How Did The Guppy Y Chromosome Evolve?

The sex chromosome pairs of many species do not undergo genetic recombination, unlike the autosomes. It has been proposed that the suppressed recombination results from natural selection favouring close linkage between sex-determining genes and mutations on this chromosome with advantages in one sex, but disadvantages in the other (these are called sexually antagonistic mutations). No example of such selection leading to suppressed recombination has been described, but populations of the guppy display sexually antagonistic mutations (affecting male coloration), and would be expected to evolve suppressed recombination. In extant close relatives of the guppy, the Y chromosomes have suppressed recombination, and have lost all the genes present on the X (this is called genetic degeneration). However, the guppy Y occasionally recombines with its X, despite carrying sexually antagonistic mutations. We describe evidence that a new Y evolved recently in the guppy, from an X chromosome like that in these relatives, replacing the old, degenerated Y, and explaining why the guppy pair still recombine. The male coloration factors probably arose after the new Y evolved, and have already evolved expression that is confined to males, a different way to avoid the conflict between the sexes.Author summary Our manuscript reports new findings concerning the long-studied the guppy XY pair, which has remained somewhat mystifying. We show that it can be understood as a case of a recent sex chromosome turnover event in which an older, highly degenerated Y chromosome was lost, and creation of a new sex chromosome from the ancestral X. This chromosome acquired a male-determining factor, possibly by a mutation in (or a duplication of) a previously X-linked gene, or (less likely) by movement of an ancestral Y-linked maleness factor onto the X. We relate the findings to theoretical models of such events, and argue that the proposed change was free from factors thought to impede such turnovers. The change resulted in the intriguing situation where the X chromosome is old and the Y is much younger, and we discuss some other species where a similar change seems likely to have occurred.