Altitudinal Divergence in Maternal Thermoregulatory Behaviour May Be Driven by Differences in Selection on Offspring Survival in a Viviparous Lizard

Abstract

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. K E Y W O R D S :Life-history evolution, maternal effect, phenotypic plasticity, selection-natural.

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

“…Reasons for this variation between similar experiments even within the same species are further explored in Uller et al (Uller et al, 2011). Despite evidence for partial compensatory shifts in female thermoregulatory behaviour in the present experiment, females that had access to the short basking opportunity had longer gestation periods, suggesting that the physiological processes affecting gestation length are more thermally sensitive than those affecting offspring length and mass (Uller et al, 2011). In addition to female thermoregulatory compensation to proximate basking restrictions, pre-programming of offspring to future basking conditions through maternal manipulation and/or embryonic thermal acclimation could further shape offspring phenotype.…”

“…Hertz and Huey, 1981;Van Damme et al, 1990;Huey et al, 2003;Caley and Schwarzkopf, 2004) (but see Uller et al, 2011).…”

“…At one extreme of the species range, mountain populations experience restricted basking opportunities and short summers, while at the other extreme, coastal populations experience warm conditions with extended basking opportunities and long summers (Atkins et al, 2007;Wapstra et al, 2009;Cadby et al, 2010b;Pen et al, 2010;Uller et al, 2011). This difference in climate has resulted in considerable variation in life-history and reproductive traits between populations, reflecting a combination of phenotypic and genotypic responses to environmental variation (Wapstra et al, 1999;Melville and Swain, 2000;Wapstra et al, 2009;Cadby et al, 2010b;Wapstra et al, 2010;Pen et al, 2010;Uller et al, 2011). For example, females from cold, mountain areas are typically larger, take longer to reach maturity, and give birth 2-4 weeks later than those from warm, coastal areas Pen et al, 2010).…”

“…Maternal thermoregulation during gestation is thought to allow the maintenance of stable developmental temperatures (Shine, 1995) and/or to provide a buffer to embryos from unsuitable developmental temperatures (Kearney et al, 2009) as well as potentially provide fitness benefits to females through, for example, reduced basking length and the costs associated with reproduction (Schwarzkopf and Shine, 1991;Schwarzkopf and Andrews, 2012a;Schwarzkopf and Andrews, 2012b;Shine, 2012). Maternal manipulation of the offspring environment may also potentially allow females to 'pre-programme' offspring phenotype to better suit the environment the offspring will encounter (or be born into) (Marshall and Uller, 2007;Cadby et al, 2010a;Pen et al, 2010;Cadby et al, 2011;Uller et al, 2011). Maternal 'pre-programming' to future developmental temperatures could occur through maternal manipulation of offspring phenotype to fit the predicted environment and/or through embryonic acclimation to the thermal conditions experienced during development (Seebacher, 2005).…”

“…Typically, you would expect the former to prevent the latter as the adjustment of female basking behaviour to the basking opportunity buffers and reduces the impact of environmental differences between populations and, thus, prevents the evolution of population-specific thermal effects (e.g. Hertz and Huey, 1981;Van Damme et al, 1990;Huey et al, 2003;Caley and Schwarzkopf, 2004) (but see Uller et al, 2011).We used the viviparous spotted skink, Niveoscincus ocellatus (Gray 1845) as our model system. In this species, maternal basking opportunity affects offspring phenotypic traits such as date of birth and offspring size (Wapstra, 2000;Cadby et al, 2010b), with the potential for concomitant effects on offspring fitness (Atkins et al, 2007;Wapstra et al, 2010;Uller et al, 2011).…”