Thermal plasticity has higher fitness costs among thermally tolerant genotypes of Tigriopus californicus

Abstract

Under climate change, ectotherms will likely face pressure to adapt to novel thermal environments by increasing their upper thermal tolerance and its plasticity, a measure of thermal acclimation. Ectotherm populations with high thermal tolerance are often less thermally plastic, a trade-off hypothesized to result from (i) a phenotypic limit on thermal tolerance above which plasticity cannot further increase the trait, (ii) negative genetic correlation or (iii) fitness trade-offs between the two traits. Whether each hypothesis causes negative associations between thermal tolerance and plasticity has implications for the evolution of each trait. We empirically tested the limit and trade-off hypotheses by leveraging the experimental tractability and thermal biology of the intertidal copepod Tigriopus californicus. Using populations from four latitudinally distributed sites in coastal California, six lines per population were reared under a laboratory common garden for two generations. Ninety-six full sibling replicates (n = 4–5 per line) from a third generation were developmentally conditioned to 21.5 and 16.5°C until adulthood. We then measured the upper thermal tolerance and fecundity of sibships at each temperature. We detected a significant trade-off in fecundity, a fitness corollary, between baseline thermal tolerance and its plasticity. Tigriopus californicus populations and genotypes with higher thermal tolerance were less thermally plastic. We detected negative directional selection on thermal plasticity under ambient temperature evidenced by reduced fecundity. These fitness costs of plasticity were significantly higher among thermally tolerant genotypes, consistent with the trade-off hypothesis. This trade-off was evident under ambient conditions, but not high temperature. Observed thermal plasticity and fecundity were best explained by a model incorporating both the limit and trade-off hypotheses rather than models with parameters associated with one hypothesis. Effects of population and family on tolerance and plasticity negatively covaried, suggesting that a negative genetic correlation could not be ruled as contributing to negative associations between the traits. Our study provides a novel empirical test of the fitness trade-off hypothesis that leverages a strong inference approach. We discuss our results' insights into how thermal adaptation may be constrained by physiological limits, genetic correlations, and fitness trade-offs between thermal tolerance and its plasticity.