Effects of gestation temperature on offspring sex and maternal reproduction in a viviparous lizard (Eremias multiocellata) living at high altitude

Journal of Thermal Biology

Volumn 37, Issue 6, 2012, Pages 438-444

  Tang, Xiao Long ^a   Yue, Feng ^a   Yan, Xue Feng ^a   Zhang, De Jiu ^a   Xin, Ying ^a   Wang, Cui ^a   Chen, Qiang ^a  

^a LANZHOU UNIVERSITY   (China)

Author keywords

Eremias multiocellata; Gestation temperature; Maternal reproduction; TSD; Viviparous lizard

Indexed keywords

ALTITUDE; ARTICLE; BODY MASS; BODY WEIGHT; CHINA; CONTROLLED STUDY; ENVIRONMENTAL TEMPERATURE; FEMALE; FEMALE ANIMAL; FERTILITY; GENDER BIAS; GEOGRAPHIC DISTRIBUTION; GESTATION PERIOD; GESTATIONAL TEMPERATURE; LITTER SIZE; LIZARD; MALE; NONHUMAN; PHENOTYPIC PLASTICITY; POPULATION RESEARCH; PROGENY; REPRODUCTION; SEX DETERMINATION PROCESS; SEX RATIO; TEMPERATURE; TEMPERATURE SENSITIVITY; VIVIPARITY; WEIGHT REDUCTION;

EREMIAS; REPTILIA; SQUAMATA; ZOOTOCA VIVIPARA;

EID: 84861331967     PISSN: 03064565     EISSN: 18790992     Source Type: Journal    
DOI: 10.1016/j.jtherbio.2012.03.002     Document Type: Article

References (60)

1. Angilletta M., Oufiero C.E., Leache' A.D. Direct and indirect effects of environmental temperature on the evolution of reproductive strategies: an information-theoretic approach. Am. Nat. 2006, 168:123-135.
2. Angilletta M.J., Niewiarowski P.H., Navas C.A. The evolution of thermal physiology in ectotherms. J. Therm. Biol. 2002, 27:249-268.
3. Aragón P., Lobo J.M., Olalla-Tárraga M.Á., Rodríguez M.Á. The Contribution of Contemporary Climate to Ectothermic and Endothermic Vertebrate Distributions in a Glacial Refuge 2010, Blackwell Publishing Ltd, pp. 40-49.
4. Ashton K.G. Are ecological and evolutionary rules being dismissed prematurely?. Diversity Distrib. 2001, 7:289-295.
5. Ashton K.G., Feldman C.R. Bergman's Rule in Nonavian Reptiles Turtles Follow it, Lizard and Snakes Reverse it 2003, Blackwell Publishing Ltd, pp. 1151-1163.
6. Beuchat C.A. Temperature effects during gestation in a viviparous lizard. J. Therm. Biol. 1988, 13:135-142.
7. Blanckenhorn W.U., Stillwell R.C., Young K.A., Fox C.W., Ashton K.G. When rensch meets bergmann: does sexual size dimorphism change systematically with latitude?. Evolution 2006, 60:2004-2011.
8. Booth D.T. Influence of incubation temperature on hatchling phenotype in reptiles. Physiol. Biochem. Zool. 2006, 79(2):274-281.
9. Bull J.J. Evolution of Sex Determining Mechanisms 1983, The Benjamin/Cummings Publishing Company, Inc.
10. ChamaillÉ-Jammes S., Massot M., AragÓ N P., Clobert J. Global Warming and Positive Fitness Response in Mountain Populations of Common Lizards Lacerta vivipara 2006, Blackwell Science Ltd, pp. 392-402.
11. Cooper W.E., Vitt L.J., Hedges R., Huey R.B. Locomotor impairment and defense in gravid lizards (Eumecesl aticeps): behaviourals hift in activitym ay offset costs of reproductionin an active forager. Behav. Ecol. Sociobiol. 1990, 27:153-157.
12. Deeming D.C., Ferguson M.W.J. Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles 2004, Cambridge University Press.
13. Du W.-G., Hu L.-J., Lu J.-L., Zhu L.-J. Effects of incubation temperature on embryonic development rate, sex ratio and post-hatching growth in the Chinese three-keeled pond turtle, Chinemys reevesii. Aquaculture 2007, 272:747-753.
14. Du W.-G., Shine R. The influence of hydric environments during egg incubation on embryonic heart rates and offspring phenotypes in a scincid lizard (Lampropholis guichenoti). Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2008, 151:102-107.
15. Du W.G., Feng J.H. Phenotypic effects of thermal mean and fluctuations on embryonic development and hatchling traits in a lacertid lizard, Takydromus septentrionalis. J. Exp. Zool. A: Ecol. Genet. Physiol. 2008, 309A:138-146.
16. Dunn P. Breeding dates and reproductive performance. Adv. Ecol. Res. 2004, 35:69-87.
17. Escobedo-Galván A.H., González-Salazar C., López-Alcaide S., Arroyo-Peña V.B., Martínez-Meyer E. Will all species with temperature-dependent sex determination respond the same way to climate change? A reply to Kallimanis (2010). Oikos 2011, 120:795-799.
18. Ferguson G.W., Fox S.F. Annual variation and survival advantage of large juvenile side-blotched lizards, Uta stansburiana: its causes and evolutionary significance. Evolution 1984, 38:342-349.
19. Gaston K.J., Blackburn T.M., Spicer J.I. Rapoport's rule: time for an epitaph?. Trends Ecol. Evol. 1998, 13:70-74.
20. Henrich S. Variation in offspring sizes of poeciliid fish Herandria formosa in relation to fitness. Oikos 1988, 51:13-18.
21. Huey R.B., Tewksbury J.J. Can behavior douse the fire of climate warming?. Proc. Natl. Acad. Sci. USA 2009, 106:3647-3648.
22. Janzen, J.F., 1994. Climate Change and Temperature-Dependent Sex Determination in Reptiles. Proceedings of the National Academy of Sciences 91, 7487-7490.
23. Ji X., Xie Y.-Y., Sun P.-Y., Zheng X.-Z. Sexual dimorphism and female reproduction in a viviparous snake, Elaphe rufodorsata. J. Herpetol. 1997, 31:420-422.
24. Ji X., Xu X.-F., Du W.-G. Female reproductive output and neonate characteristics in a viviparous water snake (Sinonatrix annularis). Acta Zool. Sinica 2001, 47:231-234.
25. Ji X., Lin L.H., Luo L.G., Lu H.L., Gao J.F., Han J. Gestation temperature affects sexual phenotype, morphology, locomotor performance, and growth of neonatal brown forest skinks, Sphenomorphus indicus. Biol. J. Linn. Soc. 2006, 88:453-463.
26. Kallimanis A.S. Temperature dependent sex determination and climate change. Oikos 2010, 119:197-200.
27. Li H., Qu Y.-F., Hu R.-B., Ji X. Evolution of viviparity in cold-climate lizards: testing the maternal manipulation hypothesis. Evol. Ecol. 2009, 23:777-790.
28. Li H., Qu Y.F., Ding G.H., Ji X. Life-history variation with respect to experienced thermal environments in the lizard, Eremias multiocellata (Lacertidae). Zool. Sci. 2011, 28:332-338.
29. Lin L.-H., Li H., An H., Ji X. Do temperature fluctuations during incubation always play an important role in shaping the phenotype of hatchling reptiles?. J. Therm. Biol. 2008, 33:193-199.
30. Lourdais O., Bonnet X., Doughty P. Costs of anorexia during pregnancy in a viviparous snake (Vipera aspis). J. Exp. Zool. 2002, 292:487-493.
31. Møller A.P. Protandry, sexual selection and climate change. Global Change Biol. 2004, 10:2028-2035.
32. Mathies T., Andrews R.M. Thermal and reproductive biology of high and low elevation populations of the lizard Sceloporus scalaris: implications for the evolution of viviparity. Oecologia 1995, 104:101-111.
33. Mayr E. Geographical character gradients and climatic adaptation. Evolution 1956, 10:105-108.
34. Parmesan C., Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 2003, 421:37-42.
35. McGinley M.A. The influence of a positive correlation between clutch size and offspring fitness on the optimal offspring size. Evol. Ecol. 1989, 3:150-156.
36. Patterson J., Davies P.M.C. The influence of temperature, sexual condition, and season on the metabolic rate of the lizard Psammodromus hispanicus. J. Comp. Physiol. B: Biochem., Syst., Environ. Physiol. 1984, 154:311-316.
37. Pen I., Uller T., Feldmeyer B., Harts A., While G.M., Wapstra E. Climate-driven population divergence in sex-determining systems. Nature 2010, 468:436-438.
38. Peters R.H. The Ecological Implications of Body Size 1986, Cambridge University Press.
39. Pulido F., Berthold P. Microevolutionary response to climatic change. Adv. Ecol. Res. 2004, 35:151-183.
40. Porter W.P., Tracy C.R. Biophysical analyses of energetics, time-space utilization, and distributional limits. Lizard Ecology: Studies of a Model Organism 1983, 55-83. Harvard University Press, Cambridge, MA. R.B. Huey, E.R. Pianka, T.W. Schoener (Eds.).
41. Post W. Advantages of coloniality in female boat-tailed Grackles. Wilson Bulletin 1998, 110:489-496.
42. Radder R.S., Pike D.A., Quinn A.E., Shine R. Offspring sex in a lizard depends on egg size. Curr. Biol. 2009, 19:1102-1105.
43. Radder R.S., Quinn A.E., Georges A., Sarre S.D., Shine R. Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol. Lett. 2007, 4:176-178.
44. Robert K.A., Thompson M.B. Sex determination: viviparous lizard selects sex of embryos. Nature 2001, 412:698-699.
45. Schwarzkopf L., Shine R. Costs of reproduction in lizards: escape tactics and susceptibility to predation. Behav. Ecol. Sociobiol. 1992, 31:17-25.
46. Shine R. Does viviparity evolve in cold climate reptiles because pregnant females maintain stable (not high) body temperatures?. Evolution 2004, 58:1809-1818.
47. Shine R., Harlow P. Maternal thermoregulation influences offspring viability in a viviparous lizard. Oecologia 1993, 96:122-127.
48. Shine R., Harlow P.S. Maternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizard. Ecology 1996, 77:1808-1817.
49. Sinervo B. The evolution of maternal investment in lizards: an experimental and comparative analysis of egg size and its effects on offspring performance. Evolution 1990, 44:279-294.
50. Sinervo B., Licht P. Hormonal and physiological control of clutch size, egg size, and egg shape in side©blotched lizards (Uta stansburiana): constraints on the evolution of lizard life histories. J. Exp. Zool. 1991, 257:252-264.
51. Thompson M.B., Seebacher F., Robert K.A. Facultative sex allocation in the viviparous lizard Eulamprus tympanum, a species with temperature-dependent sex determination. Aust. J. Zool. 2003, 51:367-370.
52. Valenzuela N., Adams C., Janzen F.J. Pattern does not equal process: exactly when is sex environmentally determined?. Am. Nat. 2003, 676-683.
53. Wapstra Erik, Uller Tobias, Sinn L.D., Olsson Mats, Mazurek Katrina, Joss Jean, Shine Richard Climate effects on offspring sex ratio in a viviparous lizard. J. Anim. Ecol. 2009, 78:84-90.
54. Wapstra E., Olsson M., Shine R., Edwards A., Swain R., Joss J.M.P. Maternal basking behaviour determines offspring sex in a viviparous reptile. Proc. R. Soc. London. Ser. B 2004, 271:230-232.
55. Warner D.A., Shine R. Reproducing lizards modify sex allocation in response to operational sex ratios. Biol. Lett. 2007, 3:47-50.
56. Witt M.J., Hawkes L.A., Godfrey M.H., Godley B.J., Broderick A.C. Predicting the impacts of climate change on a globally distributed species: the case of the loggerhead turtle. J. Exp. Biol. 2010, 213:901-911.
57. Xu D.-D., Ji X. Sexual dimorphism, female reproduction and egg incubation in the oriental leaf-toed gecko (Hemidactylus bowringii) from southern China. Zoology 2007, 110:20-27.
58. Yan X.F., Tang X.L., Yue F., Zhang D.J., Xin Y., Wang C., Chen Q. Influence of ambient temperature on maternal thermoregulation and neonate phenotypes in a viviparous lizard, Eremias multiocellata, during the gestation period. J. Therm. Biol. 2011, 36:187-192.
59. Zhang D.-J., Tang X.-L., Yue F., Chen Z., Li R.-D., Chen Q. Effect of gestation temperature on sexual and morphological phenotypes of offspring in a viviparous lizard, Eremias multiocellata. J. Therm. Biol. 2010, 35:129-133.
60. Zhao K.T. Lacertidae. Fauna Sinica, Reptilia 1999, 219-242. Science Press, Beijing, 2 (Squamata: Lacertilia). E.M. Zhao, K.T. Zhao, K.Y. Zhou (Eds.).