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

Brun-Usan, Miguel LU ; Rago, Alfredo LU ; Thies, Christoph ; Uller, Tobias LU and Watson, Richard A. (2021) In BMC Ecology and Evolution 21(1).
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... (More)

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.

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author
; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Adaptation, Genotype-phenotype-map, Mechanistic developmental models, Parental effects, Phenotypic plasticity, Plasticity-led evolution
in
BMC Ecology and Evolution
volume
21
issue
1
article number
205
publisher
Springer
external identifiers
  • pmid:34800979
  • scopus:85119506734
ISSN
2730-7182
DOI
10.1186/s12862-021-01936-0
language
English
LU publication?
yes
additional info
Publisher Copyright: © 2021, The Author(s).
id
a648910a-07f7-4669-b7d8-a943f58fc835
date added to LUP
2021-12-08 21:43:30
date last changed
2024-04-20 17:21:21
@article{a648910a-07f7-4669-b7d8-a943f58fc835,
  abstract     = {{<p>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.</p>}},
  author       = {{Brun-Usan, Miguel and Rago, Alfredo and Thies, Christoph and Uller, Tobias and Watson, Richard A.}},
  issn         = {{2730-7182}},
  keywords     = {{Adaptation; Genotype-phenotype-map; Mechanistic developmental models; Parental effects; Phenotypic plasticity; Plasticity-led evolution}},
  language     = {{eng}},
  number       = {{1}},
  publisher    = {{Springer}},
  series       = {{BMC Ecology and Evolution}},
  title        = {{Development and selective grain make plasticity 'take the lead' in adaptive evolution}},
  url          = {{http://dx.doi.org/10.1186/s12862-021-01936-0}},
  doi          = {{10.1186/s12862-021-01936-0}},
  volume       = {{21}},
  year         = {{2021}},
}