Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms

Roberta Bergero*, Jim Gardner, Beth Bader, Lengxob Yong, Deborah Charlesworth

*Corresponding author for this work

Research output: Contribution to journalArticle

13 Citations (Scopus)

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.
Original languageEnglish
Pages (from-to)6924-6931
Number of pages7
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number14
Early online date20 Mar 2019
DOIs
Publication statusPrint publication - 2 Apr 2019
Externally publishedYes

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