Shift in Thermal Preferences of Female Oviparous Common Lizards During Egg Retention: Insights into the Evolution of Reptilian Viviparity

Abstract

Pregnant female Zootoca vivipara select lower body temperatures than males or nonpregnant females, and this shift in the thermal preferendum is believed to be related to optimising the conditions for embryogenesis. Thus, subjecting embryos to the higher temperature selected by males and non-gravid females might have detrimental effects on embryonic development and on hatchling fitness, according to predictions of the ''maternal manipulation'' hypothesis on the evolution of viviparity. To test the role of gestation environment on embryonic development in oviparous Z. vivipara, we kept a number of gravid females at the temperature selected by non-gravid females in a laboratory thermal gradient, whereas control females were allowed to regulate their body temperature without restrictions. Developmental stage at oviposition was more advanced for embryos of the experimental clutches, which were heavier than those of the control group. Forced gestation temperature also affected hatching success (58.62% in the experimental treatment vs. 97.37% in the control group). In addition, hatchlings from females subjected to high temperatures during pregnancy were smaller, had shorter head length and performed worse in running trials. Our results fulfil the prediction of the ''maternal manipulation'' hypothesis, and suggest that the shift in female body temperature during pregnancy optimizes embryogenesis and hatchling phenotype by avoiding the negative effects of the high incubation temperatures preferred by non-gravid females.

Differential reproductive investment in co-occurring oviparous and viviparous common lizards (Zootoca vivipara) and implications for life-history trade-offs with viviparity

“…Particularly, the lower temperatures at higher altitudes have a negative effect on clutch development in oviparous females but can be mitigated by viviparous females (Shine 2002 ; Webb et al 2006 ). At the sampling site (> 1300 m), egg incubation time under natural conditions is not known but would be substantially longer than in our study (Rodríguez-Díaz and Braña 2011 , 2012 ). Further, hatching success for oviparous clutches was likely higher under our incubation conditions than under strictly natural settings.…”

Altitudinal variation in egg retention and rates of embryonic development in oviparous Zootoca vivipara fits predictions from the cold‐climate model on the evolution of viviparity

“…Change in thermal preferences of gravid females toward lower temperatures is probably linked to the maintenance of temperatures suitable for a successful embryonic development, in accordance with the maternal manipulation hypothesis. Therefore, this hypothesis is not incompatible with the cold‐climate hypothesis (see Rodríguez‐Díaz et al ., ), as the low temperatures selected by pregnant females would not entail an important increase in the potential incubation time (Rodríguez‐Díaz & Braña, ).…”

“…The maternal manipulation hypothesis (Shine, 1995;Webb et al, 2006) posits that egg retention evolves because females provide eggs with a more stable and warmer thermal environment than the external one, that is, with the optimum thermal environment for embryo development. Evidence on females changing their preferred body temperatures during pregnancy (Shine, 2006), as well as on incubation temperatures similar to those preferred by nonpregnant females having detrimental effects on embryonic development supports this hypothesis (Rodríguez-Díaz & Brañ a, 2011). On the other hand, the cold climate hypothesis (Shine, 1985(Shine, , 2002, which is not necessarily incompatible with the maternal manipulation hypothesis (Rodríguez-Díaz et al, 2010), posits that egg retention is favoured at high altitudes or latitudes, where environmental temperatures are much lower than female body temperatures.…”

Do gravid female Anolis nebulosus thermoregulate differently than males and non-gravid females?

“…Previous studies have found that the opportunity for gravid females to bask or otherwise thermoregulate can influence the timing of oviposition (e.g., Olsson and Shine, 1997;Shine, 2006;Telemeco et al, 2010). In addition, the temperatures at which gravid female lizards maintain themselves influence the development rate of eggs once laid, as well as their hatching success (e.g., Angilletta et al, 2000;Rodríguez-Díaz et al, 2010;Telemeco et al, 2010;Rodríguez-Díaz and Braña, 2011). Maternal thermoregulation also can affect the temperature regime (i.e., the distribution of temperatures experienced rather than the mean temperature) experienced by the eggs compared to the nest environment (e.g., Shine, 2004).…”