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Sexually antagonistic coevolution between the sex chromosomes of Drosophila melanogaster

Lund-Hansen, Katrine K. LU orcid ; Olito, Colin LU ; Morrow, Edward H. and Abbott, Jessica K. LU orcid (2021) In Proceedings of the National Academy of Sciences of the United States of America 118(8).
Abstract

Antagonistic interactions between the sexes are important drivers of evolutionary divergence. Interlocus sexual conflict is generally described as a conflict between alleles at two interacting loci whose identity and genomic location are arbitrary, but with opposite fitness effects in each sex. We build on previous theory by suggesting that when loci under interlocus sexual conflict are located on the sex chromosomes it can lead to cycles of antagonistic coevolution between them and therefore between the sexes. We tested this hypothesis by performing experimental crosses using Drosophila melanogaster where we reciprocally exchanged the sex chromosomes between five allopatric wild-type populations in a round-robin design. Disrupting... (More)

Antagonistic interactions between the sexes are important drivers of evolutionary divergence. Interlocus sexual conflict is generally described as a conflict between alleles at two interacting loci whose identity and genomic location are arbitrary, but with opposite fitness effects in each sex. We build on previous theory by suggesting that when loci under interlocus sexual conflict are located on the sex chromosomes it can lead to cycles of antagonistic coevolution between them and therefore between the sexes. We tested this hypothesis by performing experimental crosses using Drosophila melanogaster where we reciprocally exchanged the sex chromosomes between five allopatric wild-type populations in a round-robin design. Disrupting putatively coevolved sex chromosome pairs resulted in increased male reproductive success in 16 of 20 experimental populations (10 of which were individually significant), but also resulted in lower offspring egg-to-adult viability that affected both male and female fitness. After 25 generations of experimental evolution these sexually antagonistic fitness effects appeared to be resolved. To formalize our hypothesis, we developed population genetic models of antagonistic coevolution using fitness expressions based on our empirical results. Our model predictions support the conclusion that antagonistic coevolution between the sex chromosomes is plausible under the fitness effects observed in our experiments. Together, our results lend both empirical and theoretical support to the idea that cycles of antagonistic coevolution can occur between sex chromosomes and illustrate how this process, in combination with autosomal coadaptation, may drive genetic and phenotypic divergence between populations.

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author
; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Coevolution, Compensatory evolution, Interlocus sexual conflict, Sex chromosome evolution
in
Proceedings of the National Academy of Sciences of the United States of America
volume
118
issue
8
article number
e2003359118
publisher
National Academy of Sciences
external identifiers
  • scopus:85101191263
  • pmid:33602805
ISSN
0027-8424
DOI
10.1073/pnas.2003359118
language
English
LU publication?
yes
id
acf0ea06-d0b9-4335-a587-00ddaaa38038
date added to LUP
2021-03-09 10:49:03
date last changed
2024-06-13 08:07:43
@article{acf0ea06-d0b9-4335-a587-00ddaaa38038,
  abstract     = {{<p>Antagonistic interactions between the sexes are important drivers of evolutionary divergence. Interlocus sexual conflict is generally described as a conflict between alleles at two interacting loci whose identity and genomic location are arbitrary, but with opposite fitness effects in each sex. We build on previous theory by suggesting that when loci under interlocus sexual conflict are located on the sex chromosomes it can lead to cycles of antagonistic coevolution between them and therefore between the sexes. We tested this hypothesis by performing experimental crosses using Drosophila melanogaster where we reciprocally exchanged the sex chromosomes between five allopatric wild-type populations in a round-robin design. Disrupting putatively coevolved sex chromosome pairs resulted in increased male reproductive success in 16 of 20 experimental populations (10 of which were individually significant), but also resulted in lower offspring egg-to-adult viability that affected both male and female fitness. After 25 generations of experimental evolution these sexually antagonistic fitness effects appeared to be resolved. To formalize our hypothesis, we developed population genetic models of antagonistic coevolution using fitness expressions based on our empirical results. Our model predictions support the conclusion that antagonistic coevolution between the sex chromosomes is plausible under the fitness effects observed in our experiments. Together, our results lend both empirical and theoretical support to the idea that cycles of antagonistic coevolution can occur between sex chromosomes and illustrate how this process, in combination with autosomal coadaptation, may drive genetic and phenotypic divergence between populations.</p>}},
  author       = {{Lund-Hansen, Katrine K. and Olito, Colin and Morrow, Edward H. and Abbott, Jessica K.}},
  issn         = {{0027-8424}},
  keywords     = {{Coevolution; Compensatory evolution; Interlocus sexual conflict; Sex chromosome evolution}},
  language     = {{eng}},
  number       = {{8}},
  publisher    = {{National Academy of Sciences}},
  series       = {{Proceedings of the National Academy of Sciences of the United States of America}},
  title        = {{Sexually antagonistic coevolution between the sex chromosomes of Drosophila melanogaster}},
  url          = {{http://dx.doi.org/10.1073/pnas.2003359118}},
  doi          = {{10.1073/pnas.2003359118}},
  volume       = {{118}},
  year         = {{2021}},
}