No abstract

Though seemingly bizarre, the dramatic morphological and ecological transformation that occurs when immature life stages metamorphose into reproductive adults is one of the most successful developmental strategies on the planet. The adaptive decoupling hypothesis (ADH) proposes that metamorphosis is an adaptation for breaking developmental links between traits expressed in different life stages, thereby facilitating their independent evolution when exposed to opposing selection pressures. Here, we draw inspiration from the ADH to develop a conceptual framework for understanding changes in gene expression across ontogeny. We hypothesized that patterns of stage‐biased and sex‐biased gene expression are the product of both decoupling mechanisms and selection history. To test this hypothesis, we characterized transcriptome‐wide patterns of gene‐expression traits for three ecologically distinct larval stages (all male) and adult males and females of a hypermetamorphic insect (Neodiprion lecontei). We found that stage‐biased gene expression was most pronounced between larval and adult males, which is consistent with the ADH. However, even in the absence of a metamorphic transition, considerable stage‐biased expression was observed among morphologically and behaviourally distinct larval stages. Stage‐biased expression was also observed across ecologically relevant Gene Ontology categories and genes, highlighting the role of ecology in shaping patterns of gene expression. We also found that the magnitude and prevalence of stage‐biased expression far exceeded adult sex‐biased expression. Overall, our results highlight how the ADH can shed light on transcriptome‐wide patterns of gene expression in organisms with complex life cycles. For maximal insight, detailed knowledge of organismal ecology is also essential.

Complex life cycles-especially those with distinct larval and adult stages separated by a complete metamorphic event-are common in animals. The adaptive decoupling hypothesis (ADH) proposes that metamorphosis is an adaptation for optimizing expression of traits across life stages that experience opposing selection pressures. Similarly, sex-biased expression of traits is thought to evolve in response to sexually antagonistic selection. Both hypotheses predict that traits will be decoupled (i.e., genetically uncorrelated) among developmental stages and sexes, but direct comparisons between stage-specific and sex-specific decoupling are rare. Additionally, tests of the ADH have been hampered by a lack of suitable traits for among-stage comparisons and by uncertainties regarding how much decoupling is to be expected. To fill these voids, we characterize transcriptome-wide patterns of gene-expression decoupling in the hypermetamorphic and sexually dimorphic insect, Neodiprion lecontei. This species has three ecologically and morphologically distinct larval stages separated by molts, as well as a complete metamorphic transition that produces dimorphic adult males and females. Consistent with the ADH, we observe that: (1) the decoupling of gene expression becomes more pronounced as the ecological demands of developmental stages become more dissimilar and (2) gene-expression traits that mediate changing ecological interactions show stronger and more variable decoupling than expression traits that are likely to experience more uniform selection. We also find that gene-expression decoupling is more pronounced among major life stages than between the sexes. Overall, our results demonstrate that patterns of gene-expression decoupling can be predicted based on gene function and organismal ecology. Significance Statement8 out of 10 animals undergo a metamorphic transition at some point in their life. The adaptive decoupling hypothesis proposes that metamorphosis is widespread because it enables natural selection to act independently on traits expressed at different stages. Using four ecologically distinct life stages of the redheaded pine sawfly, we show that the dissimilarity of gene expression profiles can be predicted based on the ecological dissimilarity of the life stages and on whether these genes impact ecological interactions. We also find that gene expression is more dissimilar between drastic life stages than between different sexes. Together, these results provide strong support for a core assumption of the ADH: that metamorphosis enables organisms to optimize genetic correlations across development.