Biology subjects

Manier, M.

Publications and source records attributed to Manier, M..

4 recordsLinked to original sources

bioRxiv2021

Genetic coordination of sperm morphology and seminal fluid proteins promotes male reproductive success in Drosophila melanogaster

Spermatozoal morphology is highly variable both among and within species and in ways that can significantly impact fertilization success. In Drosophila melanogaster, paternity success depends on sperm length of both competing males and length of the females primary sperm storage organ. We found that genes upregulated in long sperm testes are enriched for lncRNAs and seminal fluid proteins (Sfps). Transferred in seminal fluid to the female during mating, Sfps are secreted by the male accessory glands (AG) and affect female remating rate, physiology, and behavior with concomitant advantages for male reproductive success. Despite being upregulated in long sperm testes, they have no known function in testis tissue. We found that Sex Peptide and ovulin (Acp26Aa) knockouts resulted in shorter sperm, suggesting that Sfps may regulate sperm length during spermatogenesis. However, knockout of AG function did not affect sperm length, suggesting that AG expression has no influence on spermatogenic processes. We also found that long sperm males are better able to delay female remating, suggesting higher Sfp expression in AG. These results might suggest that long sperm males have a double advantage in sperm competition by both delaying female remating, likely through transfer of more Sfps, and by resisting sperm displacement. However, we also found that this extra advantage does not necessarily translate to more progeny or higher paternity success. Thus, we found that multiple components of the ejaculate coordinate to promote male reproductive success at different stages of reproduction, but the realized fitness advantages in sperm competition are uncertain. Significance StatementThe ejaculate is comprised of sperm produced in the testis and seminal fluid primarily produced in the male accessory glands (AG). These complementary components are both critical for male reproductive success, but they are largely considered to be functionally, genetically, and developmentally independent. In a quest to understand genetic mechanisms of sperm length variation, we found that genes upregulated in long sperm testes are enriched for lncRNAs and seminal fluid proteins (Sfps). Knockout of two Sfps, Sex Peptide and ovulin, results in shorter sperm, though knockout of AG function has no effect. Moreover, long sperm males delay female remating longer. These results suggest sophisticated testis-AG coordination that amplifies male reproductive success, with implications for evolutionary integration of sexually selected traits.

genetics↗

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↗

bioRxiv2019

Two gut microbes are necessary and sufficient for normal cognition in Drosophila melanogaster

It is widely accepted that the gut microbiome can affect various aspects of brain function, including anxiety, depression, learning, and memory. However, we know little about how individual microbial species contribute to communication along the gut-brain axis. Vertebrate microbiomes are comprised of hundreds of species, making it difficult to systematically target individual microbes and their interactions. Here, we use Drosophila melanogaster as a simple model organism to tease apart individual and combined effects of gut microbes on cognition. We used an aversive phototactic suppression assay to show that two dominant gut commensals in our lab stock, Lactobacillus and Acetobacter, are necessary and sufficient for normal learning and short-term memory relative to flies with a conventional microbiome. We also demonstrate that microbes did not affect their hosts ability to detect the aversive learning stimulus (quinine), suggesting that our results were due to decreased cognition and not sensory deficits. We thus establish Drosophila as a model for elucidating mechanisms of gut-brain communication at the level of individual bacterial species.

animal behavior and cognition↗