Environmental predictability drives adaptive within‐ and transgenerational plasticity of heat tolerance across life stages and climatic regions

Abstract

Although environmental variability and predictability have been proposed as the underlying ecological context in which transgenerational plasticity (TGP) arises, the adaptive significance and interaction with within‐generation plasticity (WGP) in such scenarios is still poorly understood. To investigate these questions, we considered the tolerance to upper thermal limits of larvae and adults of the desert endemic Drosophila mojavensis adapted to different climatic regions (Desert vs. Mediterranean climate). Thermal plasticity was investigated by acclimating parents and offspring at 36°C (vs. at 25°C). We then used historical temperature variation data from both regions to perform individual‐based simulations by modelling expected components of adaptive plasticity in multiple life stages. Our results indicated that thermal response to ramping heat shocks was more pronounced in larvae, where acclimation treatments in parents and offspring increased their heat‐shock performance, while heat knockdown in adults was only increased by offspring acclimation of adults. The relative contribution of WGP and TGP was greater for the population from the more thermally variable Sonoran Desert. Similarly, individual‐based simulations of evolving maternal effects indicated that variation in tolerance to upper thermal limits across life stages and climates is expected from its adaptive significance in response to environmental predictability. Our approach offers a new perspective and interpretation of adaptive plasticity, demonstrating that environmental predictability can drive thermal responses across generations and life stages in a scenario with regional climate variability. A free Plain Language Summary can be found within the Supporting Information of this article.

Physiology and acclimation potential are tuned with phenology in larvae of a prolonged breeder amphibian

“…Since in our study animals were kept in identical conditions, external cues such as photoperiod (Sanabria and Quiroga 2011) can be ruled out as triggers of anticipatory mechanisms. Then, the observed difference in survival between autumn (Ap) and spring (S) cohorts is compatible with a scenario of TGP (Fox and Mousseau 1998, Richter-Boix et al 2014, Yin et al 2019, in which the breeding phenology of parents precondition their offspring thermal physiology and, thus, survival probability given their environment (Putnam and Gates 2015, Sun et al 2018, Diaz et al 2020.…”

“…Anticipatory TGP has been shown to increase the survival probability of offspring in a wide range of organisms, form invertebrate to vertebrate ectotherms (Rosa et al 2012, Chirgwin et al 2018, Diaz et al 2020). Our results suggest that larvae of A. almogavarii may also benefit from TGP, which might act as a link between the environment experienced by parents and the expected thermal conditions of larvae to increase survival.…”

Genotypic variation of transgenerational plasticity can be explained by environmental predictability at origins

“…This study indicates that factors driving the divergence among genotypes are not random but may involve diversifying selective forces associated with local climates. Meanwhile, comparing two Drosophila mojavensis populations revealed that the population from the habitat with higher thermal predictability has greater transgenerational plasticity to heat tolerance (Diaz et al 2020). Nevertheless, such comparative and correlative studies on the natural variation of transgenerational plasticity are still rare.…”

Exploring links between climatic predictability and the evolution of within- and transgenerational plasticity

“…When parents can predict the offspring conditions based on the prevailing environmental information, adaptive TGP can enhance offspring fitness (Burgess and Marshall 2014, Bonduriansky 2021). However, environmental predictability is scarcely quantified despite being a core pre-requisite for the evolution of adaptive TGP, especially in non-model organisms (but see Burgess and Marshall 2011, Shama 2015, Halali et al 2021, Diaz et al 2021). Experimental evolution studies on species with short generation times have explicitly shown that adaptive TGP readily evolves when selection lines are maintained in a temporally autocorrelated environment (e.g.…”