The Drosophila Post-mating Response: Gene Expression and Behavioral Changes Reveal Perdurance and Variation in Cross-Tissue Interactions

Abstract

Examining cross-tissue interactions is important for understanding physiology and homeostasis. In animals, the female gonad produces signaling molecules that act distally. We examine gene expression in Drosophila melanogaster female head tissues in 1) virgins without a germline compared to virgins with a germline, 2) post-mated females with and without a germline compared to virgins, and 3) post-mated females mated to males with and without a germline compared to virgins. In virgins, the absence of a female germline results in expression changes in genes with known roles in nutrient homeostasis. At one-and three-day(s) post-mating, genes that change expression are enriched with those that function in metabolic pathways, in all conditions. We systematically examine female post-mating impacts on sleep, food preference and re-mating, in the strains and time points used for gene expression analyses and compare to published studies. We show that post-mating, gene expression changes vary by strain, prompting us to examine variation in female re-mating. We perform a genome-wide association study that identifies several DNA polymorphisms, including four in/near Wnt signaling pathway genes. Together, these data reveal how gene expression and behavior in females are influenced by cross-tissue interactions, by examining the impact of mating, fertility, and genotype.

Investigation of Drosophila fruitless neurons that express Dpr/DIP cell adhesion molecules

“…Males display an elaborate courtship ritual that includes chasing the female, tapping her with his leg, and production of song with wing vibration (reviewed in Greenspan and Ferveur, 2000 ). The female decides whether she will mate and then, if mated, displays post-mating behaviors that include egg laying, changes in diet, and changes in receptivity to courtship (see Laturney and Billeter, 2014 ; Aranha and Vasconcelos, 2018 ; Newell et al, 2020 ).…”

Gene Expression and Alternative Splicing Dynamics Are Perturbed in Head Transcriptomes of Heterospecifically Mated Females

“…We demonstrate that the female postmating response is a complex process that involves the general female physiology as well as strong tissue-speci c transcriptional changes with variation in strength and direction [38]. By implementing an integrated transcriptional analysis in head tissues of mated females between D. mojavensis and D. arizonae, we were able to reveal previously unknown roles played by DE, AS and IR, and how these dynamics are integrated through functional specializations within the female postmating response.…”

“…6b). These pathways are all associated with nutrient homeostasis in brains and some of their metabolic functions have been previously detected in conspeci c mating experiments in D. melanogaster [28,38]. Physiological functions associated with these speci c amino acids include energy balance in brain tissues (i.e.…”

“…In fact, some of the mating-activated genes that we found in female heads are associated with functional pathways previously reported in different tissues and species. Proteolytic pathways for example, are within the most common and strongly activated genes that are part of the female response, found in both reproductive tissues and whole female bodies [10,38,70]. However, this is a complex reproductive response, given that a great part of the male ejaculate is also composed of a diverse cocktail of both proteases and their inhibitors [2].…”

“…We detected several biosynthetic pathways associated with the production of speci c amino acids important for nutrient homeostasis such as carnitine, threonine, and leucine. Although such pathways are not directly classi ed as behavioral or reproductive, some of their metabolic functions have been previously detected in conspeci c experiments in D. melanogaster [28,38]. These networks regulate energy balance [39,40] and nutritional uptake in brain tissues [41], and have been directly linked to several postcopulatory behaviors, including circadian rhythms [42,43], nutrient sensing, exploratory behavior for speci c nutrient source, consumption and posterior oviposition [26,27,75,76].…”