Evolution of thermal physiology in liolaemus lizards: Adaptation, phylogenetic inertia, and niche tracking

American Naturalist

Volumn 174, Issue 2, 2009, Pages 204-220

  Labra, Antonieta ^a   Pienaar, Jason ^b   Hansen, Thomas F ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

Adaptation; Bergmann's rule; Liolaemus; Niche tracking; Phylogenetic inertia; Thermobiology

Indexed keywords

ADAPTATION; BERGMANN RULE; CLIMATE EFFECT; CLIMATE VARIATION; COMPARATIVE STUDY; EVOLUTION; LIZARD; NICHE; PHYLOGENETICS; PHYLOGENY;

ADAPTATION; ANIMAL; ARTICLE; BODY SIZE; COMPARATIVE STUDY; EVOLUTION; FEMALE; HISTOLOGY; LIZARD; MALE; PHYLOGENY; PHYSIOLOGY; TEMPERATURE; THERMOREGULATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BODY SIZE; BODY TEMPERATURE REGULATION; EVOLUTION; FEMALE; LIZARDS; MALE; PHYLOGENY; TEMPERATURE;

LIOLAEMINAE; LIOLAEMUS; SQUAMATA;

EID: 70149106818     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/600088     Document Type: Article

References (113)

1. Andrews, R. M. 1998. Geographic variation in field body temperature of Sceloporus lizards. Journal of Thermal Biology 23:329-334.
2. Angilletta, M. J., P. H. Niewiarowski, and C. A. Navas. 2002. The evolution of thermal physiology in ectotherms. Journal of Thermal Biology 27:249-268.
3. Angilletta, M. J., A. F. Bennett, H. Guderley, C. A. Navas, F. Seebacher, and R. S. Wilson. 2006. Coadaptation: a unifying principle in evolutionary thermal biology. Physiological and Biochemical Zoology 79:282-294.
4. Ashton, K. G. 2004. Sensitivity of intraspecific latitudinal clines of body size for tetrapods to sampling, latitude and body size. Integrative and Comparative Biology 44:403-412.
5. Ashton, K. G., and C. R. Feldman. 2003. Bergmann's rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution 57:1151-1163.
6. Autumn, K., J. Jindrich, D. De Nardo, and D. Mueller. 1999. Locomotor performance at low temperature and the evolution of nocturnality in geckos. Evolution 53:580-599. (Pubitemid 29239730)
7. Autumn, K., M. J. Ryan, and D. B. Wake. 2002. Integrating historical and mechanistic biology enhances the study of adaptation. Quarterly Review of Biology 77:383-408. (Pubitemid 36080534)
8. Bakken, G. S., and D. M. Gates. 1975. Heat transfer analysis of animals: some implications from field ecology, physiology, and evolution. Pages 255-290 in D. M. Gates and R. B. Schmerl, eds. Perspectives in biophysical ecology. Springer, New York.
9. Bartholomew, G. A. 1982. Physiological control of body temperature. Pages 167-211 in C. Gans and F. H. Pough, eds. Biology of the Reptilia. Vol.12C. Physiological ecology. Academic Press, London.
10. Bauwens, D., T. Garland Jr., A. M. Castilla, and R. Van Damme. 1995. Evolution of sprint speed in lacertid lizards: morphological, physiological, and behavioral covariation. Evolution 49:848-863. (Pubitemid 3002807)
11. Bell, C. J. 1980. The scaling of the thermal inertia of lizards. Journal of Experimental Biology 86:79-85.
12. Bennett, A. F., and H. John-Alder. 1986. Thermal relations of some Australian skinks (Sauria: Scincidae). Copeia 1986:57-64.
13. Blomberg, S. P., and T. Garland Jr. 2002. Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. Journal of Evolutionary Biology 15:899-910.
14. Blomberg, S. P., T. Garland Jr., and A. R. Ives. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717-745.
15. Blouin-Demers, G., P. J. Weatherhead, and H. A. McCracken. 2003. A test of the thermal coadaptation hypothesis with black rat snakes (Elaphe obsoleta) and northern water snakes (Nerodia sipedon). Journal of Thermal Biology 28:331-340. (Pubitemid 36576133)
16. Blows, M. W., and A. A. Hoffmann. 2005. A reassessment of genetic limits to evolutionary change. Ecology 86:1371-1384.
17. Bogert, C. M. 1949. Thermoregulation in reptiles: a factor in evolution. Evolution 3:195-211.
18. Brattstrom, B. H. 1965. Body temperatures of reptiles. American Midland Naturalist 73:376-422.
19. Burnham, K. P., and D. R. Anderson. 1998. Model selection and inference: a practical information-theoretic approach. Springer, New York.
20. Butler, M. A., and A. A. King. 2004. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. American Naturalist 164:683-695.
21. Butler, M. A., T. W. Schoener, and J. B. Losos. 2000. The relationship between sexual size dimorphism and habitat use in greater Antillean Anolis lizards. Evolution 54:259-272. (Pubitemid 30186287)
22. Carothers, J. H., S. F. Fox, P. A. Marquet, and F. M. Jaksic. 1997. Thermal characteristics of ten Andean lizards of the genus Liolaemus in central Chile. Revista Chilena de Historia Natural 70: 297-309.
23. Carothers, J. H., P. A. Marquet, and F. M. Jaksic. 1998. Thermal ecology of a Liolaemus lizard assemblage along an Andean altitudinal gradient in Chile. Revista Chilena de Historia Natural 71: 39-50.
24. Cossins, A. R., and K. Bowler. 1987. Temperature biology of animals. Chapman & Hall, New York.
25. Cruz, F. B., L. A. Fitzgerald, R. E. Espinoza, and J. A. Schulte II. 2005. The importance of phylogenetic scale in tests of Bergmann's and Rapoport's rules: lessons from a clade of South American lizards. Journal of Evolutionary Biology 18:1559-1574.
26. Dawson, W. R. 1975. On the physiological significance of the preferred temperatures of reptiles. Pages 443-473 in D. M. Gates and R. B. Schmerl, eds. Perspectives in biophysical ecology. Springer, New York.
27. Díaz, J. A., D. Bauwens, and B. Asensio. 1996. A comparative study of the relation between heating rates and ambient temperatures in lacertid lizards. Physiological Zoology 69:1359-1383. (Pubitemid 27054032)
28. Diaz, J. A., P. Iraeta, and C. Monasterio. 2006. Seasonality provokes a shift of thermal preferences in a temperate lizard, but altitude does not. Journal of Thermal Biology 31:237-242.
29. di Castri, F., and E. R. Hajek. 1976. Bioclimatología de Chile. Vicerrectoria académica de la Universidad Católica de Chile, Santiago.
30. Doughty, P. 1994. Critical thermal minima of garter snakes (Thamnophis) depend on species and body size. Copeia 1994:537-540.
31. Dzialowski, E. M. 2005. Use of operative temperature and standard operative temperature models in thermal biology. Journal of Thermal Biology 30:317-334.
32. Eldredge, N., and S. J. Gould. 1972. Punctuated equilibria: an alternative to phyletic gradualism. Pages 82-115 in T. J. M. Schopf, ed. Models in paleobiology. Freeman, Cooper, San Francisco.
33. Eldredge, N., J. N. Thompson, P. M. Brakefield, S. Gavrilets, D. Jablonski, J. B. C. Jackson, R. E. Lenski, B. S. Lieberman, M. A. McPeek, and W. Miller III. 2005. The dynamics of evolutionary stasis. Paleobiology 31:133-145.
34. Espinoza, R. E., J. J. Wiens, and C. R. Tracy. 2004. Recurrent evolution of herbivory in small, cold-climate lizards: breaking the ecophysiological rules of reptilian herbivory. Proceedings of the National Academy of Sciences 101:16819-16824.
35. Estes, S., and S. J. Arnold. 2007. Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. American Naturalist 169:227-244. (Pubitemid 46184976)
36. Freckleton, R. P., P. H. Harvey, and M. Pagel. 2002. Phylogenetic analysis and comparative data: a test and review of evidence. American Naturalist 160:712-726.
37. Fuentes, E. R., and F. M. Jaksic. 1979. Activity temperature of eight Liolaemus (Iguanidae) species in central Chile. Copeia 1979:546-548.
38. Garland, T., Jr., R. B. Huey, and A. F. Bennett. 1991. Phylogeny and coadaptation of thermal physiology in lizards: a reanalysis. Evolution 45:1969-1975.
39. Garland, T., Jr., A. F. Bennett, and E. L. Rezende. 2005. Phylogenetic approaches in comparative physiology. Journal of Experimental Biology 208:3015-3035.
40. Gilchrist, G. W. 1995. Specialists and generalists in changing environments. 1. Fitness landscapes of thermal sensitivity. American Naturalist 146:252-270.
41. Gingerich, P. D. 2001. Rates of evolution on the time scale of the evolutionary process. Genetica 112/113:127-144. (Pubitemid 34119657)
42. Gvoždík, L., and A. M. Castilla. 2001. A comparative study of preferred body temperatures and critical thermal tolerance limits among populations of Zootoca vivipara (Squamata: Lacertidae) along an altitudinal gradient. Journal of Herpetology 35:486-492.
43. Hansen, T. F. 1997. Stabilizing selection and the comparative analysis of adaptation. Evolution 51:1341-1351. (Pubitemid 27491132)
44. Hansen, T. F., and D. Houle. 2004. Evolvability, stabilizing selection, and the problem of stasis. Pages 130-150 in M. Pigliucci and K. Preston, eds. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford University Press, Oxford.
45. Hansen, T. F., and S. H. Orzack. 2005. Assessing current adaptation and phylogenetic inertia as explanations of trait evolution: the need for controlled comparisons. Evolution 59:2063-2072.
46. Hansen, T. F., W. S. Armbruster, and L. Antonsen. 2000. Comparative analysis of character displacement and spatial adaptations as illustrated by the evolution of Dalechampia blossoms. American Naturalist 156(suppl.):S17-S34.
47. Hansen, T. F., J. Pienaar, and S. H. Orzack. 2008. A comparative method for studying adaptation to a randomly evolving environment. Evolution 62:1965-1977.
48. Hertz, P. E., R. B. Huey, and E. Nevo. 1983. Homage to Santa Anita: thermal sensitivity of sprint speed in agamid lizards. Evolution 37: 1075-1084.
49. Hitchcock, M. A., and L. D. McBrayer. 2006. Thermoregulation in nocturnal ectotherms: seasonal and intraspecific variation in the Mediterranean gecko (Hemidactylus turcicus). Journal of Herpetology 40:185-195.
50. Holt, R. D. 1996. Demographic constraints in evolution: towards unifying the evolutionary theories of senescence and niche conservativism. Evolutionary Ecology 10:1-11. (Pubitemid 3024382)
51. Holt, R. D., and M. S. Gaines. 1992. Analysis of adaptation in heterogeneous landscapes: implications for the evolution of fundamental niches. Evolutionary Ecology 6:433-447.
52. Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130:195-204.
53. -1998. How should we explain variation in the genetic variance of traits? Genetica 102/103:241-253.
54. Houle, D., B. Morikawa, and M. Lynch. 1996. Comparing mutational variabilities. Genetics 143:1467-1483.
55. Huang, S.-R, Y. Hsu, and M.-C. Tu. 2006. Thermal tolerance and altitudinal distribution of two Sphenomorphus lizards in Taiwan. Journal of Thermal Biology 31:378-385.
56. Huey, R. B. 1982. Temperature, physiology and the ecology of reptiles. Pages 25-91 in C. Gans and F. H. Pough, eds. Biology of the Reptilia. Vol.12C. Physiological ecology. Academic Press, London.
57. Huey, R. B., and A. F. Bennett. 1987. Phylogenetic studies of coadaptation: preferred temperatures versus optimal performance temperatures of lizards. Evolution 41:1098-1115.
58. Huey, R. B., and E. R. Pianka. 2007. Lizard thermal biology: do genders differ? American Naturalist 170:473-478.
59. Huey, R. B., and M. Slatkin. 1976. Cost and benefits of lizard thermoregulation. Quarterly Review of Biology 51:363-384.
60. Huey, R. B., P. E. Hertz, and B. Sinervo. 2003. Behavioral drive versus behavioral inertia in evolution: a null model approach. American Naturalist 161:357-366.
61. Hunt, G. 2007. The relative importance of directional change, random walks, and stasis in the evolution of fossil lineages. Proceedings of the National Academy of Sciences of the USA 104:18404-18408. (Pubitemid 350210709)
62. Ives, A. R., P. E. Midford, and T. Garland Jr. 2007. Within-species variation and measurement error in phylogenetic comparative methods. Systematic Biology 56:252-270.
63. James, F. C. 1970. Geographic size variation in birds and its relationship to climate. Ecology 51:365-390.
64. Kemp, T. S. 2006. The origin of mammalian endothermy: a paradigm for the evolution of complex biological structure. Zoological Journal of the Linnean Society 147:473-488.
65. -2007. The origin of higher taxa: macroevolutionary processes, and the case of the mammals. Acta Zoologica 88:3-22.
66. Knouft, J. H., J. B. Losos, R. E. Glor, and J. J. Kolbe. 2006. Phylogenetic analysis of the evolution of the niche in lizards of the Anolis sagrei group. Ecology 87:S29-S38.
67. Labra, A. 1998. Selected body temperatures of seven species of Chilean Liolaemus lizards. Revista Chilena de Historia Natural 71: 349-358.
68. Labra, A., and F. Bozinovic. 2002. Interplay between pregnancy and physiological thermoregulation in Liolaemus lizards. Ecoscience 9: 421-426.
69. Labra, A., and M. Rosenmann. 1994. Energy metabolism and water loss of Pristidactylus lizards. Comparative Biochemistry and Physiology A 109:369-376.
70. Labra, A., M. Soto-Gamboa, and F. Bozinovic. 2001. Behavioral and physiological thermoregulation of Atacama desert-dwelling Liolaemus lizards. Ecoscience 8:413-420. (Pubitemid 34034807)
71. Labra, A., M. A. Vidal, R. Solis, and M. Penna. 2008. Ecofisiología de reptiles. Pages 483-516 in M. A. Vidal and A. Labra, eds. Herpetología de Chile. Science, Santiago.
72. Lailvaux, S. P. 2007. Interactive effects of sex and temperature on locomotion in reptiles. Integrative and Comparative Biology 47: 189-199.
73. Lande, R. 1976. The maintenance of genetic variability by mutation in a polygenic character with linked loci. Genetical Research 26: 221-235.
74. -1979. Quantitative genetic analysis of multivariate evolution, applied to brain : body size allometry. Evolution 33:402-416.
75. Licht, P., W. Dawson, V. Shoemaker, and A. Main. 1966. Observations on the thermal relations of western Australian lizards. Copeia 1966: 97-110.
76. Lobo, F. 2001. A phylogenetic analysis of lizards of the Liolaemus chiliensis group (Iguania: Tropiduridae). Herpetological Journal 11: 137-150.
77. Losos, J. B. 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters 11:995-1003.
78. Losos, J. B., D. J. Irschick, and T. W. Schoener. 1994. Adaptation and constraint in the evolution of specialization of Bahamian Anolis lizards. Evolution 48:1786-1798.
79. Maddison, W. P., and D. R. Maddison. 2007. Mesquite: a modular system for evolutionary analysis. Version 2.0. http:// mesquiteproject.org.
80. Marquet, P. A., J. C. Ortiz, F. Bozinovic, and F. M. Jaksic. 1989. Ecological aspects of thermoregulation at high altitudes: the case of Andean Liolaemus lizards in northern Chile. Oecologia (Berlin) 81:16-20.
81. Martin, T. L., and R. B. Huey. 2008. Why "suboptimal" is optimal: Jensen's inequality and ectotherm thermal preferences. American Naturalist 171:E102-E118.
82. Martins, E. P., and T. F. Hansen. 1997. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. American Naturalist 149:646-667. (Pubitemid 27191149)
83. Martins, E. P., A. Labra, M. Halloy, and J. T. Thompson. 2004. Largescale patterns of signal evolution: an interspecific study of Liolaemus lizard headbob displays. Animal Behavior 68:453-463.
84. Morando, M., L. J. Avila, C. R. Turner, and J. W. Sites Jr. 2008. Phylogeography between valleys and mountains: the history of populations of Liolaemus koslowskyi (Squamata, Liolaemini). Zoologica Scripta 37:603-618.
85. Núñez, H. 1996. Autoecología comparada de dos especies de lagartijas de Chile central. Museo Nacional de Historia Natural de Chile Publicaciones Ocasionales 50:1-59.
86. Núñez, H., and M. A. Labra. 1985. Liolaemus curis, a new lizard from los Andes Range, central Chile. Copeia 1985:556-559.
87. Ord, T. J., and E. P. Martins. 2006. Tracing the origins of signal diversity in anole lizards: phylogenetic approaches to inferring the evolution of complex behaviour. Animal Behavior 71:1411-1429.
88. Orzack, S. H., and E. Sober. 2001. Adaptation, phylogenetic inertia, and the method of controlled comparisons. Pages 45-63 in S. H. Orzack and E. Sober, eds. Adaptationism and optimality. Cambridge University Press, New York.
89. Pincheira-Donoso, D., T. Tregenza, and D. J. Hodgson. 2007. Body size evolution in South American Liolaemus lizards of the boulengeri clade: a contrasting reassessment. Journal of Evolutionary Biology 20:2067-2071.
90. Pincheira-Donoso, D., D. J. Hodgson, and T. Tregenza. 2008. The evolution of body size under environmental gradients in ectotherms: why should Bergmann's rule apply to lizards? BMC Evolutionary Biology 8:68.
91. Price, T. 1997. Correlated evolution and independent contrasts. Philosophical Transactions of the Royal Society B: Biological Sciences 352:519-529.
92. Rogowitz, G. L. 1996. Evaluation of thermal acclimation and altitudinal variation of metabolism in a Neotropical lizard, Anolis gundlachi. Copeia 1996:535-542. (Pubitemid 26354953)
93. Row, J. R., and G. Blouin-Demers. 2006. Thermal quality influences effectiveness of thermoregulation, habitat use, and behaviour in milk snakes. Oecologia (Berlin) 148:1-11.
94. Sallaberry, M., H. Núñez, and J. Yáñez. 1982. Liolaemus hernani, nueva especie de Iguanidae de la zona central de Chile. Boletín del Museo Nacional de Historia Natural (Chile) 39:93-99.
95. Scheers, H., and R. Van Damme. 2002. Micro-scale differences in thermal habitat quality and a possible case of evolutionary flexibility in the thermal physiology of lacertid lizards. Oecologia (Berlin) 132:323-331. (Pubitemid 36059174)
96. Schulte, J. A., II, J. R. Macey, R. E. Espinoza, and A. Larson. 2000. Phylogenetic relationships in the iguanid lizard genus Liolaemus: multiple origins of viviparous reproduction and evidence for recurring Andean vicariance and dispersal. Biological Journal of the Linnean Society 69:75-102.
97. Schulte, J. A., II, J. B. Losos, F. B. Cruz, and H. Núñez. 2004. The relationship between morphology, escape behaviour and microhabitat occupation in the lizard clade Liolaemus (Iguanidae: Tropidurinae: Liolaemini). Journal of Evolutionary Biology 17:408-420.
98. Seebacher, F., and C. E. Franklin. 2005. Physiological mechanisms of thermoregulation in reptiles: a review. Journal of Comparative Physiology B 175:533-541. (Pubitemid 41677161)
99. Sepulveda, M., M. A. Vidal, J. M. Fariña, and P. Sabat. 2008. Seasonal and geographic variation in thermal biology of the lizard Microlophus atacamensis (Squamata: Tropiduridae). Journal of Thermal Biology 33:141-148.
100. Simpson, G. G. 1944. Tempo and mode in evolution. Columbia University Press, New York.
101. Spellerberg, I. F. 1972a. Temperature tolerances of southeast Australian reptiles examined in relation to reptile thermoregulatory behaviour and distribution. Oecologia (Berlin) 9:23-46.
102. -1972b. Thermal ecology of allopatric lizards (Sphenomor- phus) in southeast Australia. I. The environment and lizard critical temperatures. Oecologia (Berlin) 9:371-383.
103. -1972c. Thermal ecology of allopatric lizards (Sphenomor- phus) in southeast Australia. II. Physiological aspects of thermoregulation. Oecologia (Berlin) 9:385-398.
104. Stevenson, R. D. 1985. Body size and limits to the daily range of body-temperature in terrestrial ectotherms. American Naturalist 125:102-117.
105. Stuart-Fox, D., and A. Moussalli. 2007. Sex-specific ecomorphological variation and the evolution of sexual dimorphism in dwarf chameleons (Bradypodion spp.). Journal of Evolutionary Biology 20: 1073-1081. (Pubitemid 46663129)
106. Vidal, M. A., and A. Labra, eds. 2008. Herpetología de Chile. Springer Science, Santiago.
107. Vidal, M. A., J. C. Ortiz, and A. Labra. 2008. Intraspecific variation in a physiological thermoregulatory mechanism: the case of the lizard Liolaemus tenuis (Liolaeminae). Revista Chilena de Historia Natural 81:171-178.
108. Wagner, G. P., and K. Schwenk. 2000. Evolutionary stable configurations: functional integration and the evolution of phenotypic stability. Evolutionary Biology 31:155-217.
109. Wiens, J. J. 2004. Speciation and ecology revisited: phylogenetic niche conservativism and the origin of species. Evolution 58:193-197.
110. Wiens, J. J., and C. H. Graham. 2005. Niche conservativism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics 36:519-539.
111. Williams, G. C. 1992. Natural selection: domains, levels, and challenges. Oxford University Press, New York.
112. Witz, B. W. 2001. Aspects of the thermal biology of the six-lined racerunner, Cnemidophorus sexlineatus (Squamata: Teiidae) in west-central Florida. Journal of Thermal Biology 26:529-535.
113. Youssef, M. K., S. C. Adolph, and J. Q. Richmond. 2008. Evolutionary conserved thermal biology across continents: the North American lizard Plestiodon gilberti (Scincidae) compared to Asian Plestiodon. Journal of Thermal Biology 33:308-312.