The ecology and evolution of temperature-dependent reaction norms for sex determination in reptiles: a mechanistic conceptual model

Biological Reviews

Volumn 92, Issue 3, 2017, Pages 1348-1364

  Pezaro, Nadav ^a,b   Doody, J Sean ^c   Thompson, Michael B ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF HAIFA   (Israel)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Climate Adaptation; Climate Change; Developmental Plasticity; Developmental Switch Points; Environmental Threshold; Frequency Dependent Selection; Reaction Norms; Reptiles; Sex Ratios; Temperature Dependent sex determination

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; CLIMATE CHANGE; EVOLUTION; PHYLOGENY; PHYSIOLOGY; REPTILE; SEX DETERMINATION PROCESS; SEX RATIO; TEMPERATURE;

ANIMALS; BIOLOGICAL EVOLUTION; CLIMATE CHANGE; MODELS, BIOLOGICAL; PHYLOGENY; REPTILES; SEX DETERMINATION PROCESSES; SEX RATIO; TEMPERATURE;

EID: 84977533815     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/brv.12285     Document Type: Article

References (121)

1. Angilletta, M., Niewiarowski, P. & Navas, C. (2002). The evolution of thermal physiology in ectotherms. Journal of Thermal Biology 27, 249–268.
2. Boyle, M., Hone, J., Schwanz, L. E. & Georges, A. (2014). Under what conditions do climate-driven sex ratios enhance versus diminish population persistence? Ecology and Evolution 4, 4522–4533.
3. Bull, J. J. (1981). Evolution of environmental sex determination from genotypic sex determination. Heredity 47, 173–184.
4. Bull, J. J. (1983). Evolution of Sex Determining Mechanisms. Benjamin/Cummings, Menlo Park.
5. Bull, J. J. (1987). Temperature-sensitive periods of sex determination in a lizard: similarities with turtles and crocodilians. Journal of Experimental Zoology 241, 143–148.
6. Bull, C. M. (2000). Monogamy in lizards. Behavioural Processes 51, 7–20.
7. Bull, J. J., Vogt, R. C. & Bulmer, M. G. (1982a). Heritability of sex ratio in turtles with environmental sex determination. Evolution 36, 333–341.
8. Bull, J. J., Vogt, R. C. & McCoy, C. J. (1982b). Sex determining temperatures in turtles: a geographic comparison. Evolution 36, 326–332.
9. Bulmer, M. G. & Bull, J. J. (1982). Models of polygenic sex determination and sex-ratio control. Evolution 36, 13–26.
10. Burke, R.L. (1993). Adaptive value of sex determination mode and hatchling sex ratio bias in reptiles. Copeia 1993, 854–859.
11. Charnier, M. (1966). Action of temperature on sex-ratio in Agama agamas embryo (Agamidae Lacertilien). Societe de Biologie de L'Ouest African 160, 620–622.
12. Charnov, E. & Bull, J. (1977). When is sex environmentally determined? Nature 266, 828–830.
13. Conover, D. O. & Schultz, E. T. (1995). Phenotypic similarity and the evolutionary significance of countergradient variation. Trends in Ecology & Evolution 10, 248–252.
14. Conover, D. O. & Van Voorhees, D. A. (1990). Evolution of a balanced sex ratio by frequency-dependent selection in a fish. Science 250, 1556–1558.
15. Conover, D. O., Van Voorhees, D. A. & Ehtisham, A. (1992). Sex ratio selection and the evolution of environmental sex determination in laboratory populations of Menidia menidia. Evolution 46, 1722–1730.
16. Cox, R. M. & Kahrl, A. K. (2014). Sexual selection and sexual dimorphism. In Reproductive Biology and Phylogeny of Lizards and Tuatara (eds J. L. Rheubert, D. S. Siegel and S. E. Trauth), pp. 78–108. CRC Press, Boca Raton.
17. Crews, D., Bergeron, J. M., Bull, J. J., Flores, D., Tousignant, A., Skipper, J. K. & Wibbels, T. (1994). Temperature-dependent sex determination in reptiles: proximate mechanisms, ultimate outcomes, and practical applications. Developmental Genetics 15, 297–312.
18. Deeming, D. C. & Ferguson, M. W. J. (1989). The mechanism of temperature dependent sex determination in crocodilians: a hypothesis. American Zoologist 29, 973–985.
19. Deeming, D., Ferguson, M., Mittwoch, U., Wolf, U., Dorizzi, M., Zaborski, P. & Sharma, H. (1988). Environmental regulation of sex determination in reptiles [and discussion]. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 322, 19–39.
20. Doody, J. S. (2009). Superficial lizards in cold climates: nest site choice along an elevational gradient. Austral Ecology 34, 773–779.
21. Doody, J., Guarino, E., Georges, A., Corey, B., Murray, G. & Ewert, M. (2006). Nest site choice compensates for climate effects on sex ratios in a lizard with environmental sex determination. Evolutionary Ecology 20, 307–330.
22. Du, W. G., Warner, D. A., Langkilde, T., Robbins, T. & Shine, R. (2010). The physiological basis of geographic variation in rates of embryonic development within a widespread lizard species. The American Naturalist 176, 522–528.
23. Ewert, M.A. (1985). Embryology of turtles. In Biology of the Reptilia: Development B. (eds C. Gans, F. Billett & P. Maderson), pp. 75–268. Wiley, New York.
24. Ewert, M., Etchberger, C. & Nelson, C. (2004). Turtle sex-determining modes and TSD patterns, and some TSD pattern correlates. In Temperature-dependent Sex Determination in Vertebrates (eds N. Valenzuela and V. Lance), pp. 21–32. Smithsonian Institute, Washington.
25. Ewert, M. A., Jackson, D. R. & Nelson, C. E. (1994). Patterns of temperature-dependent sex determination in turtles. Journal of Experimental Zoology 270, 3–15.
26. Ewert, M. A., Lang, J. W. & Nelson, C. E. (2005). Geographic variation in the pattern of temperature-dependent sex determination in the American snapping turtle (Chelydra serpentina). Journal of Zoology 265, 81–95.
27. Ewert, M. A. & Nelson, C. E. (1991). Sex determination in turtles: diverse patterns and some possible adaptive values. Copeia 1, 50–69.
28. Falconer, D. S. (1960). Introduction to Quantitative Genetics. Oliver & Boyd, Edinburgh/London.
29. Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Oxford University Press, Oxford, UK.
30. Freedberg, S. & Taylor, D. R. (2007). Sex ratio variance and the maintenance of environmental sex determination. Journal of Evolutionary Biology 20, 213–220.
31. Girondot, M. (1999). Statistical description of temperature-dependent sex determination using maximum likelihood. Evolutionary Ecology Research 1, 479–486.
32. Girondot, M., Delmas, V., Rivalan, P., Courchamp, F., Prevot-Julliard, A. C. & Godfrey, M. H. (2004). Implications of temperature-dependent sex determination for population dynamics. In Temperature-dependent Sex Determination in Vertebrates (eds N. Valenzuela and V. Lance), pp. 148–155. Smithsonian Books, Washington.
33. Godfrey, M. H. & Mrosovsky, N. (2006). Pivotal temperature for green sea turtles, Chelonia mydas, nesting in Suriname. The Herpetological Journal 16, 55–61.
34. Graves, J. A. M. (2008). Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Annual Review of Genetics 42, 565–586.
35. Grigg, G. C., Beard, L. A. & Augee, M. L. (2004). The evolution of endothermy and its diversity in mammals and birds. Physiological and Biochemical Zoology 77, 982–997.
36. Harlow, P. S. & Taylor, J. E. (2000). Reproductive ecology of the jacky dragon (Amphibolurus muricatus): an agamid lizard with temperature-dependent sex determination. Austral Ecology 25, 640–652.
37. Hawkes, L. A., Broderick, A. C., Godfrey, M. H. & Godley, B. J. (2007). Investigating the potential impacts of climate change on a marine turtle population. Global Change Biology 13, 923–932.
38. Hazel, W. N., Smock, R. & Johnson, M. D. (1990). A polygenic model for the evolution and maintenance of conditional strategies. Proceedings of the Royal Society of London B: Biological Sciences 242, 181–187.
39. Hazel, W., Smock, R. & Lively, C. M. (2004). The ecological genetics of conditional strategies. The American Naturalist 163, 888–900.
40. Hoffman, A. A. & Parsons, P. A. (1997). Extreme Environmental Change and Evolution. Cambridge University Press, Cambridge.
41. Holleley, C. E., O'Meally, D., Sarre, S. D., Marshall Graves, J. A., Ezaz, T., Matsubara, K., Azad, B., Zhang, X. & Georges, A. (2015). Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature 523, 79–82.
42. Huey, R. B., Patridge, L. & Fowler, K. (1991). Thermal sensitivity of Drosophila melanogaster responds rapidly to laboratory natural selection. Evolution 45, 751–756.
43. Hulin, V., Delmas, V., Girondot, M., Godfrey, M. H. & Guillon, J.-M. (2009). Temperature-dependent sex determination and global change: are some species at greater risk? Oecologia 160, 493–506.
44. Iverson, J. B. (1991). Life history and demography of the yellow mud turtle, Kinosternon flavescens. Herpetologica 47, 373–395.
45. Izem, R. & Kingsolver, J. G. (2005). Variation in continuous reaction norms: quantifying directions of biological interest. The American Naturalist 166, 277–289.
46. Janzen, F. (1992). Heritable variation for sex-ratio under environmental sex determination in the common snapping turtle (Chelydra serpentina). Genetics 131, 155–161.
47. Janzen, F. (1994a). Climate change and temperature-dependent sex determination in reptiles. Proceedings of the National Academy of Sciences of the United States of America 91, 7487–7490.
48. Janzen, F. (1994b). Vegetational cover predicts the sex-ratio of hatchling turtles in natural nests. Ecology 75, 1593–1599.
49. Janzen, F. & Phillips, P. (2006). Exploring the evolution of environmental sex determination, especially in reptiles. Journal of Evolutionary Biology 19, 1775–1784.
50. Kearney, M. & Porter, W. P. (2004). Mapping the fundamental niche: physiology, climate, and the distribution of a nocturnal lizard. Ecology 85, 3119–3131.
51. Kingsolver, J. G. & Huey, R. B. (2003). Introduction: the evolution of morphology, performance, and fitness. American Zoologist 43, 361–366.
52. Kingsolver, J. G., Massie, K. R., Shlichta, J. G., Smith, M. H., Ragland, G. J. & Gomulkiewicz, R. (2007). Relating environmental variation to selection on reaction norms: an experimental test. The American Naturalist 169, 163–174.
53. Knies, J. L., Izem, R., Supler, K. L., Kingsolver, J. G. & Burch, C. L. (2006). The genetic basis of thermal reaction norm evolution in lab and natural phage populations. PLoS Biology 4, e201.
54. Lande, R. (2009). Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. Journal of Evolutionary Biology 22, 1435–1446.
55. Lang, J. W. & Andrews, H. V. (1994). Temperature-dependent sex determination in crocodilians. Journal of Experimental Zoology 270, 28–44.
56. Larsen, E. W. (2003). A view of phenotypic plasticity from molecules to morphogenesis. In Environment, Development and Evolution: Toward a Synthesis (eds B. K. Hall, R. Parsons and G. Muller), pp. 117–125. The MIT Press, Cambridge.
57. Lee, P. & Hays, G. (2004). Polyandry in a marine turtle: females make the best of a bad job. Proceedings of the National Academy of Sciences of the United States of America 101, 6530–6535.
58. Leimar, O., Van Dooren, T. J. M. & Hammerstein, P. (2004). Adaptation and constraint in the evolution of environmental sex determination. Journal of Theoretical Biology 227, 561–570.
59. Levins, R. (1969). Thermal acclimation and heat resistance in Drosophila species. The American Naturalist 103, 483–499.
60. Lindstrom, J. & Kokko, H. (1998). Sexual reproduction and population dynamics: the role of polygyny and demographic sex differences. Proceedings of the Royal Society of London B: Biological Sciences 265, 483–488.
61. Lynch, M. & Lande, R. (1993). Evolution and extinction in response to environmental change. In Biotic Interactions and Global Change (eds P. Kareiva, J. G. Kingsolver and R. B. Huey), pp. 234–250. Sinauer Associates Inc., Sunderland, Massachusetts.
62. Martin, T. L. & Huey, R. B. (2008). Why “suboptimal” is optimal: Jensen's inequality and ectotherm thermal preferences. American Naturalist 171, 102–118.
63. McGaugh, S. E., Bowden, R. M., Kuo, C.-H. & Janzen, F. J. (2011). Field-measured heritability of the threshold for sex determination in a turtle with temperature-dependent sex determination. Evolutionary Ecology Research 13, 75–90.
64. McGaugh, S. E. & Janzen, F. (2011). Effective heritability of targets of sex-ratio selection under environmental sex determination. Journal of Evolutionary Biology 24, 784–794.
65. Miller, K. A., Miller, H. C., Moore, J. A., Mitchell, N. J., Cree, A., Allendorf, F. W., Sarre, S. D., Keall, S. N. & Nelson, N. J. (2012). Securing the demographic and genetic future of tuatara through assisted colonization. Conservation Biology 26, 790–798.
66. Mitchell, N. J. & Janzen, F. (2010). Temperature-dependent sex determination and contemporary climate change. Sexual Development 4, 129–140.
67. Mitchell, N. J., Kearney, M. R., Nelson, N. J. & Porter, W. P. (2008). Predicting the fate of a living fossil: how will global warming affect sex determination and hatching phenology in tuatara? Proceedings of the Royal Society B: Biological Sciences 275, 2185–2193.
68. Mitchell, N. J., Nelson, N. J., Cree, A., Pledger, S., Keall, S. N. & Daugherty, C. H. (2006). Support for a rare pattern of temperature-dependent sex determination in archaic reptiles: evidence from two species of tuatara (Sphenodon). Frontiers in Zoology 3, 9.
69. Moore, J. A., Nelson, N. J., Keall, S. N. & Daugherty, C. H. (2007). Implications of social dominance and multiple paternity for the genetic diversity of a captive-bred reptile population (tuatara). Conservation Genetics 9, 1243–1251.
70. Morjan, C. L. (2003). Variation in nesting patterns affecting nest temperatures in two populations of painted turtles (Chrysemys picta) with temperature-dependent sex determination. Behavioral Ecology and Sociobiology 53, 254–261.
71. Mrosovsky, N. & Pieau, C. (1991). Transitional range of temperature, pivotal temperatures and thermosensitive stages for sex determination in reptiles. Amphibia-Reptilia 12, 169–179.
72. Muth, A. (1980). Physiological ecology of desert iguana (Dipsosaurus dorsalis) eggs temperature and water relations. Ecology 61, 1335–1343.
73. Nelson, N., Keall, S., Brown, D. & Daugherty, C. (2002a). Establishing a new wild population of tuatara (Sphenodon guntheri). Conservation Biology 16, 887–894.
74. Nelson, N. J., Keall, S. N., Pledger, S. & Daugherty, C. H. (2002b). Male-biased sex ratio in a small tuatara population. Journal of Biogeography 29, 633–640.
75. Olsson, M. & Shine, R. (1997). Advantages of multiple matings to females: a test of the infertility hypothesis using lizards. Evolution 51, 1684–1688.
76. Organ, C. L. & Janes, D. E. (2008). Evolution of sex chromosomes in Sauropsida. Integrative and Comparative Biology 48, 512–519.
77. Oufieroi, C. E. & Angilletta, M. J. (2006). Convergent evolution of embryonic growth and development in the eastern fence lizard (Sceloporus undulatus). Evolution 60, 1066–1075.
78. Parker, S. L. & Andrews, R. M. (2007). Incubation temperature and phenotypic traits of Sceloporus undulatus: implications for the northern limits of distribution. Oecologia 151, 218–231.
79. Pen, I., Uller, T., Feldmeyer, B., Harts, A., While, G. M. & Wapstra, E. (2010). Climate-driven population divergence in sex-determining systems. Nature 468, 436–438.
80. Pieau, C. (1996). Temperature variation and sex determination in reptiles. BioEssays 18, 19–26.
81. Porter, W. P., Sabo, J. L., Tracy, C. R., Reichman, O. J. & Ramankutty, N. (2002). Physiology on a landscape scale: plant-animal interactions. Integrative and Comparative Biology 42, 431–453.
82. Quinn, A. E., Georges, A., Sarre, S. D., Guarino, F., Ezaz, T. & Graves, J. A. M. (2007). Temperature sex reversal implies sex gene dosage in a reptile. Science 316, 411.
83. Quinn, A. E., Sarre, S. D., Ezaz, T., Marshall Graves, J. A. & Georges, A. (2011). Evolutionary transitions between mechanisms of sex determination in vertebrates. Biology Letters 7, 443–448.
84. Rage, J.-C. (1998). Latest Cretaceous extinctions and environmental sex determination in reptiles. Bulletin de la Societe Geologique de France 169, 479–483.
85. Rhen, T., Schroeder, A., Sakata, J. T., Huang, V. & Crews, D. (2010). Segregating variation for temperature-dependent sex determination in a lizard. Heredity 106, 649–660.
86. Roff, D. A. (1986). The evolution of wing dimorphism in insects. Evolution 40, 1009.
87. Roff, D. A. (1994a). Habitat persistence and the evolution of wing dimorphism in insects. American Naturalist 144, 772.
88. Roff, D. A. (1994b). The evolution of dimorphic traits: predicting the genetic correlation between environments. Genetics 136, 395–401.
89. Roff, D. (1996). The evolution of threshold traits in animals. Quarterly Review of Biology 71, 3–35.
90. Roff, D. A. (1998a). Evolution of threshold traits: the balance between directional selection, drift and mutation. Heredity 80, 25–32.
91. Roff, D. A. (1998b). The maintenance of phenotypic and genetic variation in threshold traits by frequency-dependent selection. Journal of Evolutionary Biology 11, 513–529.
92. Roff, D. A. (2011). Alternative strategies: the evolution of switch points. Current Biology 21, R285–R287.
93. Ruben, J. A. & Jones, T. D. (2000). Selective factors associated with the origin of fur and feathers. American Zoologist 40, 585–596.
94. Sander van Doorn, G. (2014). Patterns and mechanisms of evolutionary transitions between genetic sex-determining systems. Cold Spring Harbor Perspectives in Biology 6, a017681.
95. Sarre, S. D., Georges, A. & Quinn, A. (2004). The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. BioEssays 26, 639–645.
96. Schartl, M. (2004). Sex chromosome evolution in non-mammalian vertebrates. Current Opinion in Genetics & Development 14, 634–641.
97. Schlichting, C. D. & Pigliucci, M. (1998). Phenotypic Evolution: A Reaction Norm Perspective. Sinauer Associates, Sunderland, MA.
98. Schwanz, L. E. & Janzen, F. J. (2008). Climate change and temperature-dependent sex determination: can individual plasticity in nesting phenology prevent extreme sex ratios? Physiological and Biochemical Zoology 81, 826–834.
99. Shine, R. (1999). Why is sex determined by nest temperature in many reptiles? Trends in Ecology & Evolution 14, 186–189.
100. Silber, S., Geisler, J. H. & Bolortsetseg, M. (2011). Unexpected resilience of species with temperature-dependent sex determination at the Cretaceous-Palaeogene boundary. Biology Letters 7, 295–298.
101. Smith, A. M. A. (1987). The Sex and Survivorship of Embryos and Hatchlings of the Australian Freshwater Crocodile, Crocodylus johnstoni. Australian National University, Canberra.
102. Spencer, R. J. & Janzen, F. (2014). A novel hypothesis for the adaptive maintenance of environmental sex determination in a turtle. Proceedings of the Royal Society B: Biological Sciences 281, 20140831.
103. Thompson, M. B. (1990). Incubation of eggs of tuatara, Sphenodon punctatus. Journal of Zoology 222, 303–318.
104. Tomkins, J. L. & Hazel, W. (2007). The status of the conditional evolutionarily stable strategy. Trends in Ecology & Evolution 22, 522–528.
105. Trillmich, F. & Trillmich, K. (1984). The mating systems of pinnipeds and marine iguanas: convergent evolution of polygyny. Biological Journal of the Linnean Society 21, 209–216.
106. Valenzuela, N. (2004). Temperature-dependent sex determination. In Temperature-dependent Sex Determination in Vertebrates (eds N. Valenzuela and V. Lance), pp. 1–16. Smithsonian Books, Washington.
107. Valenzuela, N. & Lance, V. (2004). Temperature-dependent Sex Determination in Vertebrates. Smithsonian Books, Washington.
108. Van Dooren, T. J. M. & Leimar, O. (2003). The evolution of environmental and genetic sex determination in fluctuating environments. Evolution 57, 2667–2677.
109. Viets, B. E., Ewert, M. A., Talent, L. G. & Nelson, C. E. (1994). Sex-determining mechanisms in squamate reptiles. Journal of Experimental Zoology 270, 45–56.
110. Volff, J. N. & Schartl, M. (2001). Variability of genetic sex determination in poeciliid fishes. Genetica 111, 101–110.
111. Wapstra, E., Uller, T., Sinn, D. L., Olsson, M., Mazurek, K., Joss, J. & Shine, R. (2009). Climate effects on offspring sex ratio in a viviparous lizard. Journal of Animal Ecology 78, 84–90.
112. Webb, G., Manolis, C., Ottley, B. & Heyward, A. (1992). Crocodile management and research in the Northern Territory: 1990–1992. In Crocodiles. Proceedings of the 11th Working Meeting of the Crocodile Specialist Group of the Species Survival Commission of the IUCN- The World Conservation Union, pp. 233–276. IUCN/SSC Crocodile Specialist Group, Gland.
113. Wedekind, C. (2002). Manipulating sex ratios for conservation: short-term risks and long-term benefits. Animal Conservation 5, 13–20.
114. Weishampel, J. F., Bagley, D. A. & Ehrhart, L. M. (2004). Earlier nesting by loggerhead sea turtles following sea surface warming. Global Change Biology 10, 1424–1427.
115. West-Eberhard, M. J. (2003). Developmental Plasticity and Evolution. Oxford University Press, New York.
116. Wilbur, H. M. (1976). Density-dependent aspects of metamorphosis in Ambystoma and Rana sylvatica. Ecology 57, 1289.
117. Wilbur, H. M. (1977). Density-dependent aspects of growth and metamorphosis in Bufo americanus. Ecology 58, 196.
118. Yamahira, K. & Conover, D. O. (2003). Interpopulation variability in temperature-dependent sex determination of the tidewater silverside Menidia peninsulae. Copeia 2003, 155–159.
119. Yntema, C. L. & Mrosovsky, N. (1982). Critical periods and pivotal temperatures for sexual differentiation in loggerhead sea turtles. Canadian Journal of Zoology 60, 1012–1016.
120. Zamudio, K. R. & Sinervo, B. (2000). Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. Proceedings of the National Academy of Sciences of the United States of America 97, 14427–14432.
121. Zhang, F., Li, Y., Guo, Z. & Murray, B. R. (2009). Climate warming and reproduction in Chinese alligators. Animal Conservation 12, 128–137.