Thermal tolerance of early development predicts the realized thermal niche in marine ectotherms

Abstract

Predictions of ectotherms' responses to global warming depend on the relationship between environmental temperature and organismal performance. To date, most predictions of thermal responses are generated from experimentally derived measures of thermal tolerances of adults or estimates of thermal niches derived from geographic distributions of adults. It is unknown how measures derived from these different approaches compare, or, as thermal performance of ectotherms varies through ontogeny, how they compare across life stages. To understand the efficacy of the temperature–performance relationship of early developmental stages as predictors of geographic range, we empirically documented the upper and lower thermal tolerance limits of embryos of eight species of ectotherms with complex life cycles. We compared the embryonic thermal tolerances of each species to that of the adults (documented in a previous study), as well as to an estimate of the thermal niche derived from adult distributions. Our results show that in all eight species the upper thermal limit estimated from embryos is significantly lower than the upper thermal limit estimated from adults. The lower thermal limit for embryos and for adult performance are similar, but the lower thermal limit for adult survival is significantly lower. Warming tolerances, calculated as the difference between upper tolerance limit and the average ambient temperature during the warmest month, for each species are also smaller for embryos (~1°C) than for adults (~5°C). These results show that thermal tolerances of early developmental stages, which are often easier to obtain for large sample sizes over an array of temperatures than are tolerances of adults, are a powerful, and potentially more accurate tool for predicting future responses to climate change. A free Plain Language Summary can be found within the Supporting Information of this article.

Thermal Performance Curves Are Shaped by Prior Thermal Environment in Early Life

“…Such an interpretation is of course speculative at this point. Our results do, however, add to mounting evidence pointing to embryogenesis as the most critical of early life stages in aquatic ectotherms, not only for the emergence of thermal sensitivity ( Dahlke et al, 2020 ; Rebolledo et al, 2020 ; Collin et al, 2021 ), but also of thermal carryover effects. Although, our results suggest that fertilization matters less in this regard, the possibility remains that the environment at gametogenesis is more influential than the environment at fertilization, emphasising the need to better understand transgenerational effects on thermal performance.…”

“…Nevertheless, most studies to date measure thermal performance and sensitivity at single life stages ( Byrne et al, 2020 ) and predominantly in adults ( Truebano et al, 2018 ; Pandori and Sorte, 2019 ). This is problematic in light of emerging evidence that reproductive stages and embryos tend to be more thermally sensitive and may better predict the vulnerability of ectotherms to climate warming ( Dahlke et al, 2020 ; Rebolledo et al, 2020 ; Collin et al, 2021 ; Van Heerwaarden and Sgrò, 2021 ). Moreover, thermal performance at these critical stages is often incompletely characterized due to well-known challenges in gathering sufficient data, so that information about ontogenetic shifts in thermal limits and thermal optima, in particular, currently remains too limited to identify any general patterns ( Kingsolver and Buckley, 2020 ).…”

“…Evidence also suggests that these carryover effects can be more lasting and pervasive the earlier that they are induced in ontogeny, and especially when induced at embryogenesis ( Watkins and Vraspir, 2006 ; Jonsson and Jonsson, 2014 ; Noble et al, 2018 ). This outcome possibly relates to the particular thermal sensitivity of embryos ( Sanger et al, 2018 ; Rebolledo et al, 2020 ; Collin et al, 2021 ), and ample scope for thermal perturbation of cell division, differentiation, and regulatory pathways during this window of development to profoundly alter future form, function, and performance ( Van Der Have, 2002 ; Hamdoun and Epel, 2007 ; Begasse et al, 2015 ). In general, however, the adaptive significance of carryover effects – at least those attributable to plasticity – remains contentious.…”

Staying in place and moving in space: Contrasting larval thermal sensitivity explains distributional changes of sympatric sea urchin species to habitat warming

“…The cool and warm temperature limits for 50% echinopluteus larvae (EL 50 ) were used to determine larval cool and warm tolerance (CT, WT) (Collin et al, 2021; Deutsch et al, 2008). Cool tolerance (CT) was determined as the difference between the cool EL 50 and the mean ambient local SST during winter (18.6°C, Wolfe et al, 2020).…”

Differential Tolerance and Seasonal Adaptation to Temperature and Salinity Stress at a Dynamic Range Boundary Between Estuarine Gastropods

“…In diverse marine invertebrates, embryonic or larval stages commonly exhibit greater sensitivity to environmental stressors than adults (Przeslawski et al, 2015). Salinity or temperature gradients can limit adult distributions by impeding supply-side processes when conditions exceed embryonic or larval tolerance (Mann and Harding, 2003;Sanford et al, 2006;Collin et al, 2021). Here we found that embryos of both species were notably more vulnerable to prolonged immersion in low salinity than larvae or adults.…”