H2020Individual fellowship2018–2020

PLEVOCON · Pleiotropy and Evolutionary Constraint

Horizon 2020 — Marie Skłodowska-Curie Actions

Duration
2018-06-01 → 2020-09-20
EU contribution
€187,420
Participants
1
Scheme
MSCA-IF

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Results in brief

Pleiotropy and Evolutionary Constraint

Pleiotropy, or the influence of a single locus on multiple traits, is thought to be an important mechanism of evolutionary constraint and could be an important deterministic factor during adaptive evolution. Theoretical models and work in quantitative genetics has long suggest that pleiotropy strongly impacts the probability that a given locus will be used in adaptation. Despite these theoretical predictions, we have lacked explicit tests of how pleiotropy contributes to evolutionary predictability. The overarching goal of this project was to test whether pleiotropy is a source of evolutionary constraint that underlies the predictability of evolutionary responses. Specifically, we sought to identify the genomic loci associated with repeated divergence between stickleback adapted to different habitats and test whether pleiotropy levels explained the repeated use of the same loci during adaptation. Illumina sequence data from multiple independent ecotype pairs of threespine stickleback were analyzed to estimate the genome-wide patterns of genetic divergence. We found that a large portion of the genome was evolving in a repeatable manner among independently derived population pairs of stickleback. Furthermore, ecologically relevant traits mapped to these repeatedly diverged genomic regions, and ecological similarity was an important predictor of the magnitude of parallel evolution. Using two proxies for pleiotropy, gene connectivity and number of traits with mapped QTL, we estimated the relationship between the level of pleiotropy and probability of parallel evolution. We found that parallel genomic regions contained genes with significantly more pleiotropy than uniquely evolving (non-parallel) regions. The increased mean pleiotropy of parallel windows could not be explained by other genomic factors, as there was no significant difference in mean gene count, mutation or recombination rates between parallel and non-parallel windows. Interestingly, although non-parallel windows contained genes that were on average less connected and influencing fewer mapped traits than parallel windows, these windows also tended to contain the gene that were the most pleiotropic. Taken together, our findings are consistent with the idea that low or intermediate levels of pleiotropy may be beneficial for adaptation, and that it is only at high levels that pleiotropy becomes constraining. These findings may help to inform our expectations about the genetic architecture of rapid evolutionary responses in nature or in agricultural and medical settings.

Data: CORDIS, © European Union

Project objective

When organisms adapt to new environments, are the genetic mechanisms that underlie evolutionary trajectories predictable or stochastic? Recently, genomic studies have provided tantalizing clues that the genetic mechanisms that underlie evolutionary trajectories may be more constrained and deterministic than previously thought. Theoretical work has suggested that pleiotropy, or the influence of a single gene on multiple traits, might be an important deterministic factor during adaptive evolution. Specifically, high levels of pleiotropy are predicted to decrease the frequency with which a locus is used over the course of evolution because it is much more likely that mutations in that locus will have negative fitness consequences. Despite these theoretical predictions, however, we lack explicit tests of how pleiotropy contributes to evolutionary predictability. The objective of the PLEVOCON project is to test whether pleiotropy is a source of evolutionary constraint that underlies the predictability of evolutionary responses. The threespine stickleback (Gasterosteus aculeatus) is an ideal system in which to test whether pleiotropy is a source of evolutionary constraint. Crucially, these small fish have independently and repeatedly adapted to diverse freshwater habitats in the northern hemisphere since the retreat of the glaciers 12,000 years ago. Stickleback living in similar habitats have evolved similar phenotypes, providing an opportunity to ask whether the same genes underlie adaptation to these habitats, and whether genes that are repeatedly used for adaptation have lower levels of pleiotropy. I will utilize the existing wealth of genetic and genomic resources in this system and develop innovative statistical approaches to carry out the first genome-wide test of whether pleiotropy is a source of constraint in evolutionary responses.

Original text from CORDIS.

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Data: CORDIS, © European Union