Published On: Thu, Apr 18th, 2019

Higher incubation temperatures produce long-lasting upward shifts in cold tolerance, but not heat tolerance, of hatchling geckos [RESEARCH ARTICLE]

DISCUSSION

Developmental plasticity coupled with short-term heat hardening could potentially buffer lizards from the effects of summer heatwaves. In this study, we subjected developing embryos of the velvet gecko to thermal profiles that mimicked temperatures of currently used natural nests (current incubation treatment), and temperatures likely to occur during summer heatwaves in 2050 (hot incubation treatment). We found that hot-incubated hatchlings had significantly higher CTmax than current-incubated hatchlings, demonstrating that exposure to higher developmental temperatures shifted thermal tolerance upwards. This finding agrees with results from studies on Drosophila which found that flies reared at higher temperatures had higher heat tolerance than flies reared at lower temperatures (van Heerwaarden et al., 2016; Hoffmann et al., 2003; Slotsbo et al., 2016). However, in the Drosophila studies, developmental plasticity resulted in increases in heat tolerance of up to 1°C. By contrast, developmental shifts in heat tolerance in velvet geckos were small, and thus may confer little benefit to individuals.

Nonetheless, 6-week-old geckos exhibited clear heat hardening responses 4 h after exposure to high temperatures, with some individuals increasing their heat tolerance by up to 1.8°C (Fig. 2). Current-incubated geckos had significantly higher hardening capacity (mean=0.79±0.09°C) than hot-incubated geckos (mean=0.47±0.04°C). To date, few studies have measured heat hardening in lizards (Llewelyn et al., 2018; Phillips et al., 2016). In the tropical sun skink Lampropholis coggeri, the average hardening capacity was 0.42°C, with some individuals displaying upward shifts in heat tolerance of 2.6°C (Phillips et al., 2016). These authors also found an inverse relationship between initial CTmax and heat hardening, whereby skinks with higher initial heat tolerance had a lower heat hardening response than skinks with lower initial heat tolerance. This negative correlation between heat tolerance and heat hardening has been recorded for other ectotherms, including Drosophila (Berrigan and Hoffmann, 1998; Sørensen et al., 2001; Zatsepina et al., 2001) and porcelain crabs (Stillman, 2003). By contrast, we found no relationship between the initial CTmax and hardening in 6-week-old hatchlings. Nonetheless, the magnitude of the heat hardening response that we observed in velvet geckos is very similar to that reported for skinks, and suggests that like skinks, geckos have limited ability to shift their CTmax upwards (Phillips et al., 2016).

Interestingly, incubation under higher temperatures resulted in a significant upward shift in cold tolerance of hatchlings (Fig. 1B); aged 2 weeks, the CTmin of hot-incubated hatchlings was 3.3°C higher than the CTmin of current-incubated hatchlings. This finding mirrors the results of experimental studies on Drosophila. For example, in D. melanogaster, flies which developed at 15°C had a 4°C lower CTmin than flies which developed at 25°C (Slotsbo et al., 2016). Similar patterns have been reported for other species of Drosophila (reviewed in Hoffmann et al., 2003). While there are fewer comparable studies on lizards, a recent study on the rainforest sunskink, Lampropholis coggeri found that hatchlings from cool incubation (constant 23°C) had significantly lower CTmin at 1 month of age than hatchlings from warm (constant 26°C) incubation (Llewelyn et al., 2018). One question that arises from our study is whether the shift in cold tolerance was triggered by differences in the mean, variance or maximum temperature, since minimum temperatures in each treatment differed by only 0.7°C. In other organisms, both mean and variance in developmental temperatures can contribute to differences in cold tolerance. For example, a study on D. melanogaster reared flies under a warm constant environment (25°C), a warm variable environment [25±4°C (s.d.)] and a cool variable environment [18±4°C (s.d.)]. Heat tolerance of flies was unaffected by developmental temperatures, whereas chill coma recovery was longest for warm constant flies and shortest for cold variable flies (Cooper et al., 2012). However, additional studies are necessary to determine the generality of these patterns, and to elucidate the molecular pathways underpinning changes in cold tolerance.

Theoretically, developmental plasticity should result in traits that are irreversible, or at least, longer lasting than those induced via short-term heat hardening or acclimation (Piersma and Drent, 2003). To date, only one previous study on lizards has examined whether developmental plasticity for thermal tolerance persists into later life (Llewelyn et al., 2018). In a study on rainforest sunskinks, egg incubation temperature had a significant effect on the CTmin of hatchlings, but this difference was absent when the individuals were retested as adults (Llewelyn et al., 2018). In our study, developmental plasticity for heat tolerance was short-lived; when we retested hatchlings after 6 weeks, there was no difference in the CTmax of lizards from the two incubation treatments. By contrast, developmental plasticity for cold tolerance persisted into later life, and was still apparent after 6 months in the juveniles that we recaptured from our field sites. Although lizards from both incubation treatments displayed acclimation to field conditions, and shifted cold tolerance downwards, CTmin was still 2.32°C lower, on average, in lizards from the current-incubation treatment (Fig. 3). This pattern agrees with the results from similar studies on insects, which have found that developmental plasticity for cold tolerance is only partly reversible. For example, a study on D. melanogaster found that flies reared at 25°C and acclimated to 15°C as adults were able to shift their cold tolerance downwards, but still had a higher CTmin than 15°C reared flies after 24 days (Slotsbo et al., 2016).

The ecological consequences of developmental shifts in thermal tolerance remains poorly studied, and further research is needed to determine likely effects on survival and demography. In this study, hot-incubated eggs hatched, on average, 26 days earlier than current-incubated eggs. Thus, if nest temperatures increase in future, hatchlings will be born during mid-summer, when temperatures on rock outcrops can be lethally high during heatwaves (Dayananda et al., 2016). Whether the small developmentally-induced shifts in CTmax and heat hardening that we observed in the laboratory could buffer hatchlings from higher environmental temperatures requires further study. Notably, the developmental shift in CTmax was transient, and may therefore have little effect on survival or activity budgets. Furthermore, in most lizard species studied to date, increases in incubation temperatures tended to produce smaller hatchlings (While et al., 2018), a pattern that we also observed in this study. Therefore, developmental shifts in heat tolerance may not outweigh potential survival costs associated with a smaller body size (Andrews et al., 2000; Dayananda et al., 2017; Qualls and Andrews, 1999). Given that developmental shifts in cold tolerance were less reversible than heat tolerance, it is possible that increases in nest temperatures may produce lizards less able to cope with cold winter temperatures. For example, a study on Anolis cristatellus found significant downward shifts in CTmin between introduced and source populations, suggesting that selection has acted on this trait in natural populations (Leal and Gunderson, 2012). For our study species, winter rock temperatures routinely fall to 2.5°C in Nowra and 3°C in Dharawal (Webb, unpublished data), so lizards with lower cold tolerance may be more likely to survive cold snaps, or could have enhanced activity levels during winter. Future studies examining links between cold tolerance, heat tolerance and survival would help evaluate the demographic consequences of developmentally induced shifts in thermal tolerance.

In conclusion, we used a fluctuating temperature incubation experiment to examine the potential for developmental plasticity to produce upward shifts in the heat tolerance of hatchling velvet geckos. After maintaining hatchlings under identical conditions for 6 weeks, we found that the small increase in heat tolerance acquired from hot-temperature incubation was short-lived. Importantly, heat hardening capacity was greater in current-incubated than hot-incubated lizards, so that at 6 weeks of age, the capacity to withstand high temperatures was similar in both treatment groups. Strikingly, developmental shifts in cold tolerance were not reversible, and although both hot- and current-incubated hatchlings showed similar acclimation responses in the field, 6-month-old current-incubated lizards still had lower cold tolerance than hot-incubated lizards. Overall, our results add to the mounting body of evidence suggesting that there is little scope for developmental plasticity to buffer lizards from climate warming.

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