Support for the Adaptive Decoupling Hypothesis from Whole-Transcriptome Profiles of a Hypermetamorphic and Sexually Dimorphic Insect,Neodiprion lecontei

Abstract

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.

Transcriptomic and functional genetic evidence for distinct ecophysiological responses across complex life cycle stages

“…Their morphology has evolved independently in juvenile and adult stages that inhabit drastically different ecological niches. There are clear physiological differences across complex life cycle stages as well, in part because distinct developmental machinery underlies distinct morphologies and life history strategies across the life cycle (Arbeitman et al, 2002;Herrig et al, 2021;van Gestel et al, 2019). Such morphological and developmental decoupling supports the adaptive decoupling hypothesis, which posits that natural selection favors reduced genetic correlation across developmental stages to allow for stage-specific adaptation (Moran, 1994).…”

The impact of life stage and pigment source on the evolution of novel warning signal traits

“…Thus, diet quality impacts N. lecontei fitness in multiple ways, including the availability of defensive terpene compounds (39) as well as acting as a direct source of carotenoids for conspicuous warning coloration (46) and immune function. By contrast, N. lecontei adults are not aposematic, and adult and larval pigmentation is decoupled in pine sawflies (51). Therefore, larval color is not likely to be subject to sexual selection.…”

The impact of life stage and pigment source on the evolution of novel warning signal traits

“…Thus, diet quality impacts N. lecontei fitness in multiple ways, including the availability of defensive terpene compounds (Codella and Raffa 1995) as well as acting as a direct source of carotenoids for conspicuous warning coloration (Linnen et al 2018) and immune function. By contrast, N. lecontei adults are not aposematic, and expression of pigmentation genes is decoupled between larval and adult stages of this species (Herrig et al 2021). Therefore, larval color is not likely to be subject to sexual selection.…”

“…As a result, this can further strengthen selection against novel warning signal forms (Jiggins et al 2001;Reynolds and Fitzpatrick 2007). By contrast, because coloration tends to be decoupled across ontogeny (Gaitonde et al 2018;Galarza et al 2019;Medina et al 2020;Herrig et al 2021; but see Lindstedt et al 2016), aposematic larvae are not usually subject to direct sexual selection. Furthermore, aposematic larvae can occur in aggregations (Sillén-Tullberg 1988;Terbot et al 2017;Wang et al 2021), which can weaken selection against novel signals (Mappes and Alatalo 1997;Riipi et al 2001).…”