Pleiotropy increases parallel selection signatures during adaptation from standing genetic variation
The phenomenon of parallel evolution, whereby similar genomic and phenotypic changes occur across replicated pairs of populations or species, is widely studied. Nevertheless, the determining factors of parallel evolution remain poorly understood. Theoretical studies have proposed that pleiotropy, th...
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eLife Sciences Publications Ltd
2025-04-01
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| author | Wei-Yun Lai Sheng-Kai Hsu Andreas Futschik Christian Schlötterer |
| author_facet | Wei-Yun Lai Sheng-Kai Hsu Andreas Futschik Christian Schlötterer |
| author_sort | Wei-Yun Lai |
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| description | The phenomenon of parallel evolution, whereby similar genomic and phenotypic changes occur across replicated pairs of populations or species, is widely studied. Nevertheless, the determining factors of parallel evolution remain poorly understood. Theoretical studies have proposed that pleiotropy, the influence of a single gene on multiple traits, is an important factor. In order to gain a deeper insight into the role of pleiotropy for parallel evolution from standing genetic variation, we characterized the interplay between parallelism, polymorphism, and pleiotropy. The present study examined the parallel gene expression evolution in 10 replicated populations of Drosophila simulans, which were adapted from standing variation to the same new temperature regime. The data demonstrate that the parallel evolution of gene expression from standing genetic variation is positively correlated with the strength of pleiotropic effects. The ancestral variation in gene expression is, however, negatively correlated with parallelism. Given that pleiotropy is also negatively correlated with gene expression variation, we conducted a causal analysis to distinguish cause and correlation and evaluate the role of pleiotropy. The causal analysis indicated that both direct (causative) and indirect (correlational) effects of pleiotropy contribute to parallel evolution. The indirect effect is mediated by historic selective constraint in response to pleiotropy. This results in parallel selection responses due to the reduced standing variation of pleiotropic genes. The direct effect of pleiotropy is likely to reflect a genetic correlation among adaptive traits, which in turn gives rise to synergistic effects and higher parallelism. |
| format | Article |
| id | doaj-art-7b6294bdebdc49eda6bca335b45fcc21 |
| institution | OA Journals |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-04-01 |
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| spelling | doaj-art-7b6294bdebdc49eda6bca335b45fcc212025-08-20T02:17:33ZengeLife Sciences Publications LtdeLife2050-084X2025-04-011310.7554/eLife.102321Pleiotropy increases parallel selection signatures during adaptation from standing genetic variationWei-Yun Lai0https://orcid.org/0000-0002-5101-8695Sheng-Kai Hsu1https://orcid.org/0000-0002-6942-7163Andreas Futschik2Christian Schlötterer3https://orcid.org/0000-0003-4710-6526Institut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria; Vienna Graduate School of Population Genetics, Vetmeduni Vienna, Vienna, AustriaInstitut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria; Vienna Graduate School of Population Genetics, Vetmeduni Vienna, Vienna, AustriaDepartment of Applied Statistics, Johannes Kepler University Linz, Linz, AustriaInstitut für Populationsgenetik, Vetmeduni Vienna, Vienna, AustriaThe phenomenon of parallel evolution, whereby similar genomic and phenotypic changes occur across replicated pairs of populations or species, is widely studied. Nevertheless, the determining factors of parallel evolution remain poorly understood. Theoretical studies have proposed that pleiotropy, the influence of a single gene on multiple traits, is an important factor. In order to gain a deeper insight into the role of pleiotropy for parallel evolution from standing genetic variation, we characterized the interplay between parallelism, polymorphism, and pleiotropy. The present study examined the parallel gene expression evolution in 10 replicated populations of Drosophila simulans, which were adapted from standing variation to the same new temperature regime. The data demonstrate that the parallel evolution of gene expression from standing genetic variation is positively correlated with the strength of pleiotropic effects. The ancestral variation in gene expression is, however, negatively correlated with parallelism. Given that pleiotropy is also negatively correlated with gene expression variation, we conducted a causal analysis to distinguish cause and correlation and evaluate the role of pleiotropy. The causal analysis indicated that both direct (causative) and indirect (correlational) effects of pleiotropy contribute to parallel evolution. The indirect effect is mediated by historic selective constraint in response to pleiotropy. This results in parallel selection responses due to the reduced standing variation of pleiotropic genes. The direct effect of pleiotropy is likely to reflect a genetic correlation among adaptive traits, which in turn gives rise to synergistic effects and higher parallelism.https://elifesciences.org/articles/102321PleiotropyD. simulansgene expressionparallel evolutionexperimental evolutionpolygenic adaptation |
| spellingShingle | Wei-Yun Lai Sheng-Kai Hsu Andreas Futschik Christian Schlötterer Pleiotropy increases parallel selection signatures during adaptation from standing genetic variation eLife Pleiotropy D. simulans gene expression parallel evolution experimental evolution polygenic adaptation |
| title | Pleiotropy increases parallel selection signatures during adaptation from standing genetic variation |
| title_full | Pleiotropy increases parallel selection signatures during adaptation from standing genetic variation |
| title_fullStr | Pleiotropy increases parallel selection signatures during adaptation from standing genetic variation |
| title_full_unstemmed | Pleiotropy increases parallel selection signatures during adaptation from standing genetic variation |
| title_short | Pleiotropy increases parallel selection signatures during adaptation from standing genetic variation |
| title_sort | pleiotropy increases parallel selection signatures during adaptation from standing genetic variation |
| topic | Pleiotropy D. simulans gene expression parallel evolution experimental evolution polygenic adaptation |
| url | https://elifesciences.org/articles/102321 |
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