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Edited by Michael Lynch, Arizona State University, Tempe, AZ, and approved February 19, 2019 (received for review October 31, 2018)
Significance
Sexual dimorphism is common in animals and often involves mutations that improve one sex but harm the opposite sex. However, very little empirical evidence exists about such conflicts and their evolution, including sex chromosome evolution. We report genetic and genomic analyses in a fish, the guppy, whose males have variable, bright coloration patterns that are beneficial during courtship but increase predation, therefore harming females. We found that genetic recombination events are strongly restricted to chromosome tips in males, but not females, and that this recombination difference between the sexes may have evolved recently in the guppy lineage. This sex difference ensures that male beneficial mutations are rarely transmitted to females, explaining their observed enrichment on the guppy’s male-determining chromosome.
Abstract
It is often stated that polymorphisms for mutations affecting fitness of males and females in opposite directions [sexually antagonistic (SA) polymorphisms] are the main selective force for the evolution of recombination suppression between sex chromosomes. However, empirical evidence to discriminate between different hypotheses is difficult to obtain. We report genetic mapping results in laboratory-raised families of the guppy (Poecilia reticulata), a sexually dimorphic fish with SA polymorphisms for male coloration genes, mostly on the sex chromosomes. Comparison of the genetic and physical maps shows that crossovers are distributed very differently in the two sexes (heterochiasmy); in male meiosis, they are restricted to the termini of all four chromosomes studied, including chromosome 12, which carries the sex-determining locus. Genome resequencing of male and female guppies from a population also indicates sex linkage of variants across almost the entire chromosome 12. More than 90% of the chromosome carrying the male-determining locus is therefore transmitted largely through the male lineage. A lack of heterochiasmy in a related fish species suggests that it originated recently in the lineage leading to the guppy. Our findings do not support the hypothesis that suppressed recombination evolved in response to the presence of SA polymorphisms. Instead, a low frequency of recombination on a chromosome that carries a male-determining locus and has not undergone genetic degeneration has probably facilitated the establishment of male-beneficial coloration polymorphisms.
Footnotes
- ↵1To whom correspondence should be addressed. Email: r.bergero{at}ed.ac.uk.
Author contributions: R.B. and D.C. designed research; R.B., J.G., B.B., and L.Y. performed research; L.Y. contributed new reagents/analytic tools; R.B. and D.C. analyzed data; and R.B. and D.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession no. PRJEB22221). Genotyping data have been deposited in the Dryad Digital Repository (https://doi.org/10.5061/dryad.70bs72s).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1818486116/-/DCSupplemental.
Published under the PNAS license.
- aInstitute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3LF, United Kingdom;
- bCentre for Ecology and Conservation, University of Exeter, Penryn, Falmouth, TR10 9FE Cornwall, United Kingdom
Edited by Michael Lynch, Arizona State University, Tempe, AZ, and approved February 19, 2019 (received for review October 31, 2018)
Significance
Sexual dimorphism is common in animals and often involves mutations that improve one sex but harm the opposite sex. However, very little empirical evidence exists about such conflicts and their evolution, including sex chromosome evolution. We report genetic and genomic analyses in a fish, the guppy, whose males have variable, bright coloration patterns that are beneficial during courtship but increase predation, therefore harming females. We found that genetic recombination events are strongly restricted to chromosome tips in males, but not females, and that this recombination difference between the sexes may have evolved recently in the guppy lineage. This sex difference ensures that male beneficial mutations are rarely transmitted to females, explaining their observed enrichment on the guppy’s male-determining chromosome.
Abstract
It is often stated that polymorphisms for mutations affecting fitness of males and females in opposite directions [sexually antagonistic (SA) polymorphisms] are the main selective force for the evolution of recombination suppression between sex chromosomes. However, empirical evidence to discriminate between different hypotheses is difficult to obtain. We report genetic mapping results in laboratory-raised families of the guppy (Poecilia reticulata), a sexually dimorphic fish with SA polymorphisms for male coloration genes, mostly on the sex chromosomes. Comparison of the genetic and physical maps shows that crossovers are distributed very differently in the two sexes (heterochiasmy); in male meiosis, they are restricted to the termini of all four chromosomes studied, including chromosome 12, which carries the sex-determining locus. Genome resequencing of male and female guppies from a population also indicates sex linkage of variants across almost the entire chromosome 12. More than 90% of the chromosome carrying the male-determining locus is therefore transmitted largely through the male lineage. A lack of heterochiasmy in a related fish species suggests that it originated recently in the lineage leading to the guppy. Our findings do not support the hypothesis that suppressed recombination evolved in response to the presence of SA polymorphisms. Instead, a low frequency of recombination on a chromosome that carries a male-determining locus and has not undergone genetic degeneration has probably facilitated the establishment of male-beneficial coloration polymorphisms.
- crossing over
- sexual antagonism
- sex chromosomes
- guppies
- genetic maps
Footnotes
- ↵1To whom correspondence should be addressed. Email: r.bergero{at}ed.ac.uk.
Author contributions: R.B. and D.C. designed research; R.B., J.G., B.B., and L.Y. performed research; L.Y. contributed new reagents/analytic tools; R.B. and D.C. analyzed data; and R.B. and D.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession no. PRJEB22221). Genotyping data have been deposited in the Dryad Digital Repository (https://doi.org/10.5061/dryad.70bs72s).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1818486116/-/DCSupplemental.
Published under the PNAS license.
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Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms
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