Recombination rate and efficiency of linked selection in small and large stickleback populations
- 1Area of Ecology and Biodiversity, School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China.
- 2Ecological Genetics Research Unit, Research Program in Organismal and Evolutionary Biology, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland.
Abstract
Population genetic theory predicts that natural selection will be more efficient in large than small populations because genetic drift reduces the efficiency of selection in small populations. Small populations adapting to new environments can also be expected to evolve higher recombination rates to facilitate adaptation as well as to dissociate and purge harmful mutations. We tested these hypotheses (1) by investigating differences in the strength of association between nucleotide diversity (π) and recombination rate across the genomes of nine-spined sticklebacks (Pungitius pungitius) from four small freshwater (mean Ne ≈ 7 096) and four large marine (mean Ne = 376 828) populations, as well as (2) by comparing recombination rates between small and large populations using population specific linkage maps. We found the predicted positive correlation of π with recombination rate from all but the smallest freshwater populations, suggesting prevalent linked selection even after accounting for variation in GC/CpG content, and gene density. Mean recombination rates did not differ between freshwater and marine populations, except that the smallest Ne freshwater population exhibited significantly elevated recombination rate. Exploratory GWAS analyses suggested a possible polygenic basis for recombination rate. These results suggest an important role for linked selection in reducing π in low recombination regions especially in large populations. Moreover, as predicted by theory, at least one of the small freshwater populations appears to have evolved a higher recombination rate than its marine ancestors. Author summary: We investigated how population size influences the efficiency of natural selection across the genome. Evolutionary theory suggests that natural selection is more effective in large populations, while random genetic drift (a process of chance) should override selection in smaller populations. We also hypothesized that small populations might evolve higher recombination rates (the “shuffling” of genetic material) to help them adapt to new environments and separate beneficial mutations from harmful ones. To test these ideas, we analysed genomic data from eight wild stickleback populations, comparing large marine populations with much smaller freshwater ones. Our results confirmed that the link between genetic diversity and recombination is stronger in populations with larger estimated effective population sizes, where selection plays a dominant role. In contrast, this relationship was weakened in small populations subject to strong genetic drift. Interestingly, one of the freshwater populations with the smallest estimated effective population size exhibited a very high recombination rate, supporting the idea that recombination rate can evolve rapidly to help populations to adapt to new environments and separate beneficial mutations from harmful ones. Finally, we found that recombination rate is not likely to be controlled by a single gene, but likely a complex trait influenced by many genes in different parts of the genome.
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BibTeX
@article{wang2026recombination,
title = {{Recombination rate and efficiency of linked selection in small and large stickleback populations}},
author = {Hongbo Wang and Chaowei Zhang and Kerry Reid and Juha Merilä},
journal = {PLOS Genetics},
year = {2026},
month = oct,
doi = {10.1371/journal.pgen.1012335},
url = {https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1012335},
note = {CC BY},
}
RIS
TY - JOUR
TI - Recombination rate and efficiency of linked selection in small and large stickleback populations
AU - Hongbo Wang
AU - Chaowei Zhang
AU - Kerry Reid
AU - Juha Merilä
PY - 2026
DA - 2026/10/28
JO - PLOS Genetics
DO - 10.1371/journal.pgen.1012335
UR - https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1012335
AB - Population genetic theory predicts that natural selection will be more efficient in large than small populations because genetic drift reduces the efficiency of selection in small populations. Small populations adapting to new environments can also be expected to evolve higher recombination rates to facilitate adaptation as well as to dissociate and purge harmful mutations. We tested these hypotheses (1) by investigating differences in the strength of association between nucleotide diversity (π) and recombination rate across the genomes of nine-spined sticklebacks (Pungitius pungitius) from four small freshwater (mean Ne ≈ 7 096) and four large marine (mean Ne = 376 828) populations, as well as (2) by comparing recombination rates between small and large populations using population specific linkage maps. We found the predicted positive correlation of π with recombination rate from all but the smallest freshwater populations, suggesting prevalent linked selection even after accounting for variation in GC/CpG content, and gene density. Mean recombination rates did not differ between freshwater and marine populations, except that the smallest Ne freshwater population exhibited significantly elevated recombination rate. Exploratory GWAS analyses suggested a possible polygenic basis for recombination rate. These results suggest an important role for linked selection in reducing π in low recombination regions especially in large populations. Moreover, as predicted by theory, at least one of the small freshwater populations appears to have evolved a higher recombination rate than its marine ancestors. Author summary: We investigated how population size influences the efficiency of natural selection across the genome. Evolutionary theory suggests that natural selection is more effective in large populations, while random genetic drift (a process of chance) should override selection in smaller populations. We also hypothesized that small populations might evolve higher recombination rates (the “shuffling” of genetic material) to help them adapt to new environments and separate beneficial mutations from harmful ones. To test these ideas, we analysed genomic data from eight wild stickleback populations, comparing large marine populations with much smaller freshwater ones. Our results confirmed that the link between genetic diversity and recombination is stronger in populations with larger estimated effective population sizes, where selection plays a dominant role. In contrast, this relationship was weakened in small populations subject to strong genetic drift. Interestingly, one of the freshwater populations with the smallest estimated effective population size exhibited a very high recombination rate, supporting the idea that recombination rate can evolve rapidly to help populations to adapt to new environments and separate beneficial mutations from harmful ones. Finally, we found that recombination rate is not likely to be controlled by a single gene, but likely a complex trait influenced by many genes in different parts of the genome.
SN - 1553-7404
SN - 1553-7390
ER -