Comparing decoupling across development to decoupling between the
sexes
Beyond metamorphosis, the logic of the ADH applies to any situation in
which pervasive antagonistic selection favors the evolution of reduced
genetic correlations. Although theories explaining sexual dimorphism are
conceptually similar to the ADH, the evolutionary trajectories of
sexually antagonistic selection may differ predictably from those under
ontogenetically antagonistic selection. However, few studies have
directly compared patterns of sex-biased and stage-biased gene
expression. In one notable exception, Perry et al. (2014) evaluated how
patterns of sex-biased expression in gonadal tissue change between three
developmental stages of Drosophila melanogaster . In contrast to
our finding that sex-biased expression was modest compared to
stage-biased expression (Figure 2), they reported greater decoupling
between the sexes than between larvae and prepupae. This apparent
discrepancy could be explained by minimal antagonistic selection between
dispersing Drosophila larvae and prepupae, the lack of a distinct
molt between these observed stages, or tissue specificity. By
contrast—and consistent with our findings—a comprehensive analysis
of gene expression in different developmental stages, sexes, and castes
of two ant species revealed that developmental stage had the largest
impact on gene-expression profiles (Ometto et al., 2011). Given that the
intensity of sexually antagonistic selection is likely to be highly
variable across taxa, traits, and tissues (Connallon & Clark, 2013;
Connallon, Débarre, & Li, 2018; Pennell & Morrow, 2013), studies in
diverse taxa will be needed to evaluate if decoupling of stage-biased
expression consistently exceeds sex-biased expression.
A final layer of complexity is that if the genetic targets and/or
intensity of sexually antagonistic selection vary across an organism’s
life cycle, patterns of sex-biased gene expression may also be decoupled
over ontogeny. In support of this prediction, Perry et al. (2014)
reported that 18-30% of sex-biased genes exhibited stage-specific
sex-biased expression, with 4.5% of genes having opposing sex bias at
different stages. Importantly, sex- and stage-specificity impacted
evolutionary rates with male-biased genes evolving most rapidly when
expressed throughout development while female-biased genes evolved most
rapidly when expressed in larvae only. Overall, these results are
consistent with the view that sexually antagonistic and stage-specific
selection can lead to predictable differences in patterns of gene
expression and molecular evolution.