Effects of early thermal environment on the behavior and learning of a lizard with bimodal reproduction

Abstract: Early developmental temperatures influence the physiology and behavior of reptiles, with important consequences for their fitness and survival. For example, many viviparous lizards are cold adapted which may restrict their activity times during the reproductive season, increasing their susceptibility to global warming. However, it is unclear if and how lizards with different reproductive modes (oviparity vs. viviparity) can respond to rising temperatures by modifying their life-history traits. We examined the effect of developmental temperatures on hatchling behavior and learning in viviparous and oviparous populations of the lizard Saiphos equalis to test whether their reproductive behavior can buffer against rising temperatures. Gravid females from both populations were subjected to current or projected end-of-century (future) thermal environments to evaluate differences in the exploratory, foraging and antipredator behavior, and spatial learning ability of their offspring. We found that viviparous lizards were more exploratory and had a less-pronounced antipredator response than oviparous lizards. Regardless of the mode of reproduction, elevated temperatures reduced the exploratory behavior of hatchling lizards. Elevated temperatures also reduced the foraging efficiency of oviparous, but not viviparous, hatchlings. Finally, future-gestated oviparous hatchlings were more likely to choose the correct refuge and made fewer mistakes in a spatial learning task; however, we found only weak evidence of spatial learning in S. equalis. Our results suggest that although global warming is likely to have a negative impact on phenotypic traits, in S. equalis, some of these effects may be ameliorated by maternal behavior and/or physiological responses during pregnancy, particularly in viviparous populations. 

Significance statement: Computational modeling studies suggest that live-bearing lizards (viviparous) are more vulnerable to global warming compared with egg-laying ones (oviparous). However, there is little experimental evidence showing that viviparous species are indeed at a greater risk of extinction. Using a lizard species that has both oviparous and viviparous populations, we tested the effect of high developmental temperatures (projected for 2100) on the behavior and learning of their offspring. We found that elevated temperatures had a stronger negative effect on egg-laying lizards by producing hatchlings with lower foraging efficiency. Our results suggest that viviparous mothers can ameliorate some of the effects of global warming on their offspring. Moreover, our study suggests that if live bearers are indeed more vulnerable to global warming, it is likely not due to maladaptive behavior in offspring, but rather, to other causes that affect pregnant females.