DISCUSSION
Overall, we found no conclusive evidence that the lifetime fitness benefits of sexual perception reported by previous studies are due to effects on male short-term fitness components. We found no differences in mating success or mating latency between control males and female-exposed males (Fig. 1a), showing that males do not derive pre-copulatory benefits from short-term sexual perception. Given that, in our assays, focal males of either treatment (female-exposed vs control) competed directly against each other over a female, these results represent the net outcome of simultaneous pre-copulatory male-male competition and female choice in a biologically relevant scenario (Dukas, 2020). We did find some evidence that sexual perception resulted in significantly increased mating duration (Fig. 1b), such that female-exposed males mated on average for 1’05” longer than control males (i.e. a 5.54 % increase). In D. melanogaster , mating duration is mainly driven by males (MacBean and Parsons, 1967), and longer matings often translate into higher reproductive success for males (Bretman, Fricke and Chapman, 2009; Wigby et al. , 2009). Thus, this difference could be biologically meaningful. However, this difference was flagged as a potential false discovery due to inflation of experiment-wise type I error rate (i.e. Benjamini and Hochberg 1995), and should hence be interpreted with extreme caution. Empirical evidence shows that, in D. melanogaster , sperm transfer is completed after only a few minutes, and that longer matings do not yield higher sperm transfer (Gilchrist and Partridge, 1997). With that regard, we did not find significant differences in lifetime reproductive success between treatment females and control males (Fig. 3a), which could imply that female-exposed males do not transfer more of sperm to females than control males (i.e. given that these females were only mated once, to either males). In fact, previous research has linked the fitness benefits associated to longer matings to the transfer of non-sperm components that increase immediate oviposition rate in females (see Chapman et al. , 2003; Chapman and Davies, 2004; Wigby et al. , 2009). However, we found no significant differences in daily reproductive output of females over the 7 days following mating with female-exposed vs control males (Fig. 2). In promiscuous species, female remating rate is often under high sexual conflict and, while males benefit from females not remating and thus utilizing all the sperm transferred during copulation (i.e. avoiding post-copulatory competition), females can benefit from remating with several males (e.g. through increased offspring genetic diversity; Yasui, 1998; Arnqvist and Rowe, 2005). We found no difference in remating latency between treatment females and control females (Fig. 1c). This suggests that males do not transfer higher amounts of seminal fluid protein mediating female receptivity as a consequence of sexual perception prior to access to mating. Altogether, the fact that the difference observed in mating duration did not result in a net fitness advantage supports the idea that this increase was not biologically relevant, or that it is a case of false discovery.
In polygamous species with high mating rates, sperm competitiveness can be an important driver of individual fitness (Singh, Singh and Hoenigsberg, 2002; Firman and Simmons, 2011; Schnakenberg, Siegal and Bloch Qazi, 2012). Sperm competitiveness is often measured as the paternity share that a male achieves when competing against another male, within the female reproductive tract. The paternity share of the first of two males to mate with the female will define his sperm defense abilities, whereas the paternity share of the second male will define his sperm offense abilities (Boorman and Parker, 1976). InD. melanogaster, sperm-offence abilities correlate more strongly with relative lifetime reproductive success than sperm-defense abilities (Fricke et al. , 2010). We thus investigated whether sexual perception could affect sperm-offense abilities, and found no significant difference between males shortly exposed to female cues prior to access to reproduction and control males (Fig.3b). It is worth noting that, given the very high baseline level of paternity share of control males (ca. 95.17% ± 0.85 SEM), our study may lack power to pick up any effects of sexual perception on P2 , as that the magnitude of any such expected effect must be low.
The fact that the females over which males competed in our study were virgin could contribute to explain our results. In this species, virgin females are considerably less choosy than mated females (Bateman, 1948). As such, the use of relatively unselective females could have masked differences in male pre-copulatory competitiveness. Additionally,D. melanogaster males are known to adjust their ejaculate content depending on female mating status (Lüpold et al. , 2011; Sirot, Wolfner and Wigby, 2011). Consequently, female mating status could play a role in male plasticity in ejaculate content induced by sexual perception, and ultimately male post-copulatory performance.
In conclusion, we explored an array of pre- and post-copulatory short-term male fitness components and found no indication that any of the components measured are affected by brief sexual perception. While this means that the mechanisms leading to enhanced reproductive performance of males following sexual perception are still unidentified, our results suggest that these mechanisms do not involve improvement of males’ short-term fitness proxies. This corroborates the previously mentioned idea that sexual perception benefits build up along the span of males’ life (several weeks after initial perception of female cues) to yield a net lifetime fitness gain (Corbel et al. , 2022).