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

Nathan William Bailey*, Camille Desjonqueres, Ana Drago Rosa, Jack Gregory Rayner, Samantha Leigh Sturiale, Xiao Zhang

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

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.
Original languageEnglish
Pages (from-to)444-457
Number of pages14
JournalEvolution Letters
Volume5
Issue number5
Early online date23 Aug 2021
DOIs
Publication statusPublished - Oct 2021

Keywords

  • Adaptation
  • Indirect genetic effects
  • Interacting phenotype
  • Phenotypic accommodation
  • Pleiotropy
  • Social drive

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