Ancient inversion polymorphisms associate with sexually selected traits across natural guppy populations
- 1Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, Canada
Abstract
Understanding the distribution, frequency, and long-term persistence of chromosomal inversions in natural populations is key to understanding population evolution and adaptive processes. Inversions often span multiple genes, are subject to strong selective pressures and can affect complex traits. Here, we used an unbiased method to identify inversions in guppies from three different Trinidadian rivers with paired high- and low-predation populations which differ in a wide range of morphological, behavioural and life-history traits. We identified 22 inversions, ranging in age from 1 to 6 million years, which are widespread across the genome and predate the colonisation of each river. We were able to verify the breakpoints for all but one of these inversions using linked reads. We find three inversions that are significantly associated with local adaptation syndromes in high- versus low-predation populations, however, none are reciprocally fixed throughout all three replicate rivers. Additionally, we observe seven additional inversions maintained in all three rivers without evidence of local adaptation. Simulations reveal that the level of inversion polymorphism that we observe is far greater than expected under a neutral model. We observed a significant overlap between polymorphic inversions and loci previously implicated in male ornament pattern variation in guppies, suggesting that negative frequency-dependent selection due to female preference for male pattern novelty explains the maintenance of inversion polymorphisms. Overall, our results show the role of sexual selection in the long-term maintenance of inversion polymorphisms, and an interplay between sexual and natural selection in frequency dynamics.
Genomic inversions spanning many genes can persist for millions of years. This study of Trinidadian guppy populations reveals how both ecological conditions and mate choice help maintain this hidden layer of genomic diversity, linking sexual selection with long-term genome evolution.
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BibTeX
@article{lin2026ancient,
title = {{Ancient inversion polymorphisms associate with sexually selected traits across natural guppy populations}},
author = {Yuying Lin and Wouter van der Bijl and Judith E. Mank},
journal = {PLOS Biology},
year = {2026},
month = sep,
doi = {10.1371/journal.pbio.3004024},
url = {https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3004024},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Ancient inversion polymorphisms associate with sexually selected traits across natural guppy populations
AU - Yuying Lin
AU - Wouter van der Bijl
AU - Judith E. Mank
PY - 2026
DA - 2026/09/23
JO - PLOS Biology
DO - 10.1371/journal.pbio.3004024
UR - https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3004024
AB - Understanding the distribution, frequency, and long-term persistence of chromosomal inversions in natural populations is key to understanding population evolution and adaptive processes. Inversions often span multiple genes, are subject to strong selective pressures and can affect complex traits. Here, we used an unbiased method to identify inversions in guppies from three different Trinidadian rivers with paired high- and low-predation populations which differ in a wide range of morphological, behavioural and life-history traits. We identified 22 inversions, ranging in age from 1 to 6 million years, which are widespread across the genome and predate the colonisation of each river. We were able to verify the breakpoints for all but one of these inversions using linked reads. We find three inversions that are significantly associated with local adaptation syndromes in high- versus low-predation populations, however, none are reciprocally fixed throughout all three replicate rivers. Additionally, we observe seven additional inversions maintained in all three rivers without evidence of local adaptation. Simulations reveal that the level of inversion polymorphism that we observe is far greater than expected under a neutral model. We observed a significant overlap between polymorphic inversions and loci previously implicated in male ornament pattern variation in guppies, suggesting that negative frequency-dependent selection due to female preference for male pattern novelty explains the maintenance of inversion polymorphisms. Overall, our results show the role of sexual selection in the long-term maintenance of inversion polymorphisms, and an interplay between sexual and natural selection in frequency dynamics. Genomic inversions spanning many genes can persist for millions of years. This study of Trinidadian guppy populations reveals how both ecological conditions and mate choice help maintain this hidden layer of genomic diversity, linking sexual selection with long-term genome evolution.
SN - 1545-7885
ER -