Support for the Adaptive Decoupling Hypothesis from Whole-Transcriptome
Profiles of a Hypermetamorphic and Sexually Dimorphic Insect, Neodiprion
Though seemingly bizarre, the dramatic post-embryonic transformation
that occurs during metamorphosis is one of the most widespread and
successful developmental strategies on the planet. 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 genetically decoupled 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.