Genetic variation underlies temperature tolerance of embryos in the sea urchin Heliocidaris erythrogramma armigera

Journal of Evolutionary Biology

Volumn 26, Issue 10, 2013, Pages 2271-2282

  Lymbery, R A ^a   Evans, J P ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Broadcast spawning; Climate change; Evolvability; Genetic compatibility; Genetic variation; Phenotypic plasticity

Indexed keywords

ADAPTATION; COVARIANCE ANALYSIS; ENVIRONMENTAL RESPONSE; GENETIC ALGORITHM; GENETIC VARIATION; HERITABILITY; INVERTEBRATE; LIFE HISTORY TRAIT; TEMPERATURE TOLERANCE;

ECHINOIDEA; HELIOCIDARIS; HELIOCIDARIS ERYTHROGRAMMA;

ADAPTATION; ANIMAL; ANIMAL EMBRYO; ARTICLE; BROADCAST SPAWNING; CLIMATE CHANGE; EMBRYO DEVELOPMENT; EVOLVABILITY; FEMALE; FERTILIZATION; GENETIC COMPATIBILITY; GENETIC VARIABILITY; GENETICS; HELIOCIDARIS; MALE; PHENOTYPE; PHENOTYPIC PLASTICITY; PHYSIOLOGY; PRENATAL DEVELOPMENT; TEMPERATURE;

BROADCAST SPAWNING; CLIMATE CHANGE; EVOLVABILITY; GENETIC COMPATIBILITY; GENETIC VARIATION; PHENOTYPIC PLASTICITY;

ADAPTATION, BIOLOGICAL; ANIMALS; ANTHOCIDARIS; CLIMATE CHANGE; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION; MALE; PHENOTYPE; TEMPERATURE;

EID: 84883787960     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12225     Document Type: Article

References (103)

1. Agresti, A. 2002. Categorical Data Analysis, 2nd edn. John Wiley & Sons, Inc., New York, NY.
2. Auld, J.R., Agrawal, A.A. & Relyea, R.A. 2010. Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc. R. Soc. Lond. B 277: 503-511.
3. Balanya, J., Oller, J.M., Huey, R.B., Gilchrist, G.W. & Serra, L. 2006. Global genetic change tracks global climate warming in Drosophila subobscura. Science 313: 1773-1775.
4. Bijlsma, R., Bundgaard, J. & van Putten, W.F. 1999. Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J. Evol. Biol. 12: 1125-1137.
5. Binks, R.M. 2011. Investigating the evolutionary significance of morphological variation in the Australian sea urchin Heliocidaris erythrogramma. PhD Thesis, School of Animal Biology, Vol. PhD. University of Western Australia, Perth, WA.
6. Binks, R.M., Evans, J.P., Prince, J. & Kennington, W.J. 2011. Fine-scale patterns of genetic divergence within and between morphologically variable subspecies of the sea urchin Heliocidaris erythrogramma (Echinometridae). Biol. J. Linn. Soc. 103: 578-592.
7. Blows, M.W. & Hoffmann, A.A. 2005. A reassessment of genetic limits to evolutionary change. Ecology 86: 1371-1384.
8. Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H. et al. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24: 127-135.
9. Bradshaw, W.E. & Holzapfel, C.M. 2001. Genetic shifts in photoperiodic response correlated with global warming. Proc. Natl. Acad. Sci. USA 98: 14509-14511.
10. Bradshaw, W.E. & Holzapfel, C.M. 2008. Genetic response to rapid climate change: it's seasonal timing that matters. Mol. Ecol. 17: 157-166.
11. Brown, J.L., Li, S.-H. & Bhagabati, N. 1999. Long-term trend toward earlier breeding in an American bird: a response to global warming? Proc. Natl. Acad. Sci. USA 96: 5565-5569.
12. Byrne, M., Ho, M., Selvakumaraswamy, P., Nguyen, H.D., Dworjanyn, S.A. & Davis, A.R. 2009. Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proc. R. Soc. Lond. B 276: 1883-1888.
13. Byrne, M., Selvakumaraswamy, P., Ho, M.A., Woolsey, E. & Nguyen, H.D. 2011. Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules. Deep Sea Res. Part II Top. Stud. Oceanogr. 58: 712-719.
14. Carlson, S.M. & Seamons, T.R. 2008. A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change. Evol. Appl. 1: 222-238.
15. Charmantier, A. & Garant, D. 2005. Environmental quality and evolutionary potential: lessons from wild populations. Proc. R. Soc. Lond. B 272: 1415-1425.
16. Comstock, R.E. & Robinson, H.F. 1948. The components of variance in populations of biparental progenies and their use in estimating the average degree of dominance. Biometrics 4: 254-266.
17. Conner, J.K. & Hartl, D.L. 2004. A Primer of Ecological Genetics. Sinauer Associates, Sunderland, MA.
18. Crick, H.P.Q., Dudley, C., Glue, D.E. & Thomson, D.L. 1997. UK birds are laying eggs earlier. Nature 388: 526.
19. DeWitt, T.J., Sih, A. & Wilson, D.S. 1998. Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13: 77-81.
20. Dziminski, M.A., Roberts, J.D. & Simmons, L.W. 2008. Fitness consequences of parental compatibility in the frog Crinia georgiana. Evolution 62: 879-886.
21. Eads, A.R., Mitchell, N.J. & Evans, J.P. 2012. Patterns of genetic variation in dessication tolerance in embryos of the terrestrial-breeding frog Pseudophryne guentheri. Evolution 66: 2865-2877.
22. Ebert, T.A. 1982. Longevity, life history, and relative body wall size in sea urchins. Ecol. Monogr. 52: 353-394.
23. Etterson, J.R. & Shaw, R.G. 2001. Constraint to adaptive evolution in response to global warming. Science 294: 151-154.
24. Evans, J.P. & Marshall, D.J. 2005. Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59: 106-112.
25. Evans, J.P. & Sherman, C.D.H. 2013 Sexual selection and the evolution of egg-sperm interactions in broadcast spawning invertebrates. Biol. Bull., in press.
26. Evans, J.P., García-González, F. & Marshall, D.J. 2007. Sources of genetic and phenotypic variance in fertilization rates and larval traits in a sea urchin. Evolution 61: 2832-2838.
27. Evans, M.L., Neff, B.D. & Heath, D.D. 2010. Quantitative genetic and translocation experiments reveal genotype-by-environment effects on juvenile life-history traits in two populations of Chinook salmon (Oncorhynchus tshawytscha). J. Evol. Biol. 23: 687-698.
28. Falconer, D.S. & Mackay, T.F.C. 1996. Introduction to Quantitative Genetics, 4th edn. Longman, New York, NY.
29. Feng, M., Weller, E. & Hill, K. 2009. The Leeuwin Current. In: A Marine Climate Change Impacts and Adaptation Report Card for Australia 2009 (E.S. Poloczanska, A.J. Hobday & A.J. Richardson, eds), National Climate Change Adaptation Research Facility, Hobart. URL http://www.oceanclimatechange.org.au.
30. Foo, S.A., Dworjanyn, S.A., Poore, A.G.B. & Byrne, M. 2012. Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and ocean acidification: performance of early embryos. PLoS ONE 7: e42497.
31. Gienapp, P., Teplitsky, C., Alho, J.S., Mills, J.A. & Merilä, J. 2008. Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 17: 167-178.
32. Gosling, E. 2003. Bivalve Molluscs: Biology, Ecology and Culture. Fishing News Books, Oxford.
33. Gosselin, L.A. & Qian, P.-Y. 1997. Juvenile mortality in benthic marine invertebrates. Mar. Ecol. Prog. Ser. 146: 265-282.
34. Hallsson, L.R. & Björklund, M. 2012. Sex-specific genetic variances in life-history and morphological traits of the seed beetle Callosobruchus maculatus. Ecol. Evol. 2: 128-138.
35. Hansen, M.M., Olivieri, I., Waller, D.M. & Nielsen, E.E. 2012. Monitoring adaptive genetic responses to environmental change. Mol. Ecol. 21: 1311-1329.
36. Hill, W.G. & Caballero, A. 1992. Artificial selection experiments. Annu. Rev. Ecol. Syst. 23: 287-310.
37. Hoffmann, A.A. & Merilä, J. 1999. Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol. Evol. 14: 96-101.
38. Hoffmann, A.A. & Parsons, P.A. 1989. An integrated approach to environmental stress tolerance and life-history variation: dessication tolerance in Drosophila. Biol. J. Linn. Soc. 37: 117-136.
39. Hoffmann, A.A. & Sgrò, C.M. 2011. Climate change and evolutionary adaptation. Nature 470: 479-485.
40. Hoffmann, A.A., Hallas, R.J., Dean, J.A. & Schiffer, M. 2003. Low potential for climatic stress adaptation in a rainforest Drosophila species. Science 301: 100-102.
41. Huey, R.B., Patridge, L. & Fowler, K. 1991. Thermal sensitivity of Drosophila melanogaster responds rapidly to laboratory natural selection. Evolution 45: 751-756.
42. Huggett, M.J., King, C.K., Williamson, J.E. & Steinberg, P.D. 2005. Larval development and metamorphosis of the Australian diadematid sea urchin Centrostephanus rodgersii. Invertebr. Reprod. Dev. 47: 197-204.
43. Ivy, T.M. 2007. Good genes, genetic compatibility and the evolution of polyandry: use of the diallel cross to address competing hypotheses. J. Evol. Biol. 20: 479-487.
44. Joubert, D. & Bijlsma, R. 2010. Interplay between habitat fragmentation and climate change: inbreeding affects the response to thermal stress in Drosophila melanogaster. Clim. Res. 43: 57-70.
45. Keesing, J.K. 2001. The ecology of Heliocidaris erythrogramma. In: Edible Sea Urchins: Biology and Ecology (M.J. Lawrence, ed.), pp. 261-270. Elsevier, Amsterdam.
46. Kellermann, V.M., van Heerwaarden, B., Hoffmann, A.A. & Sgrò, C.M. 2006. Very low additive genetic variance and evolutionary potential in multiple populations of two rainforest Drosophila species. Evolution 60: 1104-1108.
47. Kellermann, V.M., van Heerwaarden, B., Sgrò, C.M. & Hoffmann, A.A. 2009. Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science 325: 1244-1246.
48. Kelly, M.W., Sanford, E. & Grosberg, R.K. 2012. Limited potential for adaptation to climate change in a broadly distributed marine crustacean. Proc. R. Soc. Lond. B 279: 349-356.
49. Kinlan, B.P. & Gaines, S.D. 2003. Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84: 2007-2020.
50. Koike, S. & Higuchi, H. 2002. Long-term trends in the egg-laying date and clutch size of red-cheeked Starlings Sturnia philippensis. Ibis 144: 150-152.
51. Laurila, A., Karttunen, S. & Merilä, J. 2002. Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations. Evolution 56: 617-627.
52. Levitan, D.R. & Ferrell, D.L. 2006. Selection on gamete recognition proteins depends on sex, density, and genotype frequency. Science 312: 267-269.
53. Ling, S.D., Johnson, C.R., Ridgway, K., Hobday, A.J. & Haddon, M. 2009. Climate-driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics. Glob. Change Biol. 15: 719-731.
54. Ling, S.D., Ibbott, S. & Sanderson, J.C. 2010. Recovery of canopy-forming macroalgae following removal of the enigmatic grazing sea urchin Heliocidaris erythrogramma. J. Exp. Mar. Biol. Ecol. 395: 135-146.
55. Lough, J.M. 2009. Temperature. In: A Marine Climate Change Impacts and Adaptation Report Card for Australia 2009 (E.S. Poloczanska, A.J. Hobday & A.J. Richardson, eds), National Climate Change Adaptation Research Facility, Hobart. URL http://www.oceanclimatechange.org.au.
56. Lynch, M. & Walsh, B. 1998. Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, MA.
57. Marshall, D.J., Styan, C.A. & Keough, M.J. 2000. Intraspecific co-variation between egg and body size affects fertilisation kinetics of free-spawning marine invertebrates. Mar. Ecol. Prog. Ser. 195: 305-309.
58. McMillan, W.O., Raff, R.A. & Palumbi, S.R. 1992. Population genetic consequences of developmental evolution in sea urchins (Genus Heliocidaris). Evolution 46: 1299-1312.
59. Merilä, J. 2012. Evolution in response to climate change: in pursuit of the missing evidence. BioEssays 34: 811-818.
60. Meyer, E., Davies, S., Wang, S., Willis, B.L., Abrego, D., Juenger, T.E. et al. 2009. Genetic variation in responses to a settlement cue and elevated temperature in the reef-building coral Acropora millepora. Mar. Ecol. Prog. Ser. 392: 81-92.
61. Miller, P.S. 1994. Is inbreeding depression more severe in a stressful environment? Zoo Biol. 13: 195-208.
62. Møller, A., Flensted-Jensen, E. & Mardal, W. 2006. Rapidly advancing laying date in a seabird and the changing advantage of early reproduction. J. Anim. Ecol. 75: 657-665.
63. Mousseau, T.A. & Fox, C.J. 1998. Maternal Effects as Adaptations. Oxford University Press, New York, NY.
64. Nakagawa, S. & Schielzeth, H. 2010. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. 85: 935-956.
65. Nussey, D.H., Postma, E., Gienapp, P. & Visser, M.E. 2005. Selection on heritable phenotypic plasticity in a wild bird population. Science 310: 304-306.
66. Nystrand, M., Dowling, D.K. & Simmons, L.W. 2011. Complex genotype by environment interactions and changing genetic architectures across thermal environments in the Australian field cricket, Teleogryllus oceanicus. BMC Evol. Biol. 11: 222.
67. Oreskes, N. 2004. The scientific consensus on climate change. Science 306: 1686.
68. Palumbi, S.R. 1999. All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc. Natl. Acad. Sci. USA 96: 12632-12637.
69. Palumbi, S.R. & Metz, E.C. 1991. Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol. Biol. Evol. 8: 227-239.
70. Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37: 637-669.
71. Parmesan, C., Ryrholm, N., Stefanescu, C., Hill, J.K., Thomas, C.D., Descimon, H. et al. 1999. Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399: 579-583.
72. Pearce, A., Lenanton, R., Jackson, G., Moore, J., Feng, M. & Gaughan, D. 2011. The "Marine Heat Wave" off Western Australia During the Summer of 2010/11. Department of Fisheries, Perth, WA.
73. Perry, A.L., Low, P.J., Ellis, J.R. & Reynolds, J.D. 2005. Climate change and distribution shifts in marine fishes. Science 308: 1912-1915.
74. Pespeni, M.H., Sanford, E., Gaylord, B., Hill, T.M., Hosfelt, J.D., Jaris, H.K. et al. 2013. Evolutionary change during ocean acidification. Proc. Natl. Acad. Sci. USA 110: 6937-6942.
75. Pigliucci, M. 2001. Phenotypic Plasticity: Beyond Nature and Nurture. John Hopkins University Press, Baltimore, MD.
76. Pigliucci, M. 2005. Evolution of phenotypic plasticity: where are we going now? Trends Ecol. Evol. 20: 481-486.
77. Pimm, S.L. & Raven, P. 2000. Extinction by numbers. Nature 403: 843-845.
78. Pistevos, J.C.A., Calosi, P., Widdicombe, S. & Bishop, J.D.D. 2011. Will variation among genetic individuals influence species responses to global climate change? Oikos 120: 675-689.
79. Pitcher, T.E. & Neff, B.D. 2007. Genetic quality and offspring performance in Chinook salmon: implications for supportive breeding. Conserv. Genet. 8: 607-616.
80. Przybylo, R., Sheldon, B.C. & Merilä, J. 2000. Climatic effects on breeding and morphology: evidence for phenotypic plasticity. J. Anim. Ecol. 69: 395-403.
81. Quinn, G.P. & Keough, M.J. 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.
82. R Development Core Team. 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org.
83. Raudenbush, S.W., Yang, M.L. & Yosef, M. 2000. Maximum likelihood for generalized linear models with nested random effects via high-order, multivariate Laplace approximation. J. Comput. Graph. Stat. 9: 141-157.
84. Relyea, R.A. 2002. Costs of phenotypic plasticity. Am. Nat. 159: 272-282.
85. Rosenzweig, C., Karoly, D., Vicarelli, M., Neofotis, P., Wu, Q., Casassa, G. et al. 2008. Attributing physical and biological impacts to anthropogenic climate change. Nature 435: 353-357.
86. Scheiner, S.M. 1993. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24: 35-68.
87. Scheiner, S.M. 2002. Selection experiments and the study of phenotypic plasticity. J. Evol. Biol. 15: 889-898.
88. Scheiner, S.M. & Goodnight, C.J. 1984. The comparison of phenotypic plasticity and genetic variation in populations of the grass Danthonia spicata. Evolution 38: 845-855.
89. Snell-Rood, E.C., Van Dyken, J.D., Cruickshank, T., Wade, M.J. & Moczek, A.P. 2010. Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity. BioEssays 32: 71-81.
90. Solomon, S.D., Qin, M., Manning, R.B., Chen, Z., Marquis, M., Averyt, K.B. et al. 2007. Technical summary. In: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis & K.B. Averyt, M. Tignor & H.L. Miller, eds), pp. 19-91. Cambridge University Press, Cambridge, UK.
91. Teplitsky, C., Mouawad, N.G., Balbontin, J., de Lope, F. & Moller, A.P. 2011. Quantitative genetics of migration syndromes: a study of two barn swallow populations. J. Evol. Biol. 24: 2025-2039.
92. Thomas, C.D. & Lennon, J.J. 1999. Birds extend their ranges northward. Nature 399: 213.
93. Tregenza, T. & Wedell, N. 2000. Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9: 1013-1027.
94. Vacquier, V.D. & Moy, G.W. 1977. Isolation of bindin: the protein responsible for adhesion of sperm to sea urchin eggs. Proc. Natl. Acad. Sci. USA 74: 2456-2460.
95. Vacquier, V.D., Swanson, W.J. & Hellberg, M.E. 1995. What have we learned about sea urchin sperm bindin? Dev. Growth Differ. 37: 1-10.
96. Vanderklift, M.A., Kendrick, G.A. & Smit, A.J. 2006. Differences in trophic position among sympatric sea urchin species. Estuar. Coast. Shelf Sci. 66: 291-297.
97. Via, S., Gomulklewicz, R., De Jong, G., Scheiner, S.M., Schlichting, C.D. & van Tienderen, P.H. 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. Evol. 10: 212-217.
98. Visser, M.E. 2008. Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc. R. Soc. Lond. B 275: 649-659.
99. Wernberg, T., Smale, D.A., Tuya, F., Thomsen, M.S., Langlois, T.J., de Bettignies, T. et al. 2012. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Change 3: 78-82.
100. Williams, D.H.C. & Anderson, D.T. 1975. The reproductive system, embryonic development, larval development and metamorphosis of the sea urchin Heliocidaris erythrogramma (Val.) (Echinoidea: Echinometridae). Aust. J. Zool. 23: 371-403.
101. Zeh, J.A. & Zeh, D.W. 1996. The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc. R. Soc. Lond. B 263: 1711-1717.
102. Zigler, K.S. 2008. The evolution of sea urchin sperm binding. Int. J. Dev. Biol. 52: 791-796.
103. Zigler, K.S., Raff, E.C., Popodi, E., Raff, R.A. & Lessios, H.A. 2003. Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57: 2293-2302.