Memory of social experience affects female fecundity via perception of fly deposits

Abstract

Background Animals can exhibit remarkable reproductive plasticity in response to their social surroundings, with profound fitness consequences. The presence of same-sex conspecifics can signal current or future expected competition for resources or mates. Plastic responses to elevated sexual competition caused by exposure to same-sex individuals have been well-studied in males. However, much less is known about such plastic responses in females, whether this represents sexual or resource competition, or if it leads to changes in investment in mating behaviour and/or reproduction. Here, we used Drosophila melanogaster to measure the impact of experimentally varying female exposure to other females prior to mating on fecundity before and after mating. We then deployed physical and genetic methods to manipulate the perception of different social cues and sensory pathways and reveal the potential mechanisms involved. Results The results showed that females maintained in social isolation prior to mating were significantly more likely to retain unfertilised eggs before mating, but to show the opposite and lay significantly more fertilised eggs in the 24h after mating. More than 48h of exposure to other females was necessary for this social memory response to be expressed. Neither olfactory nor visual cues were involved in mediating fecundity plasticity—instead, the relevant cues were perceived through direct contact with the non-egg deposits left behind by other females. Conclusions The results demonstrate that females show reproductive plasticity in response to their social surroundings and can carry this memory of their social experience forward through mating. Comparisons of our results with previous work show that the nature of female plastic reproductive responses and the cues they use differ markedly from those of males. The results emphasise the deep divergence in how each sex realises its reproductive success.

Socially plastic responses in females are robust to evolutionary manipulations of adult sex ratio and adult nutrition

“…2A; Fig. S3A-C) as has previously been reported in wild type females [31]. However, the magnitude of the plasticity in the fecundity responses of females to their pre-mating social environment was not significantly different across any of the sex ratio or diet regimes (table S1).…”

“…It is possible that the general culturing procedures used to maintain the sex ratio and nutritional regimes used here conferred consistent benefits of plasticity in mating latency. This could be due to greater predictability of the conditions experienced by the experimental evolution regimes (specified densities, timings of culturing stages and non overlapping generations) in comparison to normal cage culture used for the wild type flies used in previous studies, in which this effect was not observed [31, 52]. We do not yet know the drivers of plasticity in mating latency.…”

“…For example, in D. melanogaster , mated females are more aggressive towards rival females than are virgins [29, 30] and this aggression evolves to become stronger in populations maintained over time under strong female bias [30]. Female fecundity is also surprisingly plastic, and varies according to the pre- and post-mating social environment [31] [27]. For example, females maintained in same sex conspecific groups prior to mating lay significantly fewer eggs after mating than those kept alone, with the detection of deposits left by other females being key to the assessment of the female’s social environment [31].…”

“…Female fecundity is also surprisingly plastic, and varies according to the pre- and post-mating social environment [31] [27]. For example, females maintained in same sex conspecific groups prior to mating lay significantly fewer eggs after mating than those kept alone, with the detection of deposits left by other females being key to the assessment of the female’s social environment [31]. These findings show that both sexes can respond plastically according to the level of potential competition experienced.…”

“…Here we used these same lines to test how the plastic fecundity responses of females to conspecifics evolve in response to the evolutionary manipulation of sexual selection and resource levels in adults. We asked whether the plastic responses in female fecundity [31] had evolved in experimental evolution regimes selected under male-biased (MB), equal sex (ES) and female-biased (FB) adult sex ratios maintained under high or low quality adult diets. The specific predictions were (i) that a history of elevated competition among females (in FB regimes) would select for increasingly sensitive plastic fecundity responses to the presence of conspecifics, which would (ii) be magnified under poor nutritional resource regimes.…”