Selection on structural allelic variation biases plasticity estimates

Abstract

Wang and Althoff (2019) explored the capacity of Drosophila melanogaster to exhibit adaptive plasticity in a novel environment. In a full‐sib, half‐sib design, they scored the activity of the enzyme alcohol dehydrogenase (ADH) and plastic responses, measured as changes in ADH activity across ethanol concentrations in the range of 0–10% (natural variation) and 16% (the novel environment). ADH activity increased with alcohol concentration, and there was a positive association between larval viability and ADH activity in the novel environment. They also reported that families exhibiting greater plasticity had higher larval survival in the novel environment, concluding that ADH plasticity is adaptive. However, the four authors now concur that, since the study estimated plasticity from phenotypic differences across environments using full‐sib families, it is not possible to disentangle the contributions of allele frequency changes at the Adh locus from regulatory control at loci known to influence ADH activity. Selective changes in allele frequencies may thus conflate estimates of plasticity; any type of “plasticity” (adaptive, neutral, or maladaptive) could be inferred depending on allele frequencies. The problem of scoring sib‐groups after selection should be considered in any plasticity study that cannot use replicated genotypes. Researchers should monitor changes in allele frequencies as one mechanism to deal with this issue.

Rapid within‐ and transgenerational changes in thermal tolerance and fitness in variable thermal landscapes

“…Recovery of reproductive output reported in the literature and in our study might result from the synergistic effects of within-generation plasticity and genetic adaptation (Rodríguez-Romero et al, 2016). As has been recently pointed out, estimates of transgenerational plasticity can be biased due to selection and this is the case even in half-or full-sib designs (Santos, Matos, Wang, & Althoff, 2019). Consequently, these effects are particularly relevant in studies dealing with responses to stressful environments employing outbred populations (e.g., this study or results for O. labronica (Rodríguez-Romero et al, 2016)), which is a problem often neglected in the literature of transgenerational effects (Burggren, 2014;Ho & Burggren, 2010).…”

“…For instance, the drop in survival and fecundity in P flies from V may impose strong selection and observed responses in F1 could partly reflect adaptive responses in the Darwinian sense. While the growing evidence indicates that natural populations can respond rapidly to environmental changes, resulting in full or partial compensatory responses to an environmental stress, caution is warranted regarding inferences on the mechanistic basis underlying these responses (Santos et al, 2019).…”

Environmental predictability drives adaptive within‐ and transgenerational plasticity of heat tolerance across life stages and climatic regions

“…Larval acclimation involved the latter part of egg-to-larva development, and this transition may have been potentially affected by thermal selection. This effect has recently been demonstrated for ADH activity (Santos et al, 2019). Our estimations of WGP for larval tolerance should be taken with caution since potentially its measurement could have been biased.…”

“…A common bias in TGP estimations involving stress responses is the potential effect that suboptimal or stressful conditions can impose on experimental groups, particularly for early developmental stages (Heckwolf et al., 2018; Kaufmann et al., 2014). The vulnerability of early stages is not always visible and might impose selection pressure for more tolerant genotypes, resulting in a biased estimation of plasticity (Santos et al., 2019). Our approach accounted for such potential bias by acclimating the parental generation as adults.…”

Rapid within- and transgenerational changes in thermal tolerance and fitness in variable thermal landscapes

“…Recovery of reproductive output reported in the literature and in our study might result from the synergistic effects of within-generation plasticity and genetic adaptation (Rodríguez-Romero et al , 2016). As has been recently pointed out, estimates of transgenerational plasticity can be biased due to selection and this is the case even in half-or full-sibs designs (Santos et al , 2019). Consequently, these effects are particularly relevant in studies dealing with responses to stressful environments employing outbred populations (e.g., this study or results for O. labronica (Rodríguez-Romero et al , 2016)), which is a problem often neglected in the literature of transgenerational effects (Ho & Burggren, 2010;Burggren, 2014).…”