and evolutionary trends New York: Reinhold, Van Nostrand, Carter JG, 1990 471 530
18. Bone Profiler: A tool to quantify, model and statistically compare bone-section compactness profiles. Girondot M, Laurin M, Bone 2003 23 458 461
19. Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Germain D, Laurin M, Zoologica Scripta 2005 34 335 350 10.1111/j.1463-6409.2005.00198.x
20. Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences. Canoville A, Laurin M, Biol J Linn Soc 2010 100 384 406 10.1111/j.1095-8312.2010.01431.x
21. Bone microanatomy and lifestyle: A descriptive approach. Laurin M, Canoville A, Germain D, Comptes Rendus Palevol 2011 10 381 402 10.1016/j.crpv.2011.02.003
22. Life history and skeletal adaptations in the Galapagos marine iguana (Amblyrhynchus cristatus) as reconstructed with bone histological data - A comparative study of iguanines. Hugi J, Sánchez-Villagra MR, J Herpetol 2012 46 312 324 10.1670/11-071
23. The correlation between high limb-bone density and aquatic habits in recent mammals. Wall WP, Sediment Geol 1983 57 197 207
24. Bone histology of aquatic reptiles: what does it tell us about secondary adaptation to an aquatic life? Houssaye A, Biol J Linn Soc 2012 108 3 21
25. The aging of Wolffs Law: Ontogeny and responses to mechanical loading in cortical bone. Pearson OM, Lieberman DE, Am J Phys Anthropol 2004 125 63 99 10.1002/ajpa.20155
26. The evolution of metriorhynchoidea (Mesoeucrocodylia, Thalattosuchia): An integrated approach using Geometric Morphometrics, Analysis of Disparity, and Biomechanics. Young MT, Brusatte SL, Ruta M, De Andrade MB, Zoological Journal of the Linnean Society 2010 158 801 859 10.1111/j.1096-3642.2009.00571.x
27. Whos afraid of the big bad Wolff?: Wolffs law and bone functional adaptation. Ruff C, Holt B, Trinkaus E, Am J Phys Anthropol 2006 129 484 498 10.1002/ajpa.20371 16425178
28. Skeletal structural adaptations to mechanical usage (SATMU): 1. Redefining Wolffs Law: The bone modeling problem. Frost HM, Anat Rec 1990 226 403 413 10.1002/ar.1092260402 2184695
29. Skeletal structural adaptations to mechanical usage (SATMU): 2. Redefining Wolffs Law: The remodeling problem. Frost HM, Anat Rec 1990 226 414 422 10.1002/ar.1092260403 2184696
30. Regulatory divergence modifies limb length between mammals. Cretekos CJ, Wang Y, Green ED, Program NCS, Martin JF, Rasweiler JJ, Behringer RR, Genes Dev 2008 22 141 151 10.1101/gad.1620408 18198333
31. Temperature regulates limb length in homeotherms by directly modulating cartilage growth. Serrat MA, King D, Lovejoy CO, Proc Natl Acad Sci 2008 105 19348 19353 10.1073/pnas.0803319105 19047632
32. The heat shock response: Systems biology of proteotoxic stress in aging and disease. Morimoto RI, Cold Spring Harb Symp Quant Biol 2011 76 91 99 10.1101/sqb.2012.76.010637 22371371
33. Phylogenetic signal in bone histology of amniotes revisited. Legendre L, Le Roy N, Martinez-Maza C, Montes L, Laurin M, Cubo J, Zoologica Scripta 2012 42 44 53
34. A partial skeleton of Geotrypus antiquus (Talpidae, Mammalia) from the Late Oligocene of the Enspel Fossillagerstätte in Germany. Schwermann A, Martin T, Paläontol Z 2012 86 409 439 23481712
35. Notes on type specimens of European Miocene talpidae and a tentative classification of Old World Tertiary Talpidae (Insectivora: Mammalia). Hutchison JH, Geobios 1974 7 211 256 10.1016/S0016-6995(74)80009-4
36. Order Insectivora: Talpids. Ziegler R, The Miocene land mammals of Europe München: Dr. Friedrich Pfeil, Rössner GE, Heissig K, 1999 53 74
37. Microanatomical diversity of the humerus and lifestyle in lissamphibians. Canoville A, Laurin M, Acta Zoologica 2009 90 110 122 10.1111/j.1463-6395.2008. 00328.x
38. The palaeohistology of the basal ichthyosaur Mixosaurus, Baur, 1887 (Ichthyopterygia, Mixosauridae) from the Middle Triassic: palaeobiological implications. Kolb C, Sánchez-Villagra MR, Scheyer TM, Comptes Rendus Palevol 2011 10 403 411 10.1016/j.crpv.2010.10.008
39. Preparation of fossil bone for histological examination. Chinsamy A, Raath MA, Palaeontologia africana 1992 29 39 44
40. A comparative histological study of recent fossil and recent bone tissues. Part III. Enlow DH, Brown SO, Tex J Sci 1958 10 187 230
41. Bone histology suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria). Hayashi S, Houssaye A, Nakajima Y, Chiba K, Ando T, Sawamura H, Inuzuka N, Naotomo Kaneko N, Tomohiro O, PLoS One 2012 in press
42. Periosteal bone growth rates in extant ratites (Ostriche and Emu). Implications for assessing growth in dinosaurs. Castanet J, Curry Rogers K, Cubo J, Jacques-Boisard J, Comptes Rendus de lAcadémie des Sciences-Series III-Sciences de la Vie 2000 323 543 550 10.1016/S0764-4469(00)00181-5
43. An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Garland T, Midford PE, Ives AR, Am Zool 1999 39 374 388
44. Evolutionary changes in the complexity of the tectum of nontetrapods: A cladistic approach. Maximino C, PLoS One 2008 3 3582 10.1371/journal.pone. 0003582 18974789
45. PAST: Paleontological statistics software package for education and data analysis. Hammer O Harper DAT, Ryan PD, Palaeontol Electron 2001 4 9
46. The laws of bone architecture. Koch JC, Am J Anat 1917 21 298
47. The compressive properties of single osteons. Ascenzi A, Bonucci E, Anat Rec 1968 161 377 391 10.1002/ar.1091610309 4879362
48. The evolution of long bone microstructure and lifestyle in lissamphibians. Laurin M, Girondot M, Loth M-M, Paleobiology 2004 30 589 613 10.1666/0094-8373(2004)030<0589:TEOLBM>2.0.CO;2
49. Hall BK, Bones and cartilage: Developmental and evolutionary skeletal biology Oxford: Elsevier Ltd 2005 83 90