Discussion

According to the ADH, complex life cycles are pervasive in nature because they facilitate the independent evolution of traits expressed at different life stages, thereby removing constraints that may otherwise slow or prevent adaptation to novel environments (Moran, 1994). Evidence for a key prediction of the ADH—that traits are decoupled across metamorphosis—has been mixed ((Aguirre et al., 2014; Collet & Fellous, 2019; Fellous & Lazzaro, 2011; Freda, Alex, Morgan, & Ragland, 2017; Saenko et al., 2012; Sherratt et al., 2017) and references therein). Here we argue that if metamorphosis is an adaptation for optimizing genetic correlations across life stages, genetic decoupling may evolve only for traits that experience antagonistic selection across ontogeny. In other words, the ADH does not necessarily predict that all traits will be decoupled, but rather that trait decoupling should be somewhat predictable given sufficient knowledge of stage-specific selection pressures. Therefore knowledge of how selection pressures may differ on traits across development is essential to predicting and interpreting patterns of decoupling for individual gene-expression traits with respect to testing the ADH.
To evaluate the predictability of trait decoupling in light of the ADH, we took advantage of a well-characterized hypermetamorphic insect, the redheaded pine sawfly (Figure 1) to generate a priori predictions regarding the decoupling of gene-expression traits. Consistent with our predictions, we found that: 1) ecological differences between life stages enabled us to accurately predict how transcriptome-wide levels of gene-expression decoupling vary across development (Figure 2). 2) Levels of decoupling vary among functionally different genes in the transcriptome, with ecologically relevant genes being some of the most highly and variably decoupled genes between life stages (Supplemental Tables 3-5 and Figure 3). 3) Decoupling of gene-expression traits tended to be more pronounced between developmental stages than between sexes (Figures 2 and 3). Here, we compare our results to other studies of trait decoupling under ontogenetically and sexually antagonistic selection and, in light of this body of work and limitations of our own study, make suggestions for future research on the ADH.