A selection-based framework for evaluating transgenerational phenotypic plasticity under environmental change

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Abstract

Rapid environmental change has intensified interest in inter- and transgenerational phenotypic plasticity (TGP) as a potential mechanism by which populations may buffer the fitness consequences of climate change. Parental environments frequently induce shifts in offspring phenotypes, and such responses are often implicitly assumed to enhance offspring fitness and thus population persistence. However, evidence for phenotypic change alone is insufficient to demonstrate adaptive value, particularly when fitness is inferred from performance proxies rather than survival or reproduction. Here, we argue that a more agnostic null hypothesis is required when evaluating the fitness consequences of TGP: that intergenerational phenotypic shifts may be neutral, maladaptive, or context-dependent, rather than inherently beneficial. We propose selection analysis as a general, quantitative framework for assessing whether phenotypic variation associated with parental environments align with fitness variation in offspring. This approach does not seek to identify the mechanistic basis of TGP, nor to disentangle plasticity from genetic or epigenetic causation, but instead provides a diagnostic test of whether observed phenotypic shifts are associated with positive, negative, or absent selection. Using worked examples across taxa and environmental contexts, we demonstrate that TGP frequently does not align with selection, despite pronounced changes in offspring phenotype. These findings highlight the risk of over-interpreting intergenerational phenotypic responses as evidence of resilience to environmental change. Integrating selection analysis into studies of TGP provides a tractable and comparable framework for evaluating whether intergenerational responses enhance, constrain, or have no effect on population persistence under environmental change.

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