Haploid selection drives new gene male germline expression.

ABSTRACT: New genes are a major source of novelties, and a disproportionate amount of them are known to show testis expression in later phases of male gametogenesis in different groups such as mammals and plants. Here, we propose that this enhanced expression is a consequence of haploid selection during the latter stages of male gametogenesis. Because emerging adaptive mutations will be fixed faster if their phenotypes are expressed by haploid rather than diploid genotypes, new genes with advantageous functions arising during this unique stage of development have a better chance to become fixed. To test this hypothesis, expression levels of genes of differing evolutionary age were examined at various stages of Drosophila spermatogenesis. We found, consistent with a model based on haploid selection, that new Drosophila genes are both expressed in later haploid phases of spermatogenesis and harbor a significant enrichment of adaptive mutations. Additionally, the observed overexpression of new genes in the latter phases of spermatogenesis was limited to the autosomes. Because all male cells exhibit hemizygous expression for X-linked genes (and therefore effectively haploid), there is no expectation that selection acting on late spermatogenesis will have a different effect on X-linked genes in comparison to initial diploid phases. Together, our proposed hypothesis and the analyzed data suggest that natural selection in haploid cells elucidates several aspects of the origin of new genes by explaining the general prevalence of their testis expression, and a parsimonious solution for new alleles to avoid being lost by genetic drift or pseudogenization.

SUBMITTER: Raices JB 

PROVIDER: S-EPMC6633266 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature