Affiliations: 1) Division of Basic Sciences, Fred Hutchinson cancer research center, Seattle, Washington, United States of America; 2) Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America
Keywords: l. evo-devo; a. spermatogenesis
Most eukaryotes deploy histones for genome packaging functions. However, many animal species accomplish tighter packaging of genomes in sperm using short, positively charged proteins, called sperm nuclear basic proteins (SNBPs). Although histones are ancient and highly conserved, SNBP repertoires have independent evolutionary origins, differ dramatically across animal lineages, and evolve rapidly in mammalian lineages. Here, we leveraged the sequencing of many Drosophila species’ genomes to perform detailed phylogenomic and genetic analyses of SNBP genes. SNBP genes independently arose in Drosophila species via duplications of HMG (high mobility group) DNA-binding proteins. We found that 11 of 13 SNBP genes have higher protein evolution rates (dN/dS) than 95% of D. melanogaster genes. McDonald–Kreitman tests revealed that five SNBP genes have evolved under positive selection in the D. melanogaster lineage. Surprisingly, we found that the evolutionary conservation of SNBPs is not correlated with functional importance. Several ancestral, strictly retained SNBP genes are dispensable for male fertility in D. melanogaster, whereas two recently evolved SNBPs are essential for fertility. Moreover, SNBP genes necessary for fertility in D. melanogaster have been lost in other Drosophila species. To study the evolution of SNBPs, we ectopically express orthologs of one essential SNBP in D. melanogaster and found they express at different stages. Our result suggests that this SNBP might acquire function in mature sperm post-individualization and become essential. Moreover, we found extensive duplication of protamine genes across Drosophila species, with recurrent expansions of these duplications (>70%) on sex chromosomes. Our population genetic and phylogenetic analyses highlight that one X-linked SNBP amplification in D. mauritiana is under recurrent positive selection. However, the same amplification is independently lost and does not show the signature of positive selection in two sister species of D. mauritiana. These results indicate that sex chromosome-linked SNBP duplicates may be involved in either inducing or suppressing X-versus-Y meiotic drive. Our analyses suggest that the rapid evolution of SNBPs might be a universal phenomenon in animals and partly driven by genetic conflicts during spermatogenesis.