Developmental models reveal the role of phenotypic plasticity in explaining genetic evolvability

Abstract

<jats:title>Abstract</jats:title><jats:p>Biological evolution exhibits an extraordinary capability to adapt organisms to their environments. The explanation for this often takes for granted that random genetic variation produces at least some beneficial phenotypic variation for natural selection to act on. Such genetic evolvability could itself be a product of evolution, but it is widely acknowledged that the immediate selective gains of evolvability are small on short timescales. So how do biological systems come to exhibit such extraordinary capacity to evolve? One suggestion is that adaptive phenotypic plasticity makes genetic evolution find adaptations faster. However, the need to explain the origin of adaptive plasticity puts genetic evolution back in the driving seat, and genetic evolvability remains unexplained. To better understand the interaction between plasticity and genetic evolvability, we simulate the evolution of phenotypes produced by gene-regulation network-based models of development. First, we show that the phenotypic variation resulting from genetic and environmental change are highly concordant. This is because phenotypic variation, regardless of its cause, occurs within the relatively specific space of possibilities allowed by development. Second, we show that selection for genetic evolvability results in the evolution of adaptive plasticity and <jats:italic>vice versa</jats:italic>. This linkage is essentially symmetric but, unlike genetic evolvability, the selective gains of plasticity are often substantial on short, including within-lifetime, timescales. Accordingly, we show that selection for phenotypic plasticity is, in general, the most efficient and results in the rapid evolution of high genetic evolvability. Thus, without overlooking the fact that adaptive plasticity is itself a product of genetic evolution, this shows how plasticity can influence adaptive evolution and helps explain the genetic evolvability observed in biological systems.</jats:p>

Plasticity and evolutionary convergence in the locomotor skeleton of Greater Antillean Anolis lizards

“…As a result, locally adapted phenotypes should resemble environmentally induced phenotypes, a pattern supported by a meta-analysis of reciprocal transplant experiments in plants ( Radersma et al, 2020 ). The phenotype dimensions that are adaptively plastic may in fact have particularly high evolvability since theoretical and empirical studies suggest that those dimensions harbour particularly high levels of additive genetic variation ( Draghi and Whitlock, 2012 ; Noble et al, 2019 ; Brun-Usan et al, 2020 ). Thus, all three conditions above are fulfilled, making plasticity appear to take the lead in adaptive evolution ( Kovaka, 2019 ; Uller et al, 2020 ).…”

Developmental plasticity reveals hidden fish phenotypes and enables morphospace diversification

“…Plastic responses may constitute a relevant source of diversification and provide new possibilities for evolutionary processes (Gibson and Dworkin 2004; Brun‐Usan et al. 2020). Evaluation of hidden reaction norms ultimately fosters inference about evolutionary processes (Brun‐Usan et al.…”

“…Evaluation of hidden reaction norms ultimately fosters inference about evolutionary processes (Brun‐Usan et al. 2020).…”

Evolution of the locomotor skeleton in Anolis lizards reflects the interplay between ecological opportunity and phylogenetic inertia

“…Yet, the results are intelligible if evolution on the Greater Antilles had persistent effects on the lizards' developmental and behavioral biology, thereby imposing a bias on their future evolution following re-colonization of the mainland. Theoretical models of evolvability have demonstrated that strong selection for certain combinations of traits can promote the evolution of developmental interactions that make those traits vary together despite the genetic change being random [61][62][63] (reviewed in ref. 13 ).…”