Development and selective grain make plasticity 'take the lead' in adaptive evolution

Abstract

Background 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 in which natural selection can act. 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. Results 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 perturbation 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 vice versa. 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 can be effective in promoting the evolution of high genetic evolvability. Conclusions Without overlooking the fact that adaptive plasticity is itself a product of genetic evolution, we show how past selection for plasticity can exercise a disproportionate effect on genetic evolvability and, in turn, influence the course of adaptive evolution.

Beyond genotype‐phenotype maps: Toward a phenotype‐centered perspective on evolution

“…Such mechanistic, development‐based models can provide a causal understanding of the phenotypic consequences of changes in environmental variables, making it possible to construct an Environment‐Phenotype (EP) ‘map’ [Box‐2]. [ 1,33,39,60,61 ] Consider, for instance, the effect of temperature on the number and size of scutes in the turtle carapace. [ 62,63 ] Temperature typically increases cell division, suggesting that increases in temperature might lead to larger carapaces containing an increasing number of scutes.…”

“…Furthermore, each type of generative input is represented as an independent (i.e., orthogonal) axis whose values can be modified without affecting the others. Such an independence means that each type of input is irreducible to one another [ 61 ] , and that their values can be (at least theoretically) combined in many ways (i.e., {G 1 ,E 1 ,D 1 }, {G 1 ,E 1 ,D 2 }, … {G n ,E n ,D n }). The 3P‐map makes it easy to grasp why phenotypes and their variation depend on genes, environmental and epigenetic factors.…”

“…The 3P‐map makes it easy to grasp why phenotypes and their variation depend on genes, environmental and epigenetic factors. [ 61,69 ] Here, we emphasize four reasons for why this representation can be useful to address the role of development in evolution.…”

On the Origin of Phenotypic Plasticity

“…Since then, it 57 has been widely used to investigate how their structural and 58 functional properties change after evolution in static 20,22,23 59 or fluctuating 18,[24][25][26] environments. Only a few studies have 60 considered phenotypic plasticity by incorporating sensors into 61 the network [27][28][29][30] . These studies showed that the evolution 62 of phenotypic plasticity generates a correlation of phenotypic 63 variation between traits 27,29 and affects the amount of pheno-64 typic variation observed among populations encountering novel D R A F T changes (without changing genotype).…”

“…Only a few studies have 60 considered phenotypic plasticity by incorporating sensors into 61 the network [27][28][29][30] . These studies showed that the evolution 62 of phenotypic plasticity generates a correlation of phenotypic 63 variation between traits 27,29 and affects the amount of pheno-64 typic variation observed among populations encountering novel D R A F T changes (without changing genotype). In the following section, 87 we explain how a sensor gene is incorporated in the model of 88 Watson et al 18 and the other modifications we perform.…”