Josway, S. | bioRxiv Science

bioRxiv2019

A novel role for Eip74EF in male reproduction in promoting sperm elongation and male fecundity

Spermatozoa are the most morphologically variable cell type, yet little is known about genes controlling natural variation in sperm shape. Drosophila fruit flies have the longest sperm known, which are evolving under postcopulatory sexual selection, driven by sperm competition and cryptic female choice. Long sperm outcompete short sperm but primarily when females have a long seminal receptacle (SR), the primary sperm storage organ. Thus, selection on sperm length is mediated by SR length, and the two traits are coevolving across the Drosophila lineage, driven by a genetic correlation and fitness advantage of long sperm and long SR genotypes in both males and females. Ecdysone induced protein 74EF (Eip74EF) is expressed during post-meiotic stages of spermatogenesis, when spermatid elongation occurs, and we found that it is rapidly evolving under positive selection in Drosophila. Hypomorphic knockout of the E74A isoform leads to shorter sperm but does not affect SR length, suggesting that E74A may be involved in promoting spermatid elongation but is not a genetic driver of male-female coevolution. We also found that E74A knockout has opposing effects on fecundity in males and females, with an increase in fecundity for males but a decrease in females, consistent with its documented role in oocyte maturation. Our results suggest a novel function of Eip74EF in spermatogenesis and demonstrates that this gene influences both male and female reproductive success. We speculate on possible roles for E74A in spermatogenesis and male reproductive success. RESEARCH HIGHLIGHTSEip74EF promotes oocyte maturation in Drosophila. We found evidence that it also promotes sperm elongation in males, but at a cost to male fecundity. Mutant males have shorter sperm but have higher reproductive success, while females have reduced fecundity.

genetics↗

bioRxiv2019

Costs and benefits of giant sperm and sperm storage organs in Drosophila melanogaster

In the Drosophila lineage, both sperm and the primary female sperm storage organ, the seminal receptacle (SR), may reach extraordinary lengths. In D. melanogaster, long SRs bias fertilization toward long sperm during the displacement stage of sperm competition. This sperm-SR interaction, together with a genetic correlation between the traits, suggests that the coevolution of exaggerated sperm and SR lengths may be driven by Fisherian runaway selection. To further understand the costs and benefits of long sperm and SR genotypes in both sexes, we measured male and female fitness in inbred lines of D. melanogaster derived from four populations previously selected for long sperm, short sperm, long SRs, or short SRs. We specifically asked: do long SRs impose costs or benefits on the females that bear them? Do genotypes that generate long sperm in males impose a fitness cost on females sharing those genotypes? Is long sperm an honest indicator of male viability and associated with increased fitness? And finally, are the benefits of long sperm restricted to competitive fertilization success, or do long-sperm males also have increased mating success and fecundity in single matings? We found that both sexes have increased longevity in long sperm and long SR genotypes, with fewer reproduction-related benefits and evidence for trade-offs in males, compared to females. Our results suggest that sperm length and SR length are both indicators of increased viability.

evolutionary biology↗

bioRxiv2016

Pervasive Antagonistic Interactions Among Hybrid Incompatibility Loci

Species barriers, expressed as hybrid inviability and sterility, are often due to epistatic interactions between divergent loci from two lineages. Theoretical models indicate that the strength, direction, and complexity of these genetic interactions can strongly affect the expression of interspecific reproductive isolation and the rates at which new species evolve. Nonetheless, empirical analyses have not quantified the frequency with which loci are involved in interactions affecting hybrid fitness, and whether these loci predominantly interact synergistically or antagonistically, or preferentially involve loci that have strong individual effects on hybrid fitness. We systematically examined the prevalence of interactions between pairs of short chromosomal regions from one species (Solanum habrochaites) co-introgressed into a heterospecific genetic background (Solanum lycopersicum). We used lines containing pairwise combinations of 15 chromosomal segments from S. habrochaites crossed into the background of S. lycopersicum (i.e., 95 double introgression lines). We compared the strength of hybrid incompatibility (either pollen sterility or seed sterility) expressed in each double introgression line to the expected additive effect of its two component single introgressions. We found that: epistasis was common among co-introgressed regions; epistastic effects for hybrid dysfunction were overwhelmingly antagonistic (i.e., double hybrids were less unfit than expected from additive single introgression effects); and, epistasis was substantially more prevalent in pollen fertility compared to seed fertility phenotypes. Together, these results indicate that higher-order interactions frequently contribute to postzygotic sterility barriers in these species. This pervasive epistasis leads to the decoupling of the patterns of accumulation of isolation loci and isolation phenotypes, and is expected to attenuate the rate of accumulation of hybrid infertility among lineages over time (i.e., giving diminishing returns as more reproductive isolation loci accumulate). This decoupling effect might also explain observed differences between pollen and seed fertility in their fit to theoretical predictions of the accumulation of isolation loci, including the snowball effect.\n\nAUTHOR SUMMARYA characteristic feature of new species is their inability to produce fertile or viable hybrids with other lineages. This post-zygotic reproductive isolation is caused by dysfunctional interactions between genes that have newly evolved changes in the diverging lineages. Whether these interactions occur between pairs of divergent alleles, or involve more complex networks of genes, can have strong effects on how rapidly reproductive isolation--and therefore new species--evolve. The complexity of these interactions, however, is poorly understood in empirical systems. We examined the fertility of hybrids that carried one or two chromosomal regions from a close relative, finding that hybrids with two of these heterospecific regions were frequently less sterile than would be expected from the joint fitness of hybrids that have the same regions singly. This less-than-additive effect on hybrid sterility was widespread (observed in 20% of pairwise combinations), and especially pronounced for male sterility. We infer that genes contributing to male sterility form a more tightly connected network than previously thought, implying that reproductive isolation is evolving by incremental dysfunction of complex interactions rather than by independent pairwise incompatibilities. We use simulations to illustrate these expected patterns of accumulation of reproductive isolation when it involves highly interconnected gene networks.

evolutionary biology↗