Interactions between the sexual identity of the nervous system and the social environment mediate lifespan in Drosophila melanogaster

Abstract

Sex differences in lifespan are ubiquitous, but the underlying causal factors remain poorly understood. Inter- and intrasexual social interactions are well known to influence lifespan in many taxa, but it has proved challenging to separate the role of sex-specific behaviours from wider physiological differences between the sexes. To address this problem, we genetically manipulated the sexual identity of the nervous system—and hence sexual behaviour—in Drosophila melanogaster, and measured lifespan under varying social conditions. Consistent with previous studies, masculinization of the nervous system in females induced male-specific courtship behaviour and aggression, while nervous system feminization in males induced male–male courtship and reduced aggression. Control females outlived males, but masculinized female groups displayed male-like lifespans and male-like costs of group living. By varying the mixture of control and masculinized females within social groups, we show that male-specific behaviours are costly to recipients, even when received from females. However, consistent with recent findings, our data suggest courtship expression to be surprisingly low cost. Overall, our study indicates that nervous system-mediated expression of sex-specific behaviour per se—independent of wider physiological differences between the sexes, or the receipt of aggression or courtship—plays a limited role in mediating sex differences in lifespan.

Sex-specific transcriptomic responses to changes in the nutritional environment

“…Assuming that expression of these genes reflects reproductive investment, the fact that they do respond to the nutritional environment suggests that male reproductive strategies are maybe more subtle, and their investment more costly, than previously appreciated. This is plausible, as work on other insects has shown that the production of high quality sperm is costly [76] (but courtship activity does not appear to carry a significant cost, at least in fruit flies [77]).…”

Social environment drives sex and age-specific variation inDrosophila melanogastermicrobiome composition and predicted function

“…Social environments have multiple effects on individual health, including immune responses (1, 2), ageing and ultimately lifespan (3–5). Indeed meta-analyses show that adverse social environments are a health risk factor on a par with obesity and smoking (6).…”

“…Effects of social environments are complex. They are seen in animals not usually thought of as social, there are marked sex differences, and hence what constitutes a stressful social environment is not straightforward (1, 4, 5). For example, periods of social isolation can be beneficial even in gregarious species (7).…”

“…For example, periods of social isolation can be beneficial even in gregarious species (7). The mechanisms that translate information about the social environment into these effects are unclear, but it has been suggested that the microbiome (the community of microorganisms living symbiotically with a host) plays a role (5). Social impacts on microbiomes are expected given that close contact aids horizontal transmission of microbes (8, 9) and social partners will often have similar diets, a key driver of microbiome composition (10).…”

“…We chose to focus on social conditions to which males are particularly sensitive, therefore extrinsic effects of the social environment should affect both sexes equally but intrinsic effects would be seen to a greater extent in males. In adults, same-sex social contact has sex-specific impacts on actuarial and functional senescence (4, 5). Male lifespan is reduced disproportionately by the presence of same-sex cohabitants, especially when given an immune challenge (4), but both sexes can survive longer post-infection with certain bacteria if held with same-sex partners (1).…”