Support for the adaptive decoupling hypothesis from whole-transcriptome profiles of a hypermetamorphic and sexually dimorphic insect, Neodiprion lecontei

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.