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).