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Predicting the prevalence of genetic trade-offs among adaptive substitutions

Connallon, Tim ; Czuppon, Peter ; Olito, Colin LU ; Goedert, Debora ; Kokko, Hanna ; Nava-Bolaños, Angela ; Nilén, Sofie LU orcid ; Svensson, Erik I. LU orcid ; Zwoinska, Martyna and Dutoit, Ludovic , et al. (2025) In Evolution 79(7). p.1243-1255
Abstract

Genetic trade-offs - which occur when variants that are beneficial in some contexts of natural selection are harmful in others - can influence a wide range of evolutionary phenomena, from the maintenance of genetic variation to the evolution of aging and sex differences. An extensive body of evolutionary theory has focused on the consequences of such trade-offs, and recent analyses of Fisher's geometric model have further quantified the expected proportion of new mutations that exhibit trade-offs. However, the theory remains silent regarding the prevalence of trade-offs among the variants that contribute to adaptation. Here, we extend Fisher's geometric model to predict the prevalence of trade-offs among the adaptive mutations that... (More)

Genetic trade-offs - which occur when variants that are beneficial in some contexts of natural selection are harmful in others - can influence a wide range of evolutionary phenomena, from the maintenance of genetic variation to the evolution of aging and sex differences. An extensive body of evolutionary theory has focused on the consequences of such trade-offs, and recent analyses of Fisher's geometric model have further quantified the expected proportion of new mutations that exhibit trade-offs. However, the theory remains silent regarding the prevalence of trade-offs among the variants that contribute to adaptation. Here, we extend Fisher's geometric model to predict the prevalence of trade-offs among the adaptive mutations that become established or fixed in a population. We consider trade-offs between sexes, habitats, fitness components, and temporally fluctuating environments. In all 4 scenarios, trade-off alleles are consistently under-represented among established relative to new beneficial mutations - an effect that arises from the greater susceptibility of trade-off alleles to genetic drift. Adaptation during a population size decline exacerbates this deficit of trade-offs among established mutations, whereas population expansions dampen it. Consequently, threatened populations should primarily adapt using unconditionally beneficial alleles, while invasive populations are more prone to adaptation using variants that exhibit trade-offs.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
adaptation, pleiotropy, sexual conflict, trade-offs
in
Evolution
volume
79
issue
7
pages
13 pages
publisher
Wiley-Blackwell
external identifiers
  • pmid:40127022
  • scopus:105011205636
ISSN
0014-3820
DOI
10.1093/evolut/qpaf061
language
English
LU publication?
yes
additional info
Publisher Copyright: © 2025 The Author(s). Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE).
id
59e233fc-0abc-40e3-81d5-ca1c264da611
date added to LUP
2025-12-15 14:26:45
date last changed
2025-12-17 16:15:13
@article{59e233fc-0abc-40e3-81d5-ca1c264da611,
  abstract     = {{<p>Genetic trade-offs - which occur when variants that are beneficial in some contexts of natural selection are harmful in others - can influence a wide range of evolutionary phenomena, from the maintenance of genetic variation to the evolution of aging and sex differences. An extensive body of evolutionary theory has focused on the consequences of such trade-offs, and recent analyses of Fisher's geometric model have further quantified the expected proportion of new mutations that exhibit trade-offs. However, the theory remains silent regarding the prevalence of trade-offs among the variants that contribute to adaptation. Here, we extend Fisher's geometric model to predict the prevalence of trade-offs among the adaptive mutations that become established or fixed in a population. We consider trade-offs between sexes, habitats, fitness components, and temporally fluctuating environments. In all 4 scenarios, trade-off alleles are consistently under-represented among established relative to new beneficial mutations - an effect that arises from the greater susceptibility of trade-off alleles to genetic drift. Adaptation during a population size decline exacerbates this deficit of trade-offs among established mutations, whereas population expansions dampen it. Consequently, threatened populations should primarily adapt using unconditionally beneficial alleles, while invasive populations are more prone to adaptation using variants that exhibit trade-offs.</p>}},
  author       = {{Connallon, Tim and Czuppon, Peter and Olito, Colin and Goedert, Debora and Kokko, Hanna and Nava-Bolaños, Angela and Nilén, Sofie and Svensson, Erik I. and Zwoinska, Martyna and Dutoit, Ludovic and Ruzicka, Filip}},
  issn         = {{0014-3820}},
  keywords     = {{adaptation; pleiotropy; sexual conflict; trade-offs}},
  language     = {{eng}},
  month        = {{07}},
  number       = {{7}},
  pages        = {{1243--1255}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Evolution}},
  title        = {{Predicting the prevalence of genetic trade-offs among adaptive substitutions}},
  url          = {{http://dx.doi.org/10.1093/evolut/qpaf061}},
  doi          = {{10.1093/evolut/qpaf061}},
  volume       = {{79}},
  year         = {{2025}},
}