Limited plasticity in thermally tolerant ectotherm populations: evidence for a trade-off

Abstract

Many species face extinction risks owing to climate change, and there is an urgent need to identify which species' populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism's upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found few generalizable patterns to explain variation in this trait. Here, we report the results of, to our knowledge, the first meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermal acclimation capacities across 78 populations. We used meta-regression to evaluate two leading hypotheses. The climate variability hypothesis predicts that populations from more thermally variable habitats will have greater plasticity, while the trade-off hypothesis predicts that populations with the lowest heat tolerance will have the greatest plasticity. Our analysis indicates strong support for the trade-off hypothesis because populations with greater thermal tolerance had reduced plasticity. These results advance our understanding of variation in populations' susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming.

Evolution in changing seas

“…In another study, Barley et al conducted a metaanalysis of within-species variation in thermal plasticity, but did not find support for the climate variability hypothesis [18]. Instead, their analysis showed that populations with greater thermal tolerance had reduced plasticity, which was evidence for trade-offs between thermal tolerance and thermal plasticity [18].…”

“…Two studies in this Special Feature challenge the widespread notion that increased climate variability also increases thermal tolerance and plasticity [18,19]. Bitter et al reviewed theoretical predictions for the evolution of plasticity in fluctuating environments, and showed that it is the predictability (rather than the amplitude) of fluctuations that primarily drive the amount of phenotypic plasticity present in natural populations.…”

“…They proposed an experimental design that future studies can use to tease apart the effects of the amplitude, predictability and novelty of climate fluctuations on population fitness and persistence [19]. In another study, Barley et al conducted a metaanalysis of within-species variation in thermal plasticity, but did not find support for the climate variability hypothesis [18]. Instead, their analysis showed that populations with greater thermal tolerance had reduced plasticity, which was evidence for trade-offs between thermal tolerance and thermal plasticity [18].…”

Parallel adaptation to lower altitudes is associated with enhanced plasticity in Heliosperma pusillum (Caryophyllaceae)

“…Evidence from natural study systems is required to clarify under which conditions plasticity is favored or hindered by evolution. A meta-study by Barley et al (2021) quantified thermal acclimation capacity across 19 species including arthropods, molluscs, and chordates, showing that within species, marginal populations experiencing the highest thermal conditions had decreased plasticity and acclimation capacity. A negative relationship between plasticity and adaptation to heat extremes was also found in laboratory experiments (Kelly et al, 2017;Sasaki & Dam, 2021).…”

Testing for genetic assimilation with phylogenetic comparative analysis: Conceptual, methodological, and statistical considerations

“…Motivated by current debate surrounding the Trade-off Hypothesis and increasing interest in the evolution of phenotypic plasticity and genetic assimilation under global change (Gunderson and Stillman 2015; Kelly 2019; Sasaki and Dam 2019; van Heerwaarden and Kellermann 2020; Barley et al 2021; Preston et al 2021; Sasaki and Dam 2021), we used simulations to explore the more general consequences of regression to the mean for tests of genetic assimilation at the macroevolutionary level. We conducted simulations that assumed mechanistically different models for plasticity evolution, as well as different experimental sampling designs for measuring species phenotypic traits.…”