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

Miguel Brun-Usan,Richard A Watson,Alfredo Rago,Tobias Uller,Christoph Thies

doi:10.1186/s12862-021-01936-0

Miguel Brun-Usan, Richard A Watson + Show 3 more

Open Access

https://doi.org/10.1186/s12862-021-01936-0

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Abstract

BackgroundBiological 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.ResultsTo 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.ConclusionsWithout 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.

Highlights

Biological evolution exhibits an extraordinary capability to adapt organisms to their environments
Genetic evolvability could itself be a product of past evolution [7,8,9], but the idea that natural selection would be able to improve genetic evolvability is problematic because the immediate selective gains of responding adaptively to random genetic change are small on short timescales [9, 10]
The regulatory interactions of this gene regulatory networks (GRN) are encoded in the Ng x Ng matrix B, whose elements Bik represent the effect of gene k on the transcription of gene i

Summary

Introduction

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 pheno‐ typic variation in which natural selection can act. Genetic evolvability could itself be a product of past evolution [7,8,9], but the idea that natural selection would be able to improve genetic evolvability is problematic because the immediate selective gains of responding adaptively to random genetic change are small on short timescales [9, 10] Another suggestion is that the high genetic evolvability is acquired through the capability of organisms to rapidly adjust to their environment during their lifetime [11]. We seek to better understand whether phenotypic plasticity can help to explain genetic evolvability without overlooking the fact that adaptive plasticity is itself a product of genetic evolution [14]

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