Testing convergent and parallel adaptations in talpids humeral mechanical performance by means of geometric morphometrics and finite element analysis

Journal of Morphology

Volumn 273, Issue 7, 2012, Pages 696-711

  Piras, P ^a,b   Sansalone, G ^a,b,c   Teresi, L ^b   Kotsakis, T ^a,b   Colangelo, P ^c   Loy, A ^a,d  

^a LEONARDO S P A   (Italy)

^b ROMA TRE UNIVERSITY   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF MOLISE   (Italy)

Author keywords

Comparative methods; Finite element analysis; Geometric morphometrics; Parallel evolutionary trajectories; Talpid humerus

Indexed keywords

ACCLIMATIZATION; ADAPTATION; ANIMAL; ARTICLE; BIOMECHANICS; CLASSIFICATION; EVOLUTION; FINITE ELEMENT ANALYSIS; HISTOLOGY; HUMERUS; MAMMAL; MOLE (INSECTIVORA); PHENOTYPE; PHYLOGENY; PHYSIOLOGY;

ACCLIMATIZATION; ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; BIOMECHANICS; CLASSIFICATION; FINITE ELEMENT ANALYSIS; HUMERUS; MAMMALS; MOLES; PHENOTYPE; PHYLOGENY;

CONDYLURA; TALPIDAE; TALPINAE;

EID: 84861954513     PISSN: 03622525     EISSN: 10974687     Source Type: Journal    
DOI: 10.1002/jmor.20015     Document Type: Article

References (92)

1. Abe H, Ishii N. 2008. Urotrichus talpoides. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.04.00.
2. Adams DC, Collyer ML. 2009. A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution 63: 1143-1154.
3. Adams DC, Rohlf FJ, Slice DE. 2004. Geometric morphometrics: Ten years of progress following the "revolution." Ital J Zool 71: 5-16.
4. Anthony HE. 1929. Field Book of North American Mammals. Whitefish: Kessinger publishing. 748 p.
5. Arnold SJ. 1994. Is there a unifying concept of sexual selection that applies to both plants and animals? Am Nat 114: 1-12.
6. Bookstein FL. 1986. Size and shape spaces for landmark data in two dimensions. Stat Sci 1: 181-222.
7. Bookstein FL. 1991. Morphometric tools for landmark data. Cambridge: Cambridge University Press. 456 p.
8. Bookstein FL, Streissguth AP, Sampson PD, Connor PD, Barr HM. 2002. Corpus callosum shape and neuropsychological deficits in adult males with heavy fetal alcohol exposure. Neuroimage 15: 233-251.
9. Cabral MJ, Almeida J, Almeida PR, Dellinger T, Ferrand de Almeida N, Oliveira ME, Palmeiri m JM, Queiroz AI, Rogado L, Santos-Reis M. 2005. Livro Vermelho dos Vertebrados de Portugal [Red Book of Vertebrates of Portugal]. Lisbona: Instituto de Conservação da Natureza. 660 p.
10. Cabria MT, Rubines J, Gomez-Molina B, Zardoya R. 2006. On the phylogenetic position of a rare Iberian endemic mammal, the Pyrenean desman (Galemys pyrenaicus). Gene 375: 1-13.
11. Campbell KL, Hochachka W. 2000. Thermal biology and metabolism of the American shrew-mole Neurotrichus gibbsii. J Mammal 81: 578-585.
12. Campbell KL, Storz JF, Signore AV, Moriyama H, Catania KC, Payson AP, Bonaventura J, Stetefeld JJ, Weber RE. 2010. Molecular basis of a novel adaptation to hypoxic-hypercapnia in a strictly fossorial mole. BMC Evol Biol 10: 214.
13. Chiozza F. 2008. Scaptonyx fusicaudus. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.04.00.
14. Claude J. 2008. Morphometrics with R. New York: Springer Science+Business Media, LLC. 318 p.
15. Colangelo P, Bannikova A, Kristufek B, Lebedev VF, Annesi F, Capanna E, Loy A. 2010. Molecular systematics and evolutionary biogeography of the genus Talpa (Soricomorpha: Talpidae). Mol Phylogenet Evol 55: 372-80.
16. Dalquest WW, Orcutt DR. 1942. The biology of the least shrew-mole, Neurotrichus gibbsii minor. Am Midl Nat 27: 387-401.
17. Darwin CR. 1859. The Origin of Species. London: John Murray, Albemarle Street. 560 p.
18. Dobzhansky T. 1956. What is an adaptive trait? Am Nat 90: 337-347.
19. Dobzhansky T. 1970. Genetics of the Evolutionary Process. New York: Columbia University Press. 505 p.
20. Dobzhansky T, Ehrman L, Kastritsis P. 1968. Ethological isolation between sympatric and allopatric species of the obscura group of Drosophila. Anim Behav 16: 79-87.
21. Edwards LF. 1937. Morphology of the forelimb of the mole (Scalops aquaticus, L.) in relation to its fossorial habits. Ohio J Sci 37: 20-41.
22. Farke AA. 2008. Frontal sinuses and head-butting in goats: A finite element analysis. J Exp Biol 211: 3084-3095.
23. Freeman RA. 1886. The anatomy of the shoulder and upper arm of the mole (Talpa europaea). J Anat Phys XX: Pl.V.
24. Fritz SA, Purvis A. 2010. Phylogenetic diversity does not capture body size variation at risk in the world's mammals. Proc R Soc B 277: 2435-2441.
25. Gambaryan P, Gasc JP, Renous S. 2003. Cinefluorographical study of the burrowing movements in the common mole, Talpa europaea (Lipotyphla, Talpidae). Russ J Theriol 1: 91-109.
26. Glor RE. 2010. Phylogenetic insights of adaptative radiation. Annu Rev Ecol Evol Syst 41: 251-70.
27. Goodall C. 1991. Procrustes methods in the statistical analysis of shape. J R Stat Soc 53: 285-339.
28. Gould SJ. 2002. The Structure of Evolutionary Theory. Harvard MA: Harvard University Press. 1433 p.
29. Gould SJ, Lewontin RC. 1979. The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptionist programme. Proc R Soc Lond 205: 581-598.
30. Gould SJ, Vrba ES. 1982. Exaptation - A missing term in the science of form. Paleobiology 8: 4-15.
31. Gröning F, Liu J, Fagan MJ, O'Higgins P. 2009. Validating a voxel-based finite element model of a human mandible using digital speckle pattern interferometry. J Biomech 42: 1224-1229.
32. Harmon LJ, Weir J, Brock C, Glor RE, Challenger W. 2008. GEIGER: investigating evolutionary radiations. Bioinformatics 24: 129-131.
33. Hickman GC. 1983. Influence of the semiaquatic habit in determining burrow structure of the star-nosed mole (Condylura cristata). Can J Zool 61: 1688-1692.
34. Hutterer R. 2005. Order soricomorpha. In: Wilson, D.E, Reeder, D.M. (Eds.), Mammals Species of the World. A taxonomic and Geographic Reference, 3rd ed. Baltimore: The Johns Hopkins University Press, pp 220-311.
35. Ives RA, Garland TJr. 2010. Phylogenetic logistic regression for binary dependent variables. Syst Biol 59: 9-26.
36. Jones KE, Goswami A. 2010. Quantitative analysis of the influences of phylogeny and ecology on phocid and otariid pinniped (Mammalia; Carnivora) cranial morphology. J Zool 280: 297-308.
37. Kawada S, Shinohara A, Kobayashi S, Harada M, Oda S, Liang-Kong L. 2007. Revision of the mole genus Mogera (Mammalia: Lipotyphla: Talpidae) from Taiwan. Syst Biodiv 5: 223-240.
38. Kays RW, Wilson DE. 2009. Mammals of North America, 2nd ed. Princeton NJ: Princeton University Press. 248 p.
39. Klingenberg CP. 2011. MorphoJ. Faculty of Life Sciences, University of Manchester, UK. Available at:.
40. Kupczik K, Dobson CA, Fagan MJ, Crompton RH, Oxnard CE, O'Higgins P. 2007. Assessing mechanical function of the zygomatic region in macaques: Validation and sensitivity testing of finite element models. J Anat 210: 41-53.
41. Losos JB, Mahler DL. 2010. Adaptive radiation: the interaction of ecological opportunity, adaptation, and speciation. In: Bell MA, Futuyma D, Eanes WF, Levinton JS, editors. Evolution After Darwin: The First 150 Years. Chapter15. Sunderland Ma: Sinauer.
42. Losos JB, Miles DB. 2002. Testing the hypothesis that a clade has adaptively radiated: iguanid lizard clades as a case study. Am Nat 160: 147-157.
43. Loy A, Colangelo P, Annesi F, Capanna E. 2005. Origin and evolution of Western European moles (genus Talpa, Insectivora, Mammalia): A multidisciplinary approach. Mamm Study 30: 13-17.
44. Loy A. 2008. Famiglia Talpidae. In: Amori G, Contoli L, Nappi A, editors. Mammalia II Erinaceomorpha, Soricomorpha, Lagomorpha, Rodentia. Fauna d'Italia, vol. XLIV, Bologna. Edizioni Calderini de Il Sole 24 ORE Edagricole, pp 91-130.
45. Lunde DP, Musser GG, Truong Son N. 2003. A survey of small mammals from Mt. Tay Con Linh II, Vietnam, with the description of a new species of Chodsigoa (Insectivora: Soricidae). Mamm Study 28: 31-46.
46. Maddison WP, Maddison DR. 2010. Mesquite: A modular system for evolutionary analysis. Version 2.73.
47. Mahler DL, Revell LJ, Glor RE, Losos JB. 2010. Ecological opportunity and the rate of morphological evolution in the diversification of the Greater Antillean anoles. Evolution 64: 2731-2745.
48. McKenna MC, Bell SK. 1997. Classification of Mammals Above the Species Level. New York: Columbia University Press. 631 p.
49. Meloro C, Raia P, Piras P, Barbera C, O'Higgins P. 2008. The shape of the mandibular corpus in large fissiped carnivores: allometry, function and phylogeny. Zool J Linn Soc 154: 832-845.
50. Motokawa M. 2004. Phylogenetic relationships within the family Talpidae (Mammalia: Insectivora). J Zool Lond 263: 147-157.
51. O'Meara BC, Ané C, Sanderson MJ, Wainwright PC. 2006. Testing for different rates of continuous trait evolution using likelihood. Evolution 60: 922-933.
52. Perez SI, Bernal V, Gonzalez PN. 2006. Differences between sliding semi-landmark methods in geometric morphometrics, with an application to human cranio-facial and dental variation. J Anat 208: 769-784.
53. Pierce SE, Angielczyk KD, Rayfield EJ. 2008. Patterns of morphospace occupation and mechanical performance in extant crocodilian skulls: A combined geometric morphometric and finite element modeling approach. J Morphol 269: 840-864.
54. Pierce SE, Angielczyk KD, Rayfield EJ. 2009a. Morphospace occupation in thalattosuchian crocodylomorphs: Skull shape variation, species delineation and temporal patterns. Palaeontology 52: 1057-1097.
55. Pierce SE, Angielczyk KD, Rayfield EJ. 2009b. Shape and mechanics in thalattosuchian (Crocodylomorpha) skulls: Implications for feeding behaviour and niche partitioning. J Anat 215: 555-576.
56. Piras P, Maiorino L, Raia P, Marcolini F, Salvi D, Vignoli L, Kotsakis T. 2010. Functional and phylogenetic constraints in Rhinocerotinae craniodental morphology. Evol Ecol Res 12: 897-928.
57. Piras P, Salvi D, Ferrara G, Maiorino L, Delfino M, Pedde L, Kotsakis T. 2011. The role of post-natal ontogeny in the evolution of phenotypic diversity in Podarcis lizards. J Evol Biol 24: 2705-2720.
58. Raia P, Carotenuto F, Meloro C, Piras P, and D. Pushkina. 2010. The shape of contention. Adaptation, history and contingency in ungulate mandibles. Evolution 64: 1489-1503.
59. Rayfield EJ. 2007. Finite element analysis and understanding the biomechanics and evolution of living and fossil organism. Annu Rev Earth Planet Sci 35: 541-576.
60. Rayfield EJ. 2011. Strain in the ostrich mandible during simulated pecking and validation of specimen-specific finite elements model. J Anat 218: 47-58.
61. Rayfield EJ, Norman DB, Horner CC, Horner JR, May Smith P, Thomason JJ, Upchurch P. 2001 Cranial design and function in a large theropod dinosaur. Nature 409: 1033-1037.
62. Reed CA. 1951. Locomotion and appendicular anatomy in three soricoid insectivores. Am Midl Nat 45: 513-671.
63. Revell LJ. 2011. Phylogenetic tools for comparative biology (and other things). Available at:.
64. Revell LJ. 2008. On the analysis of evolutionary change along single branches in a phylogeny. Am Nat 172: 140-147.
65. Revell LJ, Johnson MA, Schulte JA, Kolbe JJ, Losos JB. 2007. A phylogenetic test for adaptive convergence in rock-dwelling lizards. Evolution 61: 2898-2912.
66. Revell LJ, Mahler DL, Peres-Neto PR, Redelings BD. 2012. A new phylogenetic method for identifying exceptional phenotypic diversification. Evolution 66: 135-146.
67. Richmond BG, Wright BW, Grosse I, Dechow PC, Ross CF, Spencer MA, Strait DS. 2005. Finite element analysis in functional morphology. Anat Rec A Discov Mol Cell Evol Biol 283: 259-274.
68. Rohlf FJ, Slice DE. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39: 40-59.
69. Rohlf FJ. 2006. TpsDig 2.05. Department of Ecology and Evolution. Stony Brook, NY: State University of NY.
70. Ross CF, Patel BA, Slice DE, Strait DS, Dechow PC, Richmond BG, Spencer MA. 2005. Modeling masticatory muscle force in finite element analysis: Sensitivity analysis using principal coordinates analysis. Anat Rec A Discov Mol Cell Evol Biol 283: 288-299.
71. Sánchez-Villagra MR, Horovitz I, Motokawa M. 2006. A comprehensive morphological analysis of talpid moles (Mammalia) Phylogenetic relationship. Cladistics 22: 59-88.
72. Sánchez-Villagra MR, Menke PR, Geisler JH. 2004. Patterns of evolutionary transformation in the humerus of moles (Talpidae, Mammalia): A character analysis. Mamm Study 29: 163-170.
73. Schluter D. 2000. The ecology of adaptive radiation. Oxford: Oxford University Press. 300 p.
74. Schwenk K. 1995. A utilitarian approach to evolutionary constraint. Zoology 98: 251-262.
75. Scott RG, Richardson RC. 2005. Realities of biologically inspired design with a subterranean digging robot example. Robot Appl 498: 1-6.
76. Shinohara A, Campbell KL, Suzuki H. 2003. Molecular phylogenetic relationships of moles, shrew moles, and desmans from the new and old worlds. Mol Phylogenet Evol 27: 247-258.
77. Shinohara A, Suzuki H, Tsuchiya K, Zhang YP, Luo J, Jiang XL, Wang YX, Campbell KL. 2004. Evolution and biogeography of talpid moles from continental East Asia and the 72 Japanese Islands inferred from mitochondrial and nuclear gene sequences. Zool Sci 21: 1177-1185.
78. Simpson GG. 1961. Principles of Animal Taxonomy. New York: Columbia University Press. 247 p.
79. Slater GJ, Figueirido B, Louis L, Yang P, Van Valkenburgh B. 2010. Biomechanical consequences of rapid evolution in the polar bear lineage. PLoS One 5: e13870.
80. Smith AT, Xie Y. 2008. A guide to the mammals of China. Princeton NJ: Princeton University Press. 576 p.
81. Stayton CT. 2006. Testing the hypotheses of convergence with multivariate data: morphological and functional convergence among herbivorous lizard. Evolution 60: 824-841.
82. Stayton CT. 2008. Is convergence surprising? An examination of the frequency of convergence in simulated datasets. J Theor Biol 252: 1-14.
83. Stayton CT. 2009. Application of thin-plate spline transformations to finite elements models, or, how to turn a bog turtle into a spotted turtle to analyze both. Evolution 63: 1348-1355.
84. Stone RD. 1995.IUCN Species Survival Commission, Insectivore, Tree-Shrew and Elephant-Shrew Specialist Group; Sultanate of Oman, Sir Peter Scott IUCN/SSC Action Plan Fund; Chicago Zoological Society; National Wildlife Federation; English Nature; WWF Gland: IUCN.
85. Strait DS, Wang Q, Dechow PC, Ross CF, Richmond BG, Spencer MA, Patel BA. 2005. Modeling elastic properties in finite-element analysis: How much precision is needed to produce an accurate model? Anat Rec A Discov Mol Cell Evol Biol 283: 275-287.
86. Strömberg CAE. 2006. Evolution of hypsodonty in equids: testing a hypothesis of adaptation. Paleobiology 32: 236-258.
87. Thomas GH, Freckleton RP, Székely T. 2006. Comparative analyses of the influence of developmental mode on phenotypic diversification rates in shorebirds. Proc R Soc Lond B 273: 1619-1624.
88. Tsytsulina K, Formozov N, Sheftel, B, Zagorodnyuk I. 2008. Desmana moschata. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.04.
89. van Cleef-Roders JT, van den Hoek Ostende LW. 2001. Dental morphology of Talpa europaea and Talpa occidentalis (Mammalia: Insectivora) with a discussion of fossil Talpa in the Pleistocene of Europe. European Talpa. Zool Med Leiden 75: 51-58.
90. Young MT, Brusatte SL, Ruta M, De Andrade MB. 2010. The evolution of Metriorhynchoidea (mesoeucrocodylia, thalattosuchia): An integrated approach using geometric morphometrics, analysis of disparity, and biomechanics. Zool J Linn Soc 158: 801-859.
91. Ziegler R. 2003. Moles (Talpidae) from the Middle Miocene in South Germany. Acta Palaeontol Pol 48: 617-648.
92. Zienkiewicz OC, Taylor RL, Zhu JZ. 2005. The finite elements method: its basis and fundamentals. Amsterdam: Elsevier. 733 p.