The predictably variable decoupling of some ecologically important
traits
If metamorphosis facilitates optimization of genetic correlations, then
patterns of trait decoupling should depend on how changing ecological
selection pressures align with genetic correlations across development
(Collet et al. 2019). Variation in selection pressures experienced by
different traits should generate corresponding variation in decoupling
patterns. If selection optimizes gene-expression traits, the extent of
gene-expression decoupling across life stages/sexes should vary even
among genes belonging to the same narrow functional category depending
on precise ecological roles (e.g., (Fellous & Lazzaro, 2011)).
Consistent with this expectation, we observed a wide range of decoupling
patterns for expression levels of different chemosensory genes (Figure
3). In some cases, antagonistic selection may have favored decoupling of
gene expression traits—for example, perhaps males and females express
different chemosensory genes to optimize mate- and host-finding,
respectively. In other cases, selection may have favored positive
genetic correlations between host-use traits expressed at different life
stages (Agrawal & Stinchcombe, 2009; Vertacnik & Linnen, 2017). For
example, in sawflies, each life stage interacts with the host plant and
these stages may express some chemosensory genes across development
(coupled expression) to monitor important host chemical cues (Figure 1A,
Figure 3D). Beyond sawflies, numerous studies of stage-specific gene
expression in many other insect taxa have found trends very similar to
those reported here, with chemosensory genes exhibiting both high and
low levels of gene-expression decoupling (Colgan et al., 2011; Etges et
al., 2015; Harker et al., 2013; Koutsos et al., 2007; Lee et al., 2016;
Sayadi, Immonen, Bayram, & Arnqvist, 2016; Schönbach et al., 2013; H.
Yang et al., 2018; Zhang, He, & Wang, 2016). Thus, high variance among
chemosensory genes in the degree of coupling/decoupling across
development may be a common outcome of adaptive gene expression
evolution (Vertacnik & Linnen, 2017).
Mixed decoupling patterns have also been observed for other types of
ecologically important gene-expression traits. One such example comes
from a 2011 study that investigated expression decoupling of two
antimicrobial peptide (AMP) genes between Drosophila melanogasterlarvae and adults (Fellous & Lazzaro, 2011). Using a quantitative
genetic approach, Fellous and Lazarro (2011) found that while one of
these immunity genes had transcription levels that were significantly
correlated across development, expression of the other gene was
genetically decoupled. Although the authors interpreted the strong
genetic correlation between larval and adult expression for one of the
AMP genes as contradicting the ADH, they also acknowledged that they
lacked a priori predictions regarding expected genetic correlations for
these immune traits. One potential explanation for these contrasting
decoupling patterns is that AMPs with decoupled expression are optimized
for stage-specific pathogens, whereas coupled AMPs respond to pathogens
that attack multiple life stages. Similarly, because some parasites and
pathogens of N. lecontei are highly stage-specific (Coppel and
Benjamin 1955; Wilson et al. 1992), we would expect at least some—but
not necessarily all—immune genes to have decoupled gene expression.
Consistent with these predictions, a manually curated set of N.
lecontei immune-related genes (Vertacnik et al., in prep) had highly
variable decoupling patterns across life stages (Supplemental Tables
3-5).
The final trait we consider that may frequently evolve under conflicting
selection pressures across development is pigmentation. In insects,
coloration is subject to diverse selection pressures—including abiotic
factors (thermoregulation, UV resistance, desiccation tolerance),
predation, and sexual selection—that are likely to change over the
course of development (Medina et al., 2020; True, 2003). Consistent with
the ADH, an analysis of larval and adult coloration in 246 butterfly
species found that color evolution is strongly decoupled across
butterfly development (Medina et al., 2020). Notably, whereas selection
stemming from predation appears to constrain larval color evolution,
sexual selection on adult males gives rise to extensive interspecific
variation in adult color. Although Medina et al. (2020) did not
investigate the genetic underpinnings of color trait decoupling, genetic
analysis in another lepidopteran (Bicyclus anynana ) demonstrates
that melanism in larvae and adults is controlled by separate loci
(Saenko et al., 2012). Similarly, our results suggest that pine sawflies
have pronounced decoupling of gene-expression traits related to
pigmentation across development. For example, among our top
differentially expressed genes among different life stages were top
candidate genes identified by a QTL mapping analysis of among-population
variation in melanin-based (pale) and carotenoid-based
(Cameo2 ) larval pigmentation traits (Linnen et al., 2018).
Together with previous studies, our findings are consistent with the ADH
prediction that selection for optimal trait decoupling across
development yields strikingly heterogeneous patterns of decoupling for
ecologically important traits. Additional studies are needed, however,
to demonstrate that highly and minimally decoupled traits evolve under
stage-specific and stage-independent selection pressures, respectively.
Nevertheless, this collection of studies highlights the importance of
taking ecology and stage-specific selection pressures into account when
testing predictions of the ADH.