Genomic responses to mating signals

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You may not know whether 'love changes everything', but, scientifically speaking, the act of mating certainly does. Research focussed on the varied and inventive mating habits of invertebrates reveals the astonishing ways in which males can remodel the behaviour and physiology of the females with which they mate. This includes the transfer during mating by males of chemicals that go deep into female brains and nervous systems to alter behaviour, and those that effectively take over the female reproductive system. Small wonder then that females are sometimes resistant to such manipulations. Our recent work reveals just how global and sophisticated are the changes wrought upon females by mating males. We examined the responses of female fruitflies that mated with males that either did or did not transfer during mating a single ejaculate 'sex peptide' known to affect female sexual receptivity and egg laying. We examined both how messenger RNAs (mRNAs, that make gene products), and microRNAs (miRs, which sit on mRNAs and block them or target them for destruction) changed in females following receipt of sex peptide. We found many alterations to mRNAs, but what was really striking was the number of miRs that were different. This is consistent with the emerging general view that miRs have extremely important and widespread roles in regulating how genes work, with 20-30% of all genes (roughly 13,000 genes in the fruitfly) estimated as targets for miRs. Hence sex peptide sets in train global effects on female genomes not only at the level of DNA to RNA synthesis (transcription), but also on the rate at which RNA is translated (i.e. made into proteins). We are interested in SP because it has a 'swiss army knife' of functions and can alter the reproductive performance of both males and females. Remarkably, SP can significantly benefit the reproductive performance of males at the expense of that of females. This shows that SP plays a role in the battle of the sexes, where males can gain by maximising their returns from each mating even if that results in a decrease in the longer term reproductive prospects of their mates. SP benefits males because it decreases female sexual receptivity for several days and increases egg-laying. Hence males that transfer SP father more offspring than males that lack SP. However, females that receive elevated levels of SP suffer adverse consequences in the long term. The effects of SP are dependent on female diet and can be significantly altered, abolished or even reversed in sign under poor and good quality food. This research puts us in a timely position to address the following two fundamental questions: (1) to find out how male sex peptide intervenes in the female genome - which are the key genes that are targeted by miRs following receipt of sex peptide? and secondly - given that female diet is key to determining how much females are able to respond to sex peptide - (2) to examine how female genomes respond to sex peptide following both short- and long-term (evolutionary) changes in diet. The research is important because this is the first example we have where we can investigate the co-ordinated changes in both mRNAs and miRs to an external stimulus like the sex peptide that underlies important reproductive functions in both sexes. The fact that diet is also an important part of how females respond to sex peptide is also crucial as it allows us to test at the level of the genome SP responses following both short- and long-term alterations to diet. Our research will also therefore show miRs that change under different dietary conditions, which is important because diet is also a crucial determinant of lifespan.