Juvenile Hormone Suppresses Resistance to Infection in Mated Female Drosophila melanogaster

Abstract

Summary Hormonal signaling provides metazoans with the ability to regulate development, growth, metabolism, immune defense, and reproduction in response to internal and external stimuli. The use of hormones as central regulators of physiology makes them prime candidates for mediating allocation of resources to competing biological functions (i.e. hormonal pleiotropy) [1]. In animals, reproductive effort often results in weaker immune responses (e.g. [2–4]) and this reduction is sometimes linked to hormone signaling (see [5–7]). In the fruit fly, Drosophila melanogaster, mating and the receipt of male seminal fluid proteins results in reduced resistance to a systemic bacterial infection [8, 9]. Here, we evaluate whether the immunosuppressive effect of reproduction in female D. melanogaster is attributable to the endocrine signal juvenile hormone (JH), which promotes the development of oocytes and the synthesis and deposition of yolk protein [10, 11]. Previous work has implicated JH as immunosuppressive [12, 13], and the male seminal fluid protein Sex Peptide (SP) activates JH biosynthesis in female D. melanogaster after mating [14]. We find that transfer of SP activates synthesis of JH in the mated female, which in turn suppresses resistance to infection through the receptor germ cell-expressed (gce). We find that mated females are more likely to die from infection, suffer higher pathogen burdens, and are less able to induce their immune responses. All of these deficiencies are rescued when JH signaling is blocked. We argue that hormonal signaling is important for regulating immune system activity and, more generally, for governing trade-offs between physiological processes.

Plasticity in male mating behavior modulates female life history in fruit flies

“…Although sex peptide on its own appeared to have no detectable effect on female longevity, it may be that other Acps transferred during mating mediate the harmful effects of mating such as those related to stimulating reproduction (Bretman and Fricke 2019). Given that, in our trials, we detected no significant difference in the average number of matings between females exposed to males housed either alone or with rivals, it is likely that the differences we observed in female longevity are due to variation in the total amount of some Acps donated during each mating, or due to variation in other factors such as increased behavioral harassment, risk of transmitting infection, or weaker immune response to infection (Schwenke and Lazzaro 2017). Future studies should continue to investigate the individual and cumulative effects of different Acps to determine their effects on female postmating phenotypes.…”

Molecular insights into post‐mating immune response in a fish with internal fertilization

“…The down‐regulation of some components of the immune system due to the ejaculate coming in contact with the FRT has been found also in other species, such as humans (Clavert, Cranz, & Bollack, 1990), fruit flies (Schwenke & Lazzaro, 2017), pigs and chickens (Atikuzzaman et al, 2015, 2017). This immune suppression effect may be a means for females to temporarily tolerate non‐self cells (sperm) to maximize the number of sperm reaching sperm storage and fertilization sites.…”

Seasonal Dynamics and Starvation Impact on the Gut Microbiome of Urochordate Ascidian Halocynthia roretzi

“…In addition, it seems that ascidian gut microorganisms could directly synthesize some plant-type and insect-type hormones, such as salicylic acid, stearidonic acid, juvenile hormone I, podecdysone B, Iloprost, Nicotinamide. Those plant hormones could induce the wound defense against diseases [55,56], and those insect hormones were involved in improving chemical defense and immunity [57][58][59][60].…”