Reproductive activity triggers accelerated male mortality and decreases lifespan: genetic and gene expression determinants in Drosophila

Abstract

Reproduction and aging evolved to be intimately associated. Experimental selection for early-life reproduction drives the evolution of decreased longevity in Drosophila whereas experimental selection for increased longevity leads to changes in reproduction. Although life history theory offers hypotheses to explain these relationships, the genetic architecture and molecular mechanisms underlying reproduction-longevity associations remain a matter of debate. Here we show that mating triggers accelerated mortality in males and identify hundreds of genes that are modulated upon mating in the fruit fly Drosophila melanogaster. Interrogation of genome-wide gene expression in virgin and recently mated males revealed coherent responses, with biological processes that are upregulated (testis-specific gene expression) or downregulated (metabolism and mitochondria-related functions) upon mating. Furthermore, using a panel of genotypes from the Drosophila Synthetic Population Resource (DSPR) as a source of naturally occurring genetic perturbation, we uncover abundant variation in longevity and reproduction-induced mortality among genotypes. Genotypes displayed more than fourfold variation in longevity and reproduction-induced mortality that can be traced to variation in specific segments of the genome. The data reveal individual variation in sensitivity to reproduction and physiological processes that are enhanced and suppressed upon mating. These results raise the prospect that variation in longevity and age-related traits could be traced to processes that coordinate germline and somatic function.

JNK signaling triggers spermatogonial dedifferentiation during chronic stress to maintain the germline stem cell pool in the Drosophila testis

“…We wondered whether males always housed with (and presumably mating with) females could force GSCs in the testis to cope with a higher demand for sperm production and thus accelerate the age-related reduction of the GSC pool. We note that while mating is a normal physiological event, it is stressful as mating significantly decreases both male and female lifespans ( Branco et al, 2017 ; Fowler and Partridge, 1989 ). However, little is known about the effects of mating on the GSC pool in males.…”

Selecting on age of female reproduction affects lifespan in both sexes and age-dependent reproductive effort in female (but not male) Ceratitis cosyra

“…A previous study supports this idea, showing that C. cosyra has a particularly long lifespan among other tephritid flies (Malod et al 2020a). Nevertheless, in C. capitata courting has a direct cost on male lifespan (Papadopoulos et al 2010), and in D. melanogaster reproductive activity alters gene expression in males, which then results in reduced lifespan (Branco et al 2017). Therefore, further investigations are needed to determine how selection on age of female reproduction affects male lifespan in mated individuals.…”

Gene expression changes in male accessory glands during ageing are accompanied by reproductive decline in Drosophila melanogaster

“…While most males might not reach such high age in the wild, senescence in the wild may also proceed faster than under laboratory conditions (Kawasaki, Brassil, Brooks, & Bonduriansky, ), putting our results within the range possibly observed in the wild. Keeping males as virgins during ageing results in a somewhat artificial state, but previous research demonstrated that males experience faster reproductive senescence when constantly kept with mates (Branco et al., ; Prowse & Partridge, ). Therefore, we conclude that our study if anything underestimates age effects on male reproduction and SFP gene expression.…”

“…We hypothesized that a change in expression (most likely a decline with age) for a particular SFP gene should be mirrored in relevant reproductive traits. SFP production might cease with age in virgin males due to a full storage of SFPs; thus, we used unmated and recently mated males to estimate the ability of males to increase gene expression after mating (Bertram et al., ; Branco, Schilling, Silkaitis, Dowling, & Lemos, ; DiBenedetto et al., ; Herndon et al., ; Monsma et al., ). A decrease in gene expression in old virgin males could be the result of a full complement of SFPs or of a functional decline in the AGs.…”