A neglected conceptual problem regarding phenotypic plasticity's role in adaptive evolution: The importance of genetic covariance and social drive

Abstract

There is tantalizing evidence that phenotypic plasticity can buffer novel, adaptive genetic variants long enough to permit their evolutionary spread, and this process is often invoked in explanations for rapid adaptive evolution. However, the strength and generality of evidence for it is controversial. We identify a conceptual problem affecting this debate: recombination, segregation, and independent assortment are expected to quickly sever associations between genes controlling novel adaptations and genes contributing to trait plasticity that facilitates the novel adaptations by reducing their indirect fitness costs. To make clearer predictions about this role of plasticity in facilitating genetic adaptation, we describe a testable genetic mechanism that resolves the problem: genetic covariance between new adaptive variants and trait plasticity that facilitates their persistence within populations. We identify genetic architectures that might lead to such a covariance, including genetic coupling via physical linkage and pleiotropy, and illustrate the consequences for adaptation rates using numerical simulations. Such genetic covariances may also arise from the social environment, and we suggest the indirect genetic effects that result could further accentuate the process of adaptation. We call the latter mechanism of adaptation social drive, and identify methods to test it. We suggest that genetic coupling of plasticity and adaptations could promote unusually rapid ‘runaway’ evolution of novel adaptations. The resultant dynamics could facilitate evolutionary rescue, adaptive radiations, the origin of novelties, and other commonly studied processes.

Behavioural plasticity compensates for adaptive loss of cricket song

“…A fundamental prediction of evolutionary theory is that new mutations under selection are prone to indirect, disruptive effects arising from negative pleiotropy (Fisher, 1958;Orr, 1998Orr, , 2005. Behaviour has been thought to play an important role in buffering such effects by enhancing the adaptive potential of populations in which such mutations invade (Bailey et al, 2021;Duckworth, 2009;Pfennig et al, 2010;West-Eberhard, 2005;Zuk et al, 2014). In Hawaiian T. oceanicus, we found evidence that populations can maintain population-level fitness despite the loss of their main sexual signal.…”

“…In contrast, behavioural flexibility could expose new beneficial phenotypes to the action of selection, eventually leading to their fixation and promoting evolutionary adaptation (Levis & Pfennig, 2016;West-Eberhard, 2005). The third potential influence of behaviour combines these processes: adaptive mutations can have indirect costs arising from negative, or antagonistic, pleiotropy (Fisher, 1958;Orr, 1998Orr, , 2005Williams, 1957), and flexible behaviours could mitigate these for long enough to allow such mutations to spread under selection (Bailey et al, 2021;West-Eberhard, 2005;Zuk et al, 2014). This process has arguably received the least attention, and it usually remains unknown whether, or how, flexibility in behaviour mitigates negative fitness effects of new adaptive variants.…”

Temporal genomics in Hawaiian crickets reveals compensatory intragenomic coadaptation during adaptive evolution

“…It is well-established that transitions or other alterations to social environments can have strong phenotypic and fitness consequences, and selection arising from these transitions has been argued to be a significant evolutionary force that affects the tempo of adaptation and diversification 65 , 66 . Genetic responses to selection are required for the latter evolutionary processes to occur, and when a new variant under selection is the cause of social transitions, the resulting feedback process is predicted to drive intragenomic coadaptation 2 , 67 . There is surprisingly little empirical data that can inform this controversial process, perhaps due to the experimental complexity of disentangling simultaneous evolutionary feedback loops (cf.…”

“…Fig. 1a ; see also 67 ), and the specific and well-characterised set of conditions required of a study system to exclude alternative explanations. As a result of the rapid bout of adaptation in Hawaiian T. oceanicus , the social environment of the Kauai population changed dramatically from one dominated by a conspicuous signal conveying information about potential mating partners or rivals to one in which the mating dynamics no longer correspond in a meaningful way to social signals in the environment (Fig.…”

Within-generation and transgenerational social plasticity interact during rapid adaptive evolution

“…Theory predicts that, following rapid environmental change, populations may exhibit a transient increase in plasticity because genotypes which shift trait expression closer to a new optimum are favored (Lande 2009). Additionally, genotypes coding for reaction norm slopes of other traits that offset negative effects of new variants spreading under selection may also be favored, as appears to be the case in T. oceanicus in Hawaii and other systems (Bailey et al 2021). If increases in WGP during an adaptive evolutionary response result in a spillover of non-adaptive TGP to the offspring generation, the role of plasticity in facilitating the establishment and spread of novel adaptations may be less straightforward than currently understood (Lacey 1998;Bonduriansky and Day 2009;Bell and Hellmann 2019).…”