When is warmer better? Disentangling within- and between-generation effects of thermal history on early survival

Understanding the fitness consequences of thermal history is necessary to predict organismal responses to global warming. This is especially challenging for ectotherms with complex life cycles, where distinct life stages can differ in thermal sensitivity, acclimate to different thermal environments and accrue responses to acclimation within and between generations. Although acclimation is often hypothesized to benefit organisms by helping them (or their offspring) to compensate for negative impacts of environmental change, mixed support for this hypothesis highlights the need to assess alternatives. Assessments that explicitly dissect responses across life stages and generations, however, remain limited. We assess alternative hypotheses of acclimation (none, beneficial, colder-is-better and warmer-is-better) within and between generations of a marine tubeworm whose vulnerability to warming rests on survival at early planktonic stages (gametes, embryos and larvae). First, we acclimate parents, gametes and embryos to ambient and projected warmer temperatures (17°C and 22°C) factorially by life stage. Next, we rear offspring with differing acclimation histories to the end of larval development at test temperatures from 10°C to 28°C (lower and upper survival limits respectively). Last, we estimate thermal survival curves for development, and compare them among thermal histories. We show that survival curves are most responsive to parental acclimation followed by acclimation at embryogenesis, but are buffered against acclimation at fertilization. Moreover, curves respond independently to acclimation within and between generations, and respond largely as predicted by the warmer-is-better hypothesis, despite the semblance of beneficial acclimation after successive doses of warmer temperature. Our study demonstrates the varied nature of thermal acclimation and the importance of considering how responses aggregate across complex life cycles when predicting vulnerability to warming. Read the free Plain Language Summary for this article on the Journal blog.