Extreme Y chromosome polymorphism corresponds to five male reproductive morphs

Abstract

Sex chromosomes form once recombination is halted between the X and Y chromosomes. This loss of recombination quickly depletes Y chromosomes of functional content and genetic variation, which is thought to severely limit their potential to generate adaptive diversity. We examined Y diversity in Poecilia parae, where males occur as one of five discrete morphs, all of which shoal together in natural populations where morph frequency has been stable for over 50 years. Each morph utilizes different complex reproductive strategies, and differ dramatically from each other in color, body size, and mating behavior. Remarkably, morph phenotype is passed perfectly from father to son, indicating there are five Y haplotypes segregating in the species, each of which encodes the complex male morph characteristics. Using linked-read sequencing on multiple P. parae females and males of all five morphs from natural populations, we found that the genetic architecture of the male morphs evolved on the Y chromosome long after recombination suppression had occurred with the X. Comparing Y chromosomes between each of the morphs revealed that although the Ys of the three minor morphs that differ predominantly in color are highly similar, there are substantial amounts of unique genetic material and divergence between the Ys of the three major morphs that differ in reproductive strategy, body size and mating behavior. Taken together, our results reveal the extraordinary ability of evolution to overcome the constraints of recombination loss to generate extreme diversity resulting in five discrete Y chromosomes that control complex reproductive strategies. Significance StatementThe loss of recombination on the Y chromosome is thought to limit the adaptive potential of this unique genomic region. Despite this, we describe an extraordinary case of Y chromosome adaptation in Poecilia parae. This species contains five co-occurring male morphs, all of which are Y-linked, and which differ in reproductive strategy, body size, coloration, and mating behavior. The five Y-linked male morphs of P. parae evolved after recombination was halted on the Y, resulting in five unique Y chromosomes within one species. Our results reveal the surprising magnitude to which non-recombining regions can generate adaptive diversity and have important implications for the evolution of sex chromosomes and the genetic control of sex-linked diversity.