Geographical differences in maternal basking behaviour and offspring growth rate in a climatically widespread viviparous reptile.

In reptiles, the thermal environment during embryonic development affects offspring phenotypic traits and potentially offspring fitness. In viviparous species, mothers can potentially manipulate the embryonic thermal environment through their basking behaviour and, thus, may be able to manipulate offspring phenotype and increase offspring fitness. One way in which mothers can maximise offspring phenotype (and thus potentially affect offspring fitness) is by fine-tuning their basking behaviour to the environment in order to buffer the embryo from deleterious developmental temperatures. In widespread species, it is unclear whether populations that have evolved under different climatic conditions will exhibit different maternal behaviours and/or thermal effects on offspring phenotype. To test this, we provided extended or reduced basking opportunity to gravid spotted skinks (Niveoscincus ocellatus) and their offspring from two populations at the climatic extremes of the species' distribution. Gravid females fine-tuned their basking behaviour to the basking opportunity, which allowed them to buffer their embryos from potentially negative thermal effects. This fine-tuning of female basking behaviour appears to have led to the expression of geographical differences in basking behaviour, with females from the cold alpine regions being more opportunistic in their basking behaviour than females from the warmer regions. However, those differences in maternal behaviour did not preclude the evolution of geographic differences in thermal effects: offspring growth varied between populations, potentially suggesting local adaptation to basking conditions. Our results demonstrate that maternal effects and phenotypic plasticity can play a significant role in allowing species to cope in changing environmental conditions, which is particularly relevant in the context of climate change.

Potentially adaptive effects of maternal nutrition during gestation on offspring phenotype of a viviparous reptile.

Viviparous reptiles have been used as model species for many studies that seek to explain the evolution of viviparity. The vast majority of such studies have focused on the advantage viviparity provides with regards to maternal control of embryonic developmental temperature. However, viviparity may also allow increased control of nutrient transfer, such that mothers adaptively manipulate offspring phenotype through varying maternal nutritional support. Because maternal nutritional transfer is temperature dependent, maternal nutritional strategies may vary between climatically distinct populations. In this study we used an orthogonal experimental design in which mothers and offspring from climatically distinct populations of a viviparous skink (Niveoscincus ocellatus) were allocated randomly to either a protein-rich or a protein-poor diet. Our results suggest that N. ocellatus mothers are able to compensate for sub-optimal nutritional conditions and can adaptively manipulate offspring phenotype to best fit the postnatal nutritional environment. Furthermore, maternal nutritional strategies appear to vary between climatically distinct populations. These results suggest that in viviparous reptiles, matrotrophy provides a means of producing an adaptive offspring phenotype, in addition to maternal control of developmental temperature.

Altitudinal divergence in maternal thermoregulatory behaviour may be driven by differences in selection on offspring survival in a viviparous lizard.

Plastic responses to temperature during embryonic development are common in ectotherms, but their evolutionary relevance is poorly understood. Using a combination of field and laboratory approaches, we demonstrate altitudinal divergence in the strength of effects of maternal thermal opportunity on offspring birth date and body mass in a live-bearing lizard (Niveoscincus ocellatus). Poor thermal opportunity decreased birth weight at low altitudes where selection on body mass was negligible. In contrast, there was no effect of maternal thermal opportunity on body mass at high altitudes where natural selection favored heavy offspring. The weaker effect of poor maternal thermal opportunity on offspring development at high altitude was accompanied by a more active thermoregulation and higher body temperature in highland females. This may suggest that passive effects of temperature on embryonic development have resulted in evolution of adaptive behavioral compensation for poor thermal opportunity at high altitudes, but that direct effects of maternal thermal environment are maintained at low altitudes because they are not selected against. More generally, we suggest that phenotypic effects of maternal thermal opportunity or incubation temperature in reptiles will most commonly reflect weak selection for canalization or selection on maternal strategies rather than adaptive plasticity to match postnatal environments.

Multi-scale approach to understanding climate effects on offspring size at birth and date of birth in a reptile.

Climate change is already impacting species around the world. Although most focus has been on the effect of temperature, changes in climatic variables other than temperature are also expected to drive biological change. Current models suggest that ectotherms, such as reptiles, will be strongly affected by climate change; however, data from natural populations are rare. Here, we use extensive data from 2 populations of a viviparous lizard (Niveoscincus ocellatus Gray, 1845) at the climatic extreme of the species distribution. We examine the effects of climate at a local, a regional and a global scale (thus, integrating a suite of variables at different spatial and temporal scales) on 2 key life history traits: offspring date of birth and size at birth. Overall, our results show that across 9 years of study, local temperature had strong effects on the offspring date of birth but not on the size at birth. Therefore, a rapid increase in local temperature throughout the species range (as predicted under global warming scenarios) is likely to affect phenological processes with potential concomitant effects on offspring fitness and survival.