The role of post-natal ontogeny in the evolution of phenotypic diversity in Podarcis lizards

Journal of Evolutionary Biology

Volumn 24, Issue 12, 2011, Pages 2705-2720

  Piras, P ^a,b   Salvi, D ^a,c   Ferrara, G ^d   Maiorino, L ^a,b   Delfino, M ^e,f   Pedde, L ^g   Kotsakis, T ^a,b  

^a Center for Evolutionary Ecology   (Italy)

^b ROMA TRE UNIVERSITY   (Italy)

^c CENTRO DE INVESTIGAÇÃO EM BIODIVERSIDADE E RECURSOS GENÉTICOS   (Portugal)

^d UNIVERSITY OF PALERMO   (Italy)

^e UNIVERSITY OF TURIN   (Italy)

^f UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^g NONE   (Italy)

Author keywords

Allometry; Cephalic scales; Geometric morphometrics; Heterochrony; Hypermorphosis; Sexual dimorphism

Indexed keywords

ALLOMETRY; BIOLOGICAL DEVELOPMENT; EVOLUTIONARY BIOLOGY; GROWTH RATE; HETEROCHRONY (ONTOGENY); LIZARD; MORPHOLOGY; MORPHOMETRY; PHENOTYPIC PLASTICITY; SEXUAL DIMORPHISM;

PODARCIS; SQUAMATA;

EID: 81155127508     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02396.x     Document Type: Article

References (96)

1. Adams, D.C. 2010. Parallel evolution of character displacement driven by competitive selection in terrestrial salamanders. BMC Evol. Biol. 10: 72.
2. Adams, D.C. & Collyer, M.L. 2007. Analysis of character divergence along environmental gradients and other covariates. Evolution 61: 510-515.
3. Adams, D.C. & Collyer, M.L. 2009. A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution 63: 1143-1154.
4. Adams, D.C. & Nistri, A. 2010. Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evol. Biol. 10: 216.
5. Adams, D.C., Rohlf, F.J. & Slice, D.E. 2004. Geometric morphometrics: ten years of progress following the "revolution". Ital. J. Zool. 71: 5-16.
6. Alberch, P. 1981. Convergence and parallelism in foot morphology in the neotropical salamander genus Bolitoglossa. I. Function. Evolution 35: 84-100.
7. Alberch, P. 1982. Developmental constraints in evolutionary processes. In: Evolution and Development (J.T. Bonner, ed.), pp. 313-332. Springer, New York.
8. Alberch, P., Gould, S.J., Oster, G.F. & Wake, D.B. 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5: 296-317.
9. Arnold, E.N. 1989. Towards a phylogeny and biogeography of the Lacertidae: relationships within an old-world family of lizards derived from morphology. Bull. Brit. Mus. Nat. Hist. 55: 209-257.
10. Arnold, E.N. 1993. Phylogeny and the Lacertidae. In: Lacertids of the Mediterranean Region (E.D. Valakos, W. Bohme, V. Perez-Mellado & P. Maragou, eds), pp. 1-16. Hellenic Zoological Society, Athens.
11. Arnold, E.N. 1998. Structural niche, limb morphology and locomotion in lacertid lizards (Squamata, Lacertidae); a preliminary survey. Bull. Nat Hist. Mus. Lond. 6: 63-89.
12. Arnold, E.N. 2002. A Field Guide to the Reptiles and Amphibians of Britain and Europe. Collins, London.
13. Arnold, E.N., Arribas, O. & Carranza, S. 2007. Systematics of the palaearctic and oriental lizard tribe Lacertini (Squamata: Lacertidae: Lacertinae), with descriptions of eight new genera. Zootaxa 1430: 1-86.
14. Badyaev, A.V., Hill, G.E. & Whittingham, L.A. 2001. The evolution of sexul size dimorphism in the house finch. IV. Population divergence in ontogeny. Evolution 55: 2534-2549.
15. de Beer, G.R. 1954. Archaeopteryx lithographica. A Study Based Upon the British Museum Specimen. British Museum (Natural History), London.
16. Bookstein, F.L. 1989. Principal warps: thin-plate splines and the decomposition of deformations. IEEE Trans. Pattern Anal. Mach. Intell. 11: 567-585.
17. Bookstein, F.L. 1991. Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press, Cambridge.
18. Bookstein, F.L., Schäfer, K., Prossinger, H., Seidler, H., Fieder, M., Stringer, C. et al. 1999. Comparing frontal cranial profiles in archaic and modern Homo by morphometric analysis. Anat. Rec. 257: 217-224.
19. Braña, F. 1996. Sexual dimorphism in lacertid lizards: male head increase vs female abdomen increase? Oikos 75: 511-523.
20. Brown, R.P., Terrasa, B., Pérez-Mellado, V., Castro, J.A., Hoskisson, P.A., Picornell, A. et al. 2008. Bayesian estimation of post-Messinian divergence times in Balearic Island lizards. Mol. Phyl. Evol. 48: 350-358.
21. Bruner, E. & Costantini, D. 2007. Head morphological variation in Podarcis muralis and Podarcis sicula: a landmark-based approach. Amphibia-Reptilia 28: 566-573.
22. Bruner, E., Costantini, D., Fanfani, A. & Dell'Omo, G. 2005. Morphological variation and sexual dimorphism of the cephalic scales in Lacerta bilineata. Acta Zool. 86: 245-254.
23. Butler, M.A. & Losos, J.B. 2002. Multivariate sexual dimorphism, sexual selection, and adaptation in Greater Antillean Anolis lizards. Ecol. Mon. 72: 541-559.
24. Butler, M.A., Sawyer, S.A. & Losos, J.B. 2007. Sexual dimorphism and adaptive radiation in Anolis lizards. Nature 447: 202-205.
25. Calsbeek, R. & Irschick, D.J. 2007. The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards. Evolution 61: 2493-2503.
26. Capula, M. & Ceccarelli, A. 2003. Distribution of genetic variation and taxonomy of insular and mainland populations of the Italian wall lizard, Podarcis sicula. Amphibia-Reptilia 24: 483-495.
27. Capula, M., Luiselli, L. & Rugiero, L. 1993. Comparative ecology in sympatric Podarcis muralis and P. sicula (Reptilia: Lacertidae) from the historical centre of Rome: what about competition and niche segregation in an urban habitat? Boll. Zool. 60: 287-291.
28. Cardini, A. 2003. The Geometry of the Marmot (Rodentia: Sciuridae). Mandible: phylogeny and patterns of morphological evolution. Syst. Biol. 52: 186-205.
29. Clarke, J.A. & Middleton, K.M. 2008. Mosaicism, modules, and the evolution of birds: results from a Bayesian approach to the study of morphological evolution using discrete character data. Syst. Biol. 57: 185-201.
30. Collyer, M.L. & Adams, D.C. 2007. Analysis of two-state multivariate phenotypic change in ecological studies. Ecology 88: 683-692.
31. Corti, C. & Lo Cascio, P. 2002. The Lizards of Italy and Adjacent Areas. Chimaira Verlag, Frankfurt-am-Main.
32. Darwin, C. 1858. On the tendency of species to form varieties, and on the perpetuation of varieties and species by natural means of selection. I. Extract from an unpublished work on species, II. Abstract of a letter from C. Darwin, Esq., to Prof. Asa Gray. J. Proc. Linn. Soc. Zoology 3: 45-53.
33. Fisěr, C., Bininda-Emonds, O.R.P., Blejec, A. & Sket, B. 2008. Can heterochrony help explain the high morphological diversity within the genus Niphargus (Crustacea: Amphipoda)? Org. Div. Evol. 8: 146-162.
34. Frankino, W.A., Zwaan, B.J., Stern, D.L. & Brakefield, P.M. 2005. Natural selection and developmental constrains in the evolution of allometries. Science 307: 718-720.
35. Fusco, G. & Minelli, A. 2010. Phenotypic plasticity in development and evolution: facts and concepts. Phil. Trans. R. Soc. B. 365: 547-556.
36. Futuyma, D.J. 2005. Evolution. Sinauer Associates, Sunderland, MA, USA.
37. Gaston, K.J. 1996. What is biodiversity. In: Biodiversity: A Biology of Numbers and Difference (K.J. Gaston, ed.), pp. 1-9. Blackwell Science Ltd, Oxford, UK.
38. Godfrey, L.R. & Sutherland, M. 1995. Flawed inference: why size-based tests of heterochronic processes do not work. J. Theor. Biol. 172: 43-61.
39. Goodall, C. 1991. Procrustes methods in the statistical analysis of shape. J. R. Statist. Soc. B 53: 285-339.
40. Gould, S.J. 1977. Ontogeny and Phylogeny. Harvard University Press, Cambridge, MA, USA.
41. Gould, S.J. 2002. The Structure of Evolutionary Theory. Harvard University Press, Cambridge.
42. Hall, B.K. 1992. Evolutionary Developmental Biology. Chapman and Hall, London.
43. Harris, D.J., Pinho, C., Carretero, M.A., Corti, C. & Böhme, W. 2005. Determination of genetic diversity within Podarcis tiliguerta using mtDNA sequence data, with a reassessment of the phylogeny of Podarcis. Amphibia-Reptilia 26: 401-407.
44. Herrel, A., Van Damme, R. & De Vree, F. 1996. Sexual dimorphism of head size in Podarcis hispanica atrata: testing the dietary divergence hypothesis by bite force analysis. Neth. J. Zool. 46: 253-262.
45. Herrel, A., de Grauw, E. & Lemos-Espinal, J.A. 2001. Head shape and bite performance in xenosaurid lizards. J. Exp. Zool. 290: 101-107.
46. Hollander, J., Adams, D.C. & Johannesson, K.K. 2006. Evolution of adaptation through allometric shifts in a marine snail. Evolution 60: 2490-2497.
47. Holtmeier, C.L. 2001. Heterochrony, maternal effects, and phenotypic variation among sympatric pupfishes. Evolution 55: 330-338.
48. Husack, J.F., Lappin, A.K., Fox, S.F. & Lemos-Espinal, J.A. 2006. Bite-force performance predicts dominance in male venerable collared lizards (Crotaphytus antiquus). Copeia 2006: 301-306.
49. Huttegger, S. & Mitteroecker, P. 2011. Invariance and meaningfulness in phenotype spaces. Evol. Biol. 38: 335-352.
50. Kaliontzopoulou, A. 2010. Proximate and evolutionary causes of phenotypic diversification: morphological variation in Iberian and North African Podarcis wall lizards. PhD Thesis, University of Barcelona, Barcelona.
51. Kaliontzopoulou, A., Carretero, M.A. & Llorente, G.A. 2007. Multivariate and geometric morphometrics in the analysis of sexual dimorphism variation in Podarcis lizards. J. Morphol. 268: 152-165.
52. Kaliontzopoulou, A., Carretero, M.A. & Llorente, G.A. 2008. Interspecific and intersexual variation in presacral vertebrae number in Podarcis bocagei and P. carbonelli. Amphibia-Reptilia 29: 288-292.
53. Kaliontzopoulou, A., Carretero, M.A. & Llorente, G.A. 2010. Intraspecific ecomorphological variation: linear and geometric morphometrics reveal habitat-related patterns within Podarcis bocagei wall lizards. J. Evol. Biol. 23: 1234-1244.
54. Kaliontzopoulou, A., Pinho, C., Harris, D.J. & Carretero, M.A. 2011. When cryptic diversity blurs the picture: a cautionary tale from Iberian and North African Podarcis wall lizards. Biol. J. Linn. Soc. 103: 779-800.
55. Kelly, C.D. & Adams, D.C. 2010. Sexual selection, ontogenetic acceleration, and hypermorphosis generates male trimorphism in Wellington tree weta. Evol. Biol. 37: 200-209.
56. Klingenberg, C.P. 2005. Developmental constraints, modules, and evolvability. In: Variation: A Central Concept in Biology (B. Hallgrimsson & B.K. Hall, eds), pp. 219-247. Elsevier Academic Press, Burlington, MA, USA.
57. Klingenberg, C.P. 2010. There's something afoot in the evolution of ontogenies. BMC Evol. Biol. 10: 221.
58. Klingenberg, C.P. 2011. MorphoJ: an integrated software package for geometric morphometrics. Mol. Ecol. Res. 11: 353-357.
59. Klingenberg, C.P., Barluenga, M. & Meyer, A. 2002. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56: 1909-1920.
60. Ljubisavljevic, K., Urosevic, A., Aleksic, I. & Ivanovic, A. 2010. Sexual dimorphism of skull shape in a lacertid lizard species (Podarcis spp., Dalmatolacerta sp., Dinarolacerta sp.) revealed by geometric morphometrics. Zoology (Jena) 113: 168-174.
61. Losos, J.B. 1990. The evolution of form and function: morphology and locomotor performance in West Indian Anolis lizards. Evolution 44: 1189-1203.
62. Losos, J.B. 2009. Lizards in an Evolutionary Tree. University of California Press, Berkeley.
63. Losos, J.B., Douglas, A.C., Glossip, D., Goellner, R., Hampton, A., Roberts, G. et al. 2000. Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54: 301-305.
64. Mabee, P.M., Olmstead, K.L. & Cubbage, C.C. 2000. An experimental study of intraspecific variation, developmental timing, and heterochrony in fishes. Evolution 54: 2091-2106.
65. Marroig, G. & Cheverud, J. 2005. Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World Monkeys. Evolution 59: 1128-1142.
66. Maynard-Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B. et al. 1985. Developmental constraints and evolution. Q. Rev. Biol. 60: 265-287.
67. McKinney, M.L. 1988. Heterochrony in Evolution. Plenum Press, New York.
68. McKinney, M.L. & McNamara, K.J. 1991. Heterochrony: The Evolution of Ontogeny. Plenum Press, New York.
69. Mitteroecker, P. & Bookstein, F. 2008. The evolutionary role of modularity and integration in the hominoid cranium. Evolution 62: 943-958.
70. Mitteroecker, P. & Gunz, P. 2009. Advances in geometric morphometrics. Evol. Biol. 36: 235-247.
71. Mitteroecker, M., Gunz, P. & Bookstein, F.L. 2005. Heterochrony and geometric morphometrics: a comparison of cranial growth in Pan paniscus versus Pan troglodytes. Evol. Dev. 7: 244-258.
72. Monteiro, L.R. 1999. Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Syst. Biol. 48: 192-199.
73. Mouton, N. & van Wyk, J.H. 1993. Sexual dimorphism in cordylid lizards: a case study of the Drakensberg crag lizard, Pseudocordylus melanotus. Can. J. Zool. 71: 1715-1723.
74. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., O'Hara, R.B., Simpson, G.L. et al. 2011. Vegan: community ecology package. R package version 1.17-7.
75. Olsson, M., Shine, R., Wapstra, E., Ujvari, B. & Madsen, T. 2002. Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection. Evolution 56: 1538-1542.
76. Pérez-Mellado, V. & Corti, C. 1993. Dietary adaptations and herbivory in lacertid lizards of the genus Podarcis from western Mediterranean islands (Reptilia: Sauria). Bonn. Zool. Beitr. 44: 193-220.
77. Piras, P., Colangelo, P., Adams, D.C., Buscalioni, A., Cubo, J. & Kotsakis, T. et al. 2010. The Gavialis-Tomistoma debate: the contribution of skull ontogenetic allometry and growth trajectories to the study of crocodilian relationships. Evol. Dev. 12: 568-579.
78. Podnar, M., Mayer, W. & Tvrtković, N. 2005. Phylogeography of the Italian wall lizard, Podarcis sicula, as revealed by mitochondrial DNA sequences. Mol. Ecol. 14: 575-588.
79. Poulakakis, N., Lymberakisa, P., Valakos, E., Pafilis, P., Zouros, E. & Mylonas, M. 2005. Phylogeography of Balkan wall lizard (Podarcis taurica) and its relatives inferred from mitochondrial DNA sequences. Mol. Ecol. 14: 2433-2443.
80. R Development Core Team 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. URL
81. Raia, P., Guarino, F.M., Turano, M., Polese, G., Rippa, D., Carotenuto, F. et al. 2010. The blue lizard spandrel and the island syndrome. BMC Evol. Biol. 10: 289.
82. Reilly, S.M. 1994. The ecological morphology of metamorphosis: heterochrony and the evolution of feeding mechanisms in salamanders. In: Ecological Morphology: Integrative Approaches in Organismal Biology (P.C. Wainwright & S.M. Reilly, eds), pp. 319-338. University of Chicago Press, Chicago.
83. Reilly, S.M., Wiley, E.O. & Meinhardt, D.J. 1997. An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomena. Biol. J. Linn. Soc. 60: 119-143.
84. Revell, L.J., Johnson, M.A., Schulte, J.A., Kolbe, J.J. & Losos, J.B. 2007. A phylogenetic test for adaptive convergence in rock-dwelling lizards. Evolution 61: 2898-2912.
85. Rohlf, F.J. & Marcus, L.F. 1993. A revolution in morphometries. Trends Ecol. Evol. 8: 129-132.
86. Rohlf, F.J. & Slice, D. 1990. Extensions of the procrustes method for the optimal superimposition of landmarks. Syst. Biol. 39: 40-59.
87. Sanger, T.J., Losos, J.B. & Gibson-Brown, J.J. 2008. A developmental staging series for the lizard genus Anolis: A new system for the integration of evolution, development, and ecology. J. Morph. 269: 129-137.
88. Schluter, D. 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford.
89. Takacs, D. 1996. The Idea of Biodiversity. Philosophies of Paradise. Johns Hopkins University Press, Baltimore, MD, USA.
90. Vanhooydonck, B. & Van Damme, R. 1999. Evolutionary relationships between body shape and habitat use in lacertid lizards. Evol. Ecol. Res. 1: 785-805.
91. Vanhooydonck, B., Van Damme, R. & Aerts, P. 2000. Ecomorphological correlates of habitat partitioning in Corsican lacertid lizards. Funct. Ecol. 14: 358-368.
92. Verwaijen, D., Van Damme, R. & Herrel, A. 2002. Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards. Funct. Ecol. 16: 842-850.
93. Werneburg, I. & Sánchez-Villagra, M.R. 2009. Timing of organogenesis support basal position of turtles in the amniote tree of life. BMC Evol. Biol. 9: 82.
94. Wilson, L.A.B. & Sánchez-Villagra, M.R. 2010. Diversity trends and their ontogenetic basis: an exploration of allometric disparity in rodents. Proc. R. Soc. B 277: 1227-1234.
95. Yeh, J. 2002. The evolution of development: two portraits of skull ossification in pipoid frogs. Evolution 56: 2484-2498.
96. Zelditch, M.L., Swiderski, D.L., Sheets, H.D. & Fink, W.L. 2004. Geometric Morphometrics for Biologists: A Primer. Elsevier/Academic Press, Amsterdam.