Sexual dimorphism in traits related to locomotion: Ontogenetic patterns of variation in Podarcis wall lizards

Biological Journal of the Linnean Society

Volumn 99, Issue 3, 2010, Pages 530-543

  Kaliontzopoulou, Antigoni ^a,b   Carretero, Miguel A ^a   Llorente, Gustavo A ^b  

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

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Ecological dimorphism; Iberian peninsula; Integration; Lacertidae

Indexed keywords

BODY SIZE; COVARIANCE ANALYSIS; HABITAT USE; LIZARD; LOCOMOTION; ONTOGENY; SEXUAL DIMORPHISM; SEXUAL SELECTION;

IBERIAN PENINSULA;

ANIMALIA; LACERTIDAE; PODARCIS; PODARCIS BOCAGEI; PODARCIS CARBONELLI; SQUAMATA;

EID: 76449114778     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2009.01385.x     Document Type: Article

References (89)

1. Abell AJ. Male-female spacing patterns in the lizard, Sceloporu virgatus. Amphibia-Reptilia 1999, 20:185-194.
2. Aerts P, Van Damme R, Vanhooydonck B, Zaaf A, Herrel A. Lizard locomotion: how morphology meets ecology. Netherlands Journal of Zoology 2000, 30:261-277.
3. Alexander RMcN. Size, shape, and structure for running and flight. A companion to animal physiology 1982, 309-324. Taylor CRJohansen KBolis L. In, eds., Cambridge, Cambridge University Press
4. Andersson M. Sexual selection 1994, Princeton, NJ, Princeton University Press
5. Arnold EN. Relationships of the Palearctic lizards assigned to the genera Lacerta, Algyroides and Psammodromus (Reptilia: Lacertidae). Bulletin of the British Museum Natural History (Zoology) 1973, 25:289-366.
6. Arnold EN. Towards a phylogeny and biogeography of the Lacertidae: relationships within an Old-World family of lizards derived from morphology. Bulletin of the British Museum Natural History (Zoology) 1989, 55:209-257.
7. Arnold EN. Structural niche, limb morphology and locomotion in lacertid lizards (Squamata, Lacertidae): a preliminary study. Bulletin of the British Museum Natural History (Zoology) 1998, 64:63-89.
8. Arnold SJ. Sexual selection: the interface of theory and empiricism. Mate choice 1983, 67-107. Bateson P. In, ed., Cambridge, Cambridge University Press
9. Barreto-Caldas F, Honrado J, Paiva AP. Vegetação da área de paisagem Protegida do Litoral de Esposende (Portugal). Quercetea 1999, 1:39-59.
10. Bauwens D, Garland T, Castilla AM, Van Damme R. Evolution of sprint speed in lacertid lizards: morphological, physiological, and behavioral covariation. Evolution 1995, 49:848-863.
11. 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 1995, 57:289-300.
12. Braña F. Sexual dimorphism in lacertid lizards: male head increase vs female abdomen increase? Oikos 1996, 75:511-523.
13. Brecko J, Huyghe K, Vanhooydonck B, Herrel A, Grbac I, Van Damme R. Functional and ecological relevance of intraspecific variation in body size and shape in the lizard Podarcis melisellensis (Lacertidae). Biological Journal of the Linnean Society 2008, 94:251-264.
14. Brown JH, West GB, Enquist BJ. Scaling in biology: patterns and processes, causes and consequences. Scaling in biology 2000, 1-24. Brown JH, West GB, In, eds., New York, NY, Oxford University Press
15. Burnaby TP. Growth-invariant discriminant functions and generalized distances. Biometrics 1966, 22:96-110.
16. Butler M, Losos J. Multivariate sexual dimorphism, sexual selection, and adaptation in Greater Antillean Anolis lizards. Ecological Monographs 2002, 72:541-559.
17. Carretero MA, Llorente GA. Morfometría en una comunidad de lacértidos mediterráneos, y su relación con la ecología. Historia Animalium 1993, 2:77-79.
18. Carretero MA, Ribeiro R, Barbosa D, Sá-Sousa P, Harris DJ. Spermatogenesis in two Iberian Podarcis lizards: relationships with male traits. Animal Biology 2006, 56:1-12.
19. Carretero MA, Sá-Sousa P, Barbosa D, Harris DJ, Pinho C. Sintopía estricta entre Podarcis bocagei y Podarcis carbonelli. Boletín de la Asociación Herpetológica Española 2002, 13:20-24.
20. Christian A, Garland T. Scaling of limb proportions in monitor lizards. Journal of Herpetology 1996, 30:219-230.
21. Cox RM, Skelly SL, John-Alder HB. A comparative test of adaptive hypotheses for sexual size dimorphism in lizards. Evolution 2005, 57:1653-1669.
22. Curran-Everett D. Multiple comparisons: philosophies and illustrations. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2000, 279:R1-R8.
23. D'Thompson AW. On growth and form 1917, London, Macmillan
24. Darwin C. The descent of man and selection in relation to sex 1874, New York, NY, Humboldt
25. Atlas do Ambiente 1995, Direcção Geral do Ambiente, Lisboa, Direcção Geral do Ambiente
26. Du W, Ji X, Shine R. Does body volume constrain reproductive output in lizards? Biology Letters 2005, 1:98-100.
27. Eble GJ. The macroevolution of phenotypic integration. The evolutionary biology of compex phenotypes 2003, 253-273. Pigliucci MPreston K. In, eds., Oxford, Oxford University Press
28. Elstrott J, Irschick DJ. Evolutionary correlations among morphology, habitat use and clinging performance in Caribbean Anolis lizards. Biological Journal of the Linnean Society 2004, 83:389-398.
29. Fairbairn DJ. Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics 1997, 28:659-687.
30. Falster DS, Warton DI, Wright IJ. SMATR: standardised major axis tests and routines. 2006, http://www.bio.mq.edu.au/ecology/SMATR/, Version 2.0. Available at:
31. Farley CT, Ko TC. Mechanics of locomotion in lizards. Journal of Experimental Biology 1997, 200:2177-2188.
32. Garland T, Hankins E, Huey RB. Locomotor capacity and social dominance in male lizards. Functional Ecology 1990, 4:243-250.
33. Harris DJ, Sá-Sousa P. Species distinction and relationships of the Western Iberian Podarcis lizards (Reptilia, Lacertidae) based on morphology and mitochondrial DNA sequences. Herpetological Journal 2001, 11:129-136.
34. Harris DJ, Sá-Sousa P. Molecular phylogenetics of Iberian Wall Lizards (Podarcis): is Podarcis hispanica a species complex? Molecular Phylogenetics and Evolution 2002, 23:75-81.
35. Herrel A, De Grauw E, Lemos-Espinal JA. Head shape and bite performance in xenosaurid lizards. Journal of Experimental Zoology 2001a, 290:101-107.
36. Herrel A, Meyers JJ, Vanhooydonck B. Relations between microhabitat use and limb shape in phrynosomatid lizards. Biological Journal of the Linnean Society 2002, 77:149-163.
37. Herrel A, Van Damme R, De Vree F. Sexual dimorphism of head size in Podarcis hispanica atrata: testing the dietary divergence hypothesis by bite force analysis. Netherlands Journal of Zoology 1996, 46:253-262.
38. Herrel A, Van Damme R, Vanhooydonck B, De Vree F. The implications of bite performance for diet in two species of lacertid lizards. Canadian Journal of Zoology 2001b, 79:662-670.
39. Hews DK. Size and scaling of sexually-selected traits in the lizard, Uta palmeri. Journal of Zoology 1996, 238:743-757.
40. Irschick DJ. Evolutionary approaches for studying functional morphology: examples from studies of performance capacity. Integrative and Comparative Biology 2002, 42:278-290.
41. Irschick DJ, Carlisle E, Elstrott J, Ramos M, Buckley C, Vanhooydonck B, Meyers J, Herrel A. A comparison of habitat use, morphology, clinging performance and escape behaviour among two divergent green anole lizard (Anolis carolinensis) populations. Biological Journal of the Linnean Society 2005, 85:223-234.
42. Irschick DJ, Jayne BC. Size matters: ontogenetic variation in the three-dimensional kinematics of steady-speed locomotion in the lizard Dipsosaurus dorsalis. Journal of Experimental Biology 2000, 203:2133-2148.
43. Jayne BC. Comparative morphology of the semispinalis-spinalis muscle of snakes and correlations with locomotion and constriction. Journal of Morphology 1982, 172:83-96.
44. Jayne BC. Muscular mechanisms of snake locomotion: an electromyographic study of the sidewinding and concertina modes of Crotalus cerastes, Nerodia fasciata and Elaphe obsoleta. Journal of Experimental Biology 1988a, 40:1-33.
45. Jayne BC. Muscular mechanisms of snake locomotion: an electromyographic study of lateral undulation of the florida banded water snake (Nerodia fasciata) and the yellow rat snake (Elaphe obsoleta). Journal of Morphology 1988b, 197:159-181.
46. Kaliontzopoulou A, Carretero MA, Llorente GA. Differences in the pholidotic patterns of Podarcis bocagei and P. carbonelli and implications for species determination. Revista Española de Herpetología 2005, 19:71-86.
47. Kaliontzopoulou A, Carretero MA, Llorente GA. Multivariate and geometric morphometrics in the analysis of sexual dimorphism variation in Podarcis lizards. Journal of Morphology 2007, 268:152-165.
48. Kaliontzopoulou A, Carretero MA, Llorente GA. Head shape allometry and proximate causes of head sexual dimorphism in Podarcis lizards: joining linear and geometric morphometrics. Biological Journal of the Linnean Society 2008a, 93:111-124.
49. Kaliontzopoulou A, Carretero MA, Llorente GA. Interspecific and intersexual variation in presacral vertebrae number in Podarcis bocagei and P. carbonelli. Amphibia-Reptilia 2008b, 29:288-292.
50. Klingenberg CP. Morphological integration and developmental modularity. Annual Review of Ecology, Evolution and Systematics 2008, 39:115-132.
51. López P, Martín J. Locomotor capacity and dominance in male lizards Lacerta monticola: a trade-off between survival and reproductive success? Biological Journal of the Linnean Society 2002, 77:201-209.
52. Losos JB. The evolution of form and function: morphology and locomotor performance in West Indian Anolis lizards. Evolution 1990a, 44:1189-1203.
53. Losos JB. Ecomorphology, performance capability and scaling of West Indian Anolis lizards: an evolutionary analysis. Ecological Monographs 1990b, 60:369-388.
54. McArdle BH. The structural relationship: regression in biology. Canadian Journal of Zoology 1988, 66:2329-2339.
55. Miles DB, Snell HL, Snell HM. Intrapopulation variation in endurance of Galápagos lava lizards (Microlophus albemarlensis): evidence for an interaction between natural and sexual selection. Ibid 2001, 3:795-804.
56. Mosimann JE. Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions. Journal of the American Statistical Association 1970, 65:930-945.
57. Olsson M, Shine R, Wapstra E, Ujvari B, Madsen T. Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection. Evolution 2002, 56:1538-1542.
58. Perry G, Levering K, Girard I, Garland T. Locomotor performance and social dominance in male Anolis cristatellus. Animal Behaviour 2004, 67:37-47.
59. Peterson CG, Husack JF. Locomotor performance and sexual selection: individual variation in sprint speed of collared lizards (Crotaphytus collaris). Copeia 2006, 2006: 2:216-224.
60. Pinho C, Ferrand N, Harris DJ. Reexamination of the Iberian and North African Podarcis (Squamata: Lacertidae) phylogeny based on increased mitochondrial DNA sequencing. Molecular Phylogenetics and Evolution 2006, 38:266-273.
61. Pinho C, Harris DJ, Ferrand N. Comparing patterns of nuclear and mitochondrial divergence in a cryptic species complex: the case of Iberian and North African wall lizards (Podarcis, Lacertidae). Biological Journal of the Linnean Society 2007, 91:121-133.
62. Ritter D. Lateral bending during lizard locomotion. Journal of Experimental Biology 1992, 173:1-10.
63. Robson MA, Miles DB. Locomotor performance and dominance in male Tree Lizards, Urosaurus ornatus. Functional Ecology 2000, 14:338-344.
64. Rohlf FJ, Bookstein FL. A comment on shearing as a method for 'size correction'. Systematic Zoology 1988, 36:356-367.
65. Russell AP, Bels V. Biomechanics and kinematics of limb-based locomotion in lizards: a review, synthesis and prospectus. Comparative Biochemistry and Physiology Part A 2001, 131:89-112.
66. Sá-Sousa P. A controversa sistemática das lagartixas do género Podarcis Wagler, 1830 (Sauria, Lacertidae) em Portugal. 2001a, PhD Thesis, University of Lisbon
67. Sá-Sousa P. Comparative chorology between Podarcis bocagei and P. carbonellae (Sauria: Lacertidae) in Portugal. Revista Española de Herpetología 2001b, 15:85-97.
68. Sá-Sousa P, Almeida AP, Rosa H, Vicente L, Crespo EG. Genetic and morphological relationships of the Berlenga wall lizard (Podarcis bocagei berlengensis: Lacertidae). Journal of Zoological Systematics and Evolutionary Research 2000, 38:95-102.
69. Sá-Sousa P, Harris DJ. Podarcis carbonelli Perez-Mellado, 1981 is a distinct species. Amphibia-Reptilia 2002, 23:459-468.
70. Schoener TW. The ecological significance of sexual dimorphism in size in the lizard Anolis conspersus. Science 1967, 155:474-477.
71. Schulte JA, Losos JB, Cruz FB, Núñez H. The relationship between morphology, escape behaviour and microhabitat occupation in the lizard clade Liolaemus (Iguanidae: Tropidurinae*: Liolaemini). Journal of Evolutionary Biology 2004, 17:408-420.
72. Shea BT. Developmental perspective on size change and allometry in evolution. Evolutionary Anthropology 1992, 1:125-134.
73. Shine R. Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Quarterly Review of Biology 1989, 64:419-461.
74. Shine R. Proximate determinants of sexual differences in adult body size. American Naturalist 1990, 135:278-283.
75. Slatkin M. Ecological causes of sexual dimorphism. Evolution 1984, 38:622-630.
76. Sokal RR, Rohlf FJ. Biometry: the principles and practice of statistics in biological research 1995, New York, NY, WH Freeman and Co
77. Sprent P. The mathematics of size and shape. Biometrics 1972, 28:23-37.
78. Stamps J. Sexual selection, sexual dimorphism and territoriality. Lizard ecology: studies of a model organism 1983, 169-204. Huey RBPianka ERSchoener TW. In, eds., Cambridge, MA, Harvard University Press
79. Stamps J. Sexual size dimorphism in species with asymptotic growth after maturity. Biological Journal of the Linnean Society 1993, 50:123-145.
80. Thompson GG, Withers PC. Comparative morphology of Western Australian varanid lizards (Squamata: Varanidae). Journal of Morphology 1997, 233:127-152.
81. Thompson GG, Withers PC. The relationship between size-free body shape and choice of retreat for Western Australian Ctenophorus (Agamidae) dragon lizards. Amphibia-Reptilia 2005, 26:65-72.
82. Toro E, Herrel A, Vanhooydonck B, Irschick DJ. A biomechanical analysis of intra- and interspecific scaling of jumping and morphology in Caribbean Anolis lizards. Journal of Experimental Biology 2003, 206:2641-2652.
83. Van Damme R, Vanhooydonck B. Speed versus manoeuvrability: association between vertebral number and habitat structure in lacertid lizards. Journal of Zoology, London 2002, 258:327-334.
84. Van Damme R, Vanhooydonck B, Aerts P, De Vree F. Evolution of lizard locomotion: context and constraint. Vertebrate biomechanics and evolution 2003, 267-282. Bels VL, Gasc JP, Casinos A, In, eds., Oxford, BIOS Scientific Publishers
85. Vanhooydonck B, Herrel A, Irschick DJ. Out of a limb: the differential effect of substrate diameter on acceleration capacity in Anolis lizards. Journal of Experimental Biology 2006, 209:4515-4523.
86. Vanhooydonck B, Herrel A, Irschick DJ. Determinants of sexual differences in escape behaviour in lizards of the genus Anolis: a comparative approach. Integrative and Comparative Biology 2007, 47:200-210.
87. Vincent SE, Herrel A. Functional and ecological correlates of ecologically-based dimorphisms in squamate reptiles. Integrative and Comparative Biology 2007, 47:172-188.
88. Warton DI, Wright IJ, Falster DS, Westoby M. Bivariate line-fitting methods for allometry. Biological Reviews 2006, 81:259-291.
89. Watkins GG. Proximate causes of sexual size dimorphism in the iguanian lizard Microlophus occipitalis. Ecology 1996, 77:1473-1482.