Pre-maturation social experience affects female reproductive strategies and offspring quality in a highly polyandrous insect

Pre-maturation social experiences may affect post-maturation reproductive strategies of females, including mating preferences and investment in offspring. Whether pre-maturation social experiences affect other aspects of females’ reproductive strategies, including the number of accepted males and post-copulatory decisions, is still an open question. To address this question, we performed laboratory experiments using the highly polyandrous cricket Teleogryllus commodus. Previous studies showed that juvenile females reared in an acoustic environment with male calls of different rates (MIX) are more responsive to highly attractive calls than females reared in an environment with male calls of only high calling rates (HIGH). We exposed juvenile females to the same two acoustic environments (MIX and HIGH) and estimated the number of accepted males, time of spermatophore retention, and offspring quality. We found that the acoustic environment did not change the number of accepted males, indicating that the higher responsiveness shown in a previous study does not translate into high degree of polyandry. An increased number of mates reduced offspring quality, suggesting that polyandry is costly to females. Finally, when compared with females of the HIGH group, females of the MIX group retained spermatophores for shorter periods and produced higher quality offspring if mated with highly attractive males. This finding suggests that both the pre-maturation acoustic environment and the quality of the mates found by the adult females determine their post-copulatory decisions and eventually offspring quality. Taken together, our results indicate that both the pre- and post-mating strategies of females are subject to socially cued plasticity. SIGNIFICANCE STATEMENT: There is increasing evidence that pre-maturation experiences affect mating decisions of females after maturity, making them more or less selective. Both the pre-maturation social environment and the quality of potential mates found by an adult female may determine the number and quality of accepted males, which in turn may influence offspring quality. We experimentally tested this hypothesis using a highly polyandrous cricket species and showed that the pre-maturation acoustic environment does not affect the number and attractiveness of males accepted by the females. However, offspring quality was determined by an interaction between the pre-maturation acoustic environment and attractiveness of males accepted by the females. This result provides a link between the pre- and post-maturation social experience of a female and the quality of her offspring.