Evolution of viviparity in cold-climate lizards: Testing the maternal manipulation hypothesis

Evolutionary Ecology

Volumn 23, Issue 5, 2009, Pages 777-790

  Li, Hong ^a   Qu, Yan Fu ^a   Hu, Rui Bin ^a   Ji, Xiang ^a,b  

^a NANJING NORMAL UNIVERSITY   (China)

^b HANGZHOU NORMAL UNIVERSITY   (China)

Author keywords

Cold climate; Eremias prezwalskii; Growth; Lacertidae; Locomotor performance; Maternal basking; Morphology; Viviparity

Indexed keywords

CLIMATE CHANGE; EVOLUTION; EVOLUTIONARY BIOLOGY; FITNESS; LIZARD; LOCOMOTION; NEONATE; PHENOTYPE; PREGNANCY; THERMOREGULATION; VIVIPARITY;

ASIA; CHINA; EURASIA; FAR EAST; NEI MONGGOL;

ELAGATIS; EREMIAS; LACERTIDAE; REPTILIA; SQUAMATA;

EID: 70350717053     PISSN: 02697653     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10682-008-9272-2     Document Type: Article

References (60)

1. Alberts AC, Perry AM, Lemm JM, Phillips JA (1997) Effects of incubation temperature and water potential on growth and thermoregulatory behavior of hatchling Cuban rock iguanas (Cyclura nubila). Copeia 1997:766-776. doi:10.2307/1447294.
2. Andrews RM (2000) Evolution of viviparity in squamate reptiles (Sceloporus spp.): a variant of the cold-climate model. J Zool (Lond) 250:243-253. doi:10.1111/j.1469-7998.2000.tb01075.x.
3. Andrews RM, Rose BR (1994) Evolution of viviparity: constraints on egg retention. Physiol Zool 67:1006-1024.
4. Bauwens D, Garland T Jr, Castilla AM, van Damme R (1995) Evolution of sprint speed in lacertid lizards: morphological, physiological, and behavioral covariation. Evolution 49:848-863. doi:10.2307/2410408.
5. Beuchat CA (1988) Temperature effects during gestation in a viviparous lizard. J Therm Biol 13:135-142. doi:10.1016/0306-4565(88)90024-1.
6. Blackburn DG (1982) Evolutionary origins of viviparity in the Reptilia. I. Sauria. Amphib-reptil 3:185-205. doi:10.1163/156853882X00419.
7. Blackburn DG (1985) Evolutionary origins of viviparity in the Reptilia. II. Serpentes, Amphisbaenia, and Ichthyosauria. Amphib-Reptil 5:259-291. doi:10.1163/156853885X00290.
8. Blackburn DG (1999) Are viviparity and egg-guarding evolutionarily labile in squamates? Herpetologica 55:556-572.
9. Blackburn DG (2000) Reptilian viviparity: past research, future directions, and appropriate models. Comp Biochem Physiol A 127:391-409.
10. Braña F (1993) Shifts in body-temperature and escape behavior of female Podarcis muralis during pregnancy. Oikos 66:216-222. doi:10.2307/3544807.
11. Braña F, Ji X (2000) The influence of incubation temperature on morphology, locomotor performance, and early growth of hatchling wall lizards (Podarcis muralis). J Exp Zool 286:422-433. doi:10.1002/(SICI)1097-010X(20000301)286:4<422::AID-JEZ10>3.0.CO;2-D.
12. Brown RP, Griffin S (2005) Lower selected body temperatures after food deprivation in the lizard Anolis carolinensis. J Therm Biol 30:79-83. doi:10.1016/j.jtherbio.2004.07.005.
13. Charland MB (1995) Thermal consequences of reptilian viviparity: thermal regulation in gravid and nongravid snakes (Thamnophis). J Herpetol 29:383-390. doi:10.2307/1564988.
14. Charland MB, Gregory PT (1990) The influence of female reproductive status on thermoregulation in a viviparous, Crotalus viridis. Copeia 1990:1089-1098. doi:10.2307/1446493.
15. Daut EF, Andrews RM (1993) The effect of pregnancy on the thermoregulatory behavior of the viviparous lizard Calchides ocellatus. J Herpetol 27:6-13. doi:10.2307/1564898.
16. Deeming DC, Ferguson MWJ (1991) Physiological effects of temperature on embryonic development in reptiles and birds. In: Deeming DC, Ferguson MWJ (eds) Egg incubation: its effects on embryonic development in reptiles and birds. Cambridge University Press, Cambridge, pp 147-171.
17. Du WG, Ji X (2006) Effects of constant and fluctuating temperatures on egg survival and hatchling traits in the northern grass lizard (Takydromus septentrionalis, Lacertidae). J Exp Zool A 305:47-54. doi:10.1002/jez.a.243.
18. Duellman WE, Trueb L (1986) Biology of amphibians. McGraw-Hill, New York.
19. Galán P (1996) Sexual maturity in a population of the lacertid lizard Podarcis bocagei. Herpetol J 6:87-93.
20. Goodwin NB, Dulvy NK, Reynolds JD (2002) Life-history correlates of the evolution of live bearing in fishes. Philos Trans R Soc Lond B 357:259-267. doi:10.1098/rstb.2001.0958.
21. Hao QL, Liu HX, Ji X (2006) Phenotypic variation in hatchling Mongolian racerunners (Eremias argus) from eggs incubated at constant versus fluctuating temperatures. Acta Zool Sin 52:1049-1057.
22. Hodges WL (2004) Evolution of viviparity in horned lizards (Phrynosoma): testing the cold-climate hypothesis. J Evol Biol 17:1230-1237. doi:10.1111/j.1420-9101.2004.00770.x.
23. Ji X, Lin LH, Luo LG, Lu HL, Gao JF, Han J (2006) Gestation temperature affects sexual phenotype, morphology, locomotor performance and growth of neonatal brown forest skink, Sphenomorphus indicus. Biol J Linn Soc 88:453-463. doi:10.1111/j.1095-8312.2006.00633.x.
24. Ji X, Lin CX, Lin LH, Qiu QB, Du Y (2007) Evolution of viviparity in warm-climate lizards: an experimental test of the maternal manipulation hypothesis. J Evol Biol 20:1037-1045. doi:10.1111/j.1420-9101.2006.01296.x.
25. Lin CX, Du Y, Qiu QB, Ji X (2007) Relatively high but narrow incubation temperatures in lizards depositing eggs in warm and thermally stable nests. Acta Zool Sin 53:437-445.
26. Lin ZH, Ji X, Luo LG, Ma XM (2005) Incubation temperature affects hatching success, embryonic expenditure of energy and hatchling phenotypes of a prolonged egg-retaining snake, Deinagkistrodon acutus (Viperidae). J Therm Biol 30:289-297. doi:10.1016/j.jtherbio.2005.01.002.
27. Lutterschmidt WI, Hutchison VH (1997) The critical thermal maximum: history and critique. Can J Zool 75:1561-1574. doi:10.1139/z97-783.
28. Mathies T, Andrews RM (1997) Influence of pregnancy on thermal biology of the lizard, Sceloporus jarrovi: why do pregnant females exhibit low body temperatures? Funct Ecol 11:498-507. doi:10.1046/j.1365-2435.1997.00119.x.
29. Mell R (1929) Preliminary contributions to an ecology of East Asiatic reptiles, especially snakes. Lingnan Sci J 8:187-197.
30. Miles DB, Fitzgerald LA, Snell HL (1995) Morphological correlates of locomotor performance in hatchling Amblyrhynchus cristatus. Oecologia 103:261-264. doi:10.1007/BF00329089.
31. Olsson M, Shine R (1997) The limits to reproductive output: offspring size versus number in the sand lizard (Lacerta agilis). Am Nat 149:179-188. doi:10.1086/285985.
32. Qualls CP (1997) The effects of reproductive mode and climate on reproductive success in the Australian lizard, Lerista bougainvavillii. J Herpetol 31:60-65. doi:10.2307/1565329.
33. Qualls CP, Andrews RM (1999) Cold climates and the evolution of viviparity in reptiles: cold incubation temperatures produce poor-quality offspring in the lizard, Sceloporus virgatus. Biol J Linn Soc 67:353-376.
34. Qualls CP, Shine R (1998) Lerista bougainvavillii: a case study for the evolution of viviparity in reptiles. J Evol Biol 11:63-78. doi:10.1007/s000360050066.
35. Peterson CR, Gibson AR, Dorcas ME (1993) Snake thermal ecology: the causes and consequences of body-temperature variation. In: Seigel RA, Collins JT (eds) Snake: ecology and behavior. McGraw-Hill, New York, pp 241-314.
36. Reynolds JD, Goodwin NB, Freckleton RP (2002) Evolutionary transitions in parental care and live bearing in vertebrates. Philos Trans R Soc Lond B Biol Sci 357:269-281. doi:10.1098/rstb.2001.0930.
37. Rhen T, Lang JW (1995) Phenotypic plasticity for growth in the common snapping turtle: effects of incubation temperature, clutch, and their interaction. Am Nat 146:726-747. doi:10.1086/285822.
38. Rock J, Andrews RM, Cree A (2000) Effects of reproductive condition, season and site on selected temperatures of a viviparous gecko. Physiol Biochem Zool 73:344-355. doi:10.1086/316741.
39. Schwarzkopf L, Shine R (1991) Thermal biology of reproduction in viviparous skinks, Eulamprus tympanum: why do gravid females bask more? Oecologia 88:562-569.
40. Sergeev AM (1940) Researches in the viviparity of reptiles. Moscow Soc Nat JubileeIssue:1-34.
41. Shine R (1983) Reptilian viviparity in cold climates: testing the assumptions of an evolutionary hypothesis. Oecologia 57:397-405. doi:10.1007/BF00377186.
42. Shine R (1985) The evolution of viviparityin reptiles: an ecological analysis. In: Gans C, Billet F (eds) Biology of Reptilia, vol 15. Wiley, New York, pp 605-695.
43. Shine R (1987) The evolution of viviparity: ecological correlates of reproductive mode within a genus of Australian snakes (Pseudechis; Elapidae). Copeia 1987:551-563. doi:10.2307/1445650.
44. Shine R (1995) A new hypothesis for the evolution of viviparity in reptiles. Am Nat 145:809-823. doi:10.1086/285769.
45. Shine R (2002) An empirical test of the 'predictability' hypothesis for the evolution of viviparity in reptiles. J Evol Biol 15:553-560. doi:10.1046/j.1420-9101.2002.00420.x.
46. Shine R (2003) Locomotor speeds of gravid lizards: placing 'costs of reproduction' within an ecological context. Funct Ecol 17:526-533. doi:10.1046/j.1365-2435.2003.00756.x.
47. Shine R (2004) Does viviparity evolve in cold climate reptiles because pregnant females maintain stable (not high) body temperatures? Evolution 58:1809-1818.
48. Shine R (2005) Life-history evolution in reptiles. Annu Rev Ecol Evol Syst 36:23-46. doi:10.1146/annurev.ecolsys.36.102003.152631.
49. Shine R (2006) Is increased maternal basking an adaptation or a pre-adaptation to viviparity in lizards? J Exp Zool A 305:524-535. doi:10.1002/jez.a.291.
50. Shine R, Harlow PS (1993) Maternal manipulation influence offspring viability in a viviparous lizard. Oecologia 96:122-127. doi:10.1007/BF00318039.
51. Shine R, Harlow PS (1996) Maternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizard. Ecology 77:1808-1817. doi:10.2307/2265785.
52. Tinkle DW, Gibbons JW (1977) The distribution and evolution of viviparity in reptiles. Misc Publ Univ Mich Mus Zool 154:1-55.
53. van Damme R, Bauwens D, Verheyen RF (1986) Selected body temperatures in the lizard Lacerta vivipara: variation within and between populations. J Therm Biol 11:219-222. doi:10.1016/0306-4565(86)90006-9.
54. van Damme R, Bauwens D, Braña F, Verheyen RF (1992) Incubation temperature differentially affects hatching time, egg survival and sprint speed in the lizard Podarcis muralis. Herpetologica 48:220-228.
55. Wapstra E (2000) Maternal basking opportunity affects juvenile phenotype in a viviparous lizard. Funct Ecol 14:345-352. doi:10.1046/j.1365-2435.2000.00428.x.
56. Webb JK, Shine R, Christian KA (2006) The adaptive significance of reptilian viviparity in the tropics: testing the maternal manipulation hypothesis. Evolution 60:115-122.
57. Weekes HC (1933) On the distribution, habitat and reproductive habits of certain European and Australian snakes and lizards, with particular regard to their adoption of viviparity. Proc Linn Soc NSW 58:270-274.
58. Yang J, Sun YY, An H, Ji X (2008) Northern grass lizards (Takydromus septentrionalis) from different populations do not differ in thermal preference and thermal tolerance when acclimated under identical thermal conditions. J Comp Physiol B 178:343-349. doi:10.1007/s00360-007-0227-7.
59. Zhao KT (1999) Lacertidae. In: Zhao EM, Zhao KT, Zhou KY (eds) Fauna Sinica, Reptilia, vol 2. Science Press, Beijing, pp 219-242.
60. Zhao EM, Adler K (1993) Herpetology of China. Published by the Society of the Study of Amphibians and Reptiles, Oxford, OH.