Turtle mating patterns buffer against disruptive effects of climate change

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1736, 2012, Pages 2122-2127

  Wright, Lucy I ^a   Stokes, Kimberley L ^a   Fuller, Wayne J ^b   Godley, Brendan J ^a   McGowan, Andrew ^a   Snape, Robin ^a,c   Tregenza, Tom ^a   Broderick, Annette C ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b EUROPEAN UNIVERSITY OF LEFKE   (Turkey)

^c SOCIETY FOR PROTECTION OF TURTLES   (Turkey)

Author keywords

Chelonia mydas; Climate change; Marine turtle; Sex ratio; mating patterns; Temperature dependent sex determination

Indexed keywords

CLIMATE CHANGE; EFFECTIVE POPULATION SIZE; ENDANGERED SPECIES; MARINE ECOSYSTEM; MATING SUCCESS; PARENT-OFFSPRING INTERACTION; REPRODUCTIVE STRATEGY; SATELLITE DATA; SEX DETERMINATION; SEX RATIO; SPECIES CONSERVATION; TRACKING; TURTLE;

EID: 84859947182     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2011.2285     Document Type: Article

References (57)

1. Janzen, F. J. 1994 Climate change and temperature-dependent sex determination in reptiles. Proc. Natl Acad. Sci. USA 91, 7487-7490. (doi:10.1073/pnas.91. 16.7487)
2. 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. J. Anim. Ecol. 78, 84-90. (doi:10.1111/j.1365-2656.2008.01470.x)
3. 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? Proc. R. Soc. B 275, 2185-2193. (doi:10.1098/rspb.2008.0438)
4. Hawkes, L. A., Broderick, A. C., Godfrey, M. H. & Godley, B. J. 2009 Climate change and marine turtles. Endang. Sp. Res. 7, 137-154. (doi:10.3354/esr00198)
5. Freedberg, S. & Bowne, D. R. 2006 Monitoring juveniles across years reveals non-Fisherian sex ratios in a reptile with environmental sex determination. Evol. Ecol. Res. 8, 1499-1510.
6. Fuentes, M. M. P. B., Hamann, M. & Limpus, C. J. 2010 Past, current and future thermal profiles of green turtle nesting grounds: implications from climate change. J. Exp. Mar. Biol. Ecol. 383, 56-64. (doi:10.1016/j. jembe.2009.11.003)
7. Witt, M. J., Hawkes, L. A., Godfrey, M. H., Godley, B. J. & Broderick, A. C. 2010 Predicting the impacts of climate change on a globally distributed species: The case of the loggerhead turtle. J. Exp. Biol. 213, 901-911. (doi:10.1242/ jeb.038133)
8. Frankham, R. 1995 Effective population-size adult-population size ratios in wildlife-a review. Genet. Res. 66, 95-107. (doi:10.1017/S0016672300034455)
9. Milner-Gulland, E. J., Bukreevea, O. M., Coulson, T., Lushchekina, A. A., Kholodova, M. V., Bekenov, A. B. & Grachev, I. A. 2003 Reproductive collapse in saiga antelope harems. Nature 422, 135. (doi:10.1038/422135a)
10. Morjan, C. L. 2003 How rapidly can maternal behavior affecting primary sex ratio evolve in a reptile with environmental sex determination? Am. Nat. 162, 205- 219. (doi:10.1086/376583)
11. Doody, J. S., Guarino, E., Corey, B., Murray, G., Ewert, M. & Georges, A. 2006 Nest site choice compensates for climate effects on sex ratios in a lizard with environmental sex determination. Evol. Ecol. 20, 307-330. (doi:10. 1007/s10682-006-0003-2)
12. Weishampel, J. F., Bagley, D. A. & Ehrhart, L. M. 2004 Earlier nesting by loggerhead sea turtles following sea surface warming. Global Change Biol. 10, 1424-1427. (doi:10.1111/j.1529-8817.2003.00817.x)
13. Weishampel, J. F., Bagley, D. A., Ehrhart, L. M. & Weishampel, A. C. 2010 Nesting phenologies of two sympatric sea turtle species related to sea surface temperatures. Endang. Sp. Res. 12, 41-47. (doi:10.3354/ esr00290)
14. Schwanz, L. E. & Janzen, F. J. 2008 Climate change and temperature-dependent sex determination: can individual plasticity in nesting phenology prevent extreme sex ratios? Physiol. Biochem. Zool. 81, 826-834. (doi:10. 1086/590220)
15. Janzen, F. J. & Paukstis, G. L. 1988 Environmental sex determination in reptiles. Nature 332, 790. (doi:10. 1038/332790a0)
16. 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). J. Zool. 265, 81-95. (doi:10.1017/S0952836904006120)
17. Braun-McNeill, J., Epperly, S. P., Owens, D. W., Avens, L. & Williams, E. 2007 Seasonal reliability of testosterone radioimmunoassay (RIA) for predicting sex ratios of juvenile loggerhead (Caretta caretta) turtles. Herpetologica 63, 275-284. (doi:10.1655/0018-0831(2007)63[275: SROTRR]2.0.CO;2)
18. Stabenau, E. K., Stanley, K. S. & Landry Jr, A. M. 1996 Sex ratios from stranded sea turtles on the upper Texas coast. J. Herpetol. 30, 427-430. (doi:10.2307/1565186)
19. Chaloupka, M. & Limpus, C. 2001 Trends in the abundance of sea turtles resident in southern Great Barrier Reef waters. Biol. Conserv. 102, 235-249. (doi:10.1016/ S0006-3207(01)00106-9)
20. Limpus, C. J. 1993 The green turtle, Chelonia mydas, in Queensland: breeding males in the southern Great Barrier Reef. Wild Res. 20, 513-523. (doi:10.1071/ WR9930513)
21. Sugg, D. W. & Chesser, R. K. 1994 Effective population sizes with multiple paternity. Genetics 137, 1147-1155.
22. Broderick, A. C., Glen, F., Godley, B. J. & Hays, G. C. 2002 Estimating the number of green and loggerhead turtles nesting annually in the Mediterranean. Oryx 36, 227-235. (doi:10.1017/S0030605302000431)
23. Broderick, A. C., Godley, B. J., Reece, S. & Downie, J. R. 2000 Incubation periods and sex ratios of green turtles: highly female biased hatchling production in the eastern Mediterranean. Mar. Ecol. Prog. Ser. 202, 273-281. (doi:10.3354/meps202273)
24. Casale, P., Gerosa, G. & Yerli, S. 2000 Female-biased primary sex ratio of the green turtle, Chelonia mydas, estimated through sand temperatures at Akyatan, Turkey. Zool. Middle East 20, 33-42.
25. Nicholls, J. A., Double, M. C., Rowell, D. M. & Magrath, D. 2000 The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). J. Avian Biol. 31, 165-176. (doi:10.1034/j.1600-048X. 2000.310208.x)
26. Dutton, P. H. & Frey, A. 2009 Characterization of polymorphic microsatellite markers for the green turtle (Chelonia mydas). Mol. Ecol. Res. 9, 354-356. (doi:10. 1111/j.1755-0998.2008.02443.x)
27. FitzSimmons, N. N., Moritz, C. & Moore, S. S. 1995 Conservation and dynamics of microsatellite loci over 300-million years of marine turtle evolution. Mol. Biol. Evol. 12, 432-440.
28. Kichler, K., Holder, M. T., Davis, S. K., Marquez, R. & Owens, D. W. 1999 Detection of multiple paternity in the Kemp's ridley sea turtle with limited sampling. Mol. Ecol. 8, 819-830. (doi:10.1046/j.1365-294X. 1999.00635.x)
29. Aggarwal, R. K., Velavan, T. P., Udaykumar, D., Hendre, P. S., Shanker, K., Choudhury, B. C. & Singh, L. 2004 Development and characterization of novel microsatellite markers from the olive ridley sea turtle (Lepidochelys olivacea). Mol. Ecol. Notes 4, 77-79. (doi:10.1046/j.1471-8286.2003.00574.x)
30. Monzon-Arguello, C., Munoz, J., Marco, A., Lopez-Jurado, L. F. & Rico, C. 2008 Twelve new polymorphic microsatellite markers from the loggerhead sea turtle (Caretta caretta) and cross-species amplification on other marine turtle species. Conserv. Genet. 9, 1045-1049. (doi:10.1007/s10592-007-9446-4)
31. Shamblin, B. M., Faircloth, B. C., Dodd, M. G., Bagley, D. A., Ehrhart, L. M., Dutton, P. H., Frey, A. & Nairn, C. J. 2009 Tetranucleotide markers from the loggerhead sea turtle (Caretta caretta) and their cross-amplification in other marine turtle species. Conserv. Genet. 10, 577-580. (doi:10.1007/s10592-008-9573-6)
32. Shamblin, B. M., Faircloth, B. C., Dodd, M. G., Wood-Jones, A., Castleberry, S. B., Carroll, J. P. & Nairn, C. J. 2007 Tetranucleotide microsatellites from the loggerhead sea turtle (Caretta caretta). Mol. Ecol. Notes 7, 784-787. (doi:10.1111/j.1471-8286.2007. 01701.x)
33. Marshall, T. C., Slate, J., Kruuk, L. E. B. & Pemberton, J. M. 1998 Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7, 639-655. (doi:10.1046/j.1365-294x.1998.00374.x)
34. Raymond, M. & Rousset, F. 1995 GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86, 248-249.
35. Neff, B. D. & Pitcher, T. E. 2002 Assessing the statistical power of genetic analyses to detect multiple mating in fishes. J. Fish Biol. 61, 739-750. (doi:10.1111/j.1095-8649.2002.tb00908.x)
36. Wang, J. & Santure, A. W. 2009 Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181, 1579-1594. (doi:10.1534/genetics.108. 100214)
37. Wang, J. 2004 Sibship reconstruction from genetic data with typing errors. Genetics 166, 1963-1979. (doi:10. 1534/genetics.166.4.1963)
38. Godley, B. J., Richardson, S., Broderick, A. C., Coyne, M. S., Glen, F. & Hays, G. C. 2002 Long-term satellite telemetry of the movements and habitat utilisation by green turtles in the Mediterranean. Ecography 25, 352- 362. (doi:10.1034/j.1600-0587.2002.250312.x)
39. Coyne, M. S. & Godley, B. J. 2005 Satellite Tracking and Analysis Tool (STAT): an integrated system for archiving, analyzing and mapping animal tracking data. Mar. Ecol. Prog. Ser. 301, 1-7. (doi:10.3354/meps301001)
40. Verhoeven, K. J. F., Simonsen, K. L. & McIntyre, L. M. 2005 Implementing false discovery rate control: increasing your power. Oikos 108, 643-647. (doi:10.1111/j. 0030-1299.2005.13727.x)
41. Kasparek, M., Godley, B. J. & Broderick, A. C. 2001 Nesting of the green turtle, Chelonia mydas, in the Mediterranean: a review of status and conservation needs. Zool. Middle East 24, 45-74.
42. Canbolat, A. 2004 A review of sea turtle nesting activity along the Mediterranean coast of Turkey. Biol. Conserv. 116, 81-91. (doi:10.1016/S0006-3207(03)00179-4)
43. Rees, A., Saad, A. & Jony, M. 2008 Discovery of a regionally important green turtle Chelonia mydas rookery in Syria. Oryx 42, 456-459. (doi:10.1017/S003060530 8000926)
44. Emlen, S. T. & Oring, L. W. 1977 Ecology, sexual selection, and evolution of mating systems. Science 197, 215-223. (doi:10.1126/science.327542)
45. Clutton-Brock, T. H. & Vincent, A. C. J. 1991 Sexual selection and the potential reproductive rates of males and females. Nature 351, 58-60. (doi:10.1038/351058a0)
46. Hays, G. C., Fossette, S., Katselidis, K.A., Schofield, G. & Gravenor, M. B. 2010 Breeding periodicity for male sea turtles, operational sex ratios, and implications in the face of climate change. Conserv. Biol. 24, 1636-1643. (doi:10.1111/j.1523-1739.2010.01531.x)
47. Bell, C. D., Blumenthal, J. M., Broderick, A. C. & Godley, B. J. 2010 Investigating potential for depensation in marine turtles: how low can you go? Conserv. Biol. 24, 226-235. (doi:10.1111/j.1523-1739.2009.01313.x)
48. Pearse, D. E., Janzen, F. J. & Avise, J. C. 2002 Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature. Behav. Ecol. Sociobiol. 51, 164-171. (doi:10. 1007/s00265-001-0421-7)
49. Bowen, B. W. & Karl, S. A. 2007 Population genetics and phylogeography of sea turtles. Mol. Ecol. 16, 4886-4907. (doi:10.1111/j.1365-294X.2007.03542.x)
50. FitzSimmons, N. N., Moritz, C., Limpus, C. J., Pope, L. & Prince, R. 1997 Geographic structure of mitochondrial and nuclear gene polymorphisms in Australian green turtle populations and male-biased gene flow. Genetics 147, 1843-1854.
51. Broderick, A. C. & Godley, B. J. 1997 Observations of reproductive behaviour of male green turtles (Chelonia mydas) at a nesting beach in Cyprus. Chelonian Conserv. Biol. 2, 615-616.
52. Broderick, A. C., Coyne, M. S., Fuller, W. J., Glen, F. & Godley, B. J. 2007 Fidelity and over-wintering of sea turtles. Proc. R. Soc. B 274, 1533-1538. (doi:10.1098/ rspb.2007.0211)
53. Lohmann, K. J., Luschi, P. & Hays, G. C. 2008 Goal navigation and island-finding in sea turtles. J. Exp. Mar. Biol. Ecol. 356, 83-95. (doi:10.1016/j.jembe.2007.12.017)
54. Godley, B. J., Broderick, A. C., Frauenstein, R., Glen, F. & Hays, G. C. 2002 Reproductive seasonality and sexual dimorphism in green turtles. Mar. Ecol. Prog. Ser. 226, 125-133. (doi:10.3354/meps226125)
55. Lee, P. L. M. 2008 Molecular ecology of marine turtles: New approaches and future directions. J. Exp. Mar. Biol. Ecol. 356, 25-42. (doi:10.1016/j.jembe.2007.12.021)
56. Karl, S. A. 2008 The effect of multiple paternity on the genetically effective size of a population. Mol. Ecol. 17, 3973-3977. (doi:10.1111/j.1365-294X.2008.03902.x)
57. Heppell, S. S., Snover, M. L. & Crowder, L. B. 2003 Sea turtle population ecology. In The biology of sea turtles, vol. 2 (eds P. L. Lutz, J. A. Musick & J. Wyneken), pp. 275-306. Boca Raton, FL: CRC Press.