Expansion and loss of sperm nuclear basic protein genes in <i>Drosophila</i> correspond with genetic conflicts between sex chromosomes.

Abstract

Many animal species employ sperm nuclear basic proteins (SNBPs) or protamines to package sperm genomes tightly. SNBPs vary across animal lineages and evolve rapidly in mammals. We used a phylogenomic approach to investigate SNBP diversification in <i>Drosophila</i> species. We found that most SNBP genes in <i>Drosophila melanogaster</i> evolve under positive selection except for genes essential for male fertility. Unexpectedly, evolutionarily young SNBP genes are more likely to be critical for fertility than ancient, conserved SNBP genes. For example, <i>CG30056</i> is dispensable for male fertility despite being one of three SNBP genes universally retained in <i>Drosophila</i> species. We found 19 independent SNBP gene amplification events that occurred preferentially on sex chromosomes. Conversely, the <i>montium</i> group of <i>Drosophila</i> species lost otherwise-conserved SNBP genes, coincident with an X-Y chromosomal fusion. Furthermore, SNBP genes that became linked to sex chromosomes via chromosomal fusions were more likely to degenerate or relocate back to autosomes. We hypothesize that autosomal SNBP genes suppress meiotic drive, whereas sex-chromosomal SNBP expansions lead to meiotic drive. X-Y fusions in the <i>montium</i> group render autosomal SNBPs dispensable by making X-versus-Y meiotic drive obsolete or costly. Thus, genetic conflicts between sex chromosomes may drive SNBP rapid evolution during spermatogenesis in <i>Drosophila</i> species.