Sperm length correlates with the rapid evolution and turnover of male genes in bees

The evolution of eusociality is often preceded by a period of obligate monogamy followed by a shift to polyandry. This transition can have dramatic effects on sperm length evolution. Small monandrous colonies and large, polyandrous colonies tend to have long sperm while intermediates (e.g., communal bees) generally have intermediately sized sperm. As a result, sperm length is expected to correlate with genetic features associated with male traits and have implications for evolution in male social bees.  Here, we studied genes with sex-biased expression patterns across bee species with different colony sizes and mating systems. We used this novel dataset to explore the evolutionary consequences of sperm length selection on genomic evolution. First, selection for longer sperm increases male-biased expression compared to ancestral monandrous bees with short sperm. Second, we found selection for longer sperm promotes sexual conflict, which is expected to constrain the evolution of male reproductive traits. To overcome this constraint, it appears species with long sperm increase alternative splicing and expression in the male gonads to resolve conflict. Third, selection for longer sperm intensified selection, especially negative selection. Finally, we find sperm length and male-gonadal biased gene families exhibited elevated gene losses across Hymenoptera. Overall, these results suggest selection for longer sperm not only intensified selection of males, but drove the rapid evolution of male-gonadal expression patterns and gene sequences.