INTRODUCTION
Phenotypic plasticity is defined as the capacity of a genotype to
produce alternative phenotypes depending on the environmental context it
is exposed to (Gause, 1947; Levins, 1963; Bradshaw, 1965). In
particular, adaptive phenotypic plasticity allows organisms to adjust
their phenotype in order to cope with contrasting environmental
conditions (Demmig-Adams et al. , 2008). Whether adaptive
phenotypic plasticity can evolve or not depends on its associated costs
and is contingent on a certain degree of environmental predictability
(DeWitt, Sih and Wilson, 1998; Reed et al. , 2010; Botero et
al. , 2015). More specifically, plasticity in reproductive behaviour and
strategies (reproductive plasticity ) is a central component of
individual fitness, particularly so in the face of high spatio-temporal
heterogeneity in socio-sexual contexts (Dewsbury, 1982; Gage, 1995;
Kokko and Rankin, 2006; Rebar, Barbosa and Greenfield, 2019). For this
reason, reproductive plasticity is often considered to be a key
determinant of population responses to rapid environmental change
(Agrawal, 2001; Charmantier et al. , 2008).
Across the animal kingdom, sexual selection is generally male-biased
(Bateman, 1948; Janicke et al. , 2016), and because relatively
high variance in reproductive success increases the adaptive value of
phenotypic plasticity, males can be expected to display high plasticity
in reproductive behaviour (Bretman, Gage and Chapman, 2011). Male
plastic responses to intra-sexual competition are rather well documented
across distant taxa (delBarco-Trillo and Ferkin, 2004; Aragón, 2009;
Bretman, Gage and Chapman, 2011). For instance, males of different
species have been shown to strategically adjust mating duration
(Bretman, Fricke and Chapman, 2009; Mazzi et al. , 2009), mate
guarding behaviour (Carazo et al. 2007), sperm transfer (Gage, 1991;
Gage and Baker, 1991), and even seminal fluid protein transfer (Wigbyet al. , 2009) in response to the socio-sexual environment (e.g.
sperm competition risk and/or intensity cues; Shifferman, 2012).
Ultimately, high intra-sexual competition can even lead to the evolution
of adaptive alternative strategies in reproductive behaviour
(Hurtado-Gonzales and Uy, 2010).
Recently an empirical study reported that, in Drosophila
melanogaster , short-term perception of female cues ahead of access to
reproduction (termed sexual perception ) can increase male
reproductive performance in a competitive environment (Corbel et
al. , 2022). This plastic response to female cues seems to be adaptive,
and may explain previously documented survival and reproductive costs
linked with sexual perception in males (Gendron et al. , 2014;
Harvanek et al. , 2017; García-Roa, Serra and Carazo, 2018).
Interestingly, this study found that sexual perception benefits tended
to be rapidly induced (noticeable as early as over the first 24 hours
following access to females), and spanned across the lifespan of males.
Given that male plastic responses to sexual perception can magnify the
opportunity for selection (Carazo et al. , 2017; García-Roa, Serra
and Carazo, 2018; Corbel et al. , 2022) and may help explain
ageing in response to sensory stimuli (Gendron et al. , 2014;
Harvanek et al. , 2017), identifying the mechanisms responsible
for such male plasticity could provide valuable information.
Here, we aimed to investigated the short-term fitness consequences of
sexual perception in detail. To this aim, we studied the effect of
sexual perception on several short-term pre- and post-copulatory fitness
components in D. melanogaster males. Similarly to other
polygamous species with high intra-sexual competition, pre-copulatory
fitness of males of this species is modulated by male-male competition
and female choice, both of which contribute to determine male mating
success in a competitive scenario (Dow and Von Schilcher, 1975;
Andersson, 1994; Arbuthnott et al. , 2017). Post-copulatory male
fitness, in turn, is largely driven by sperm competitiveness (mostly
sperm-offense, see Fricke et al. , 2010; Simmons and Fitzpatrick,
2012). Additionally, male manipulation of female reproductive behaviour
via the transfer of accessory gland proteins within the seminal fluid is
known to benefit male post-copulatory fertilisation success (Chenet al. , 1988; Aigaki et al. , 1991; Chapman, 2001; Chapmanet al. , 2003; Liu and Kubli, 2003; Fiumera, Dumont and Clark,
2005; Ravi Ram and Wolfner, 2007; Fricke et al. , 2009; Hopkinset al. , 2019). In fact, there is ample evidence that males
strategically adjust their seminal fluid protein transfer depending on
the socio-sexual environment context they experience (see for instance
Wigby et al. , 2009; Hopkins et al. , 2019). Thus, in order
to fully capture the effects of sexual perception on short-term fitness,
we exposed virgin males to female cues for a period of 24 hours (while
preventing mating) and subsequently measured the following male fitness
components: a) mating success, b) mating latency and duration, c) sperm
competitiveness, and d) ejaculate effects on female receptivity and
oviposition rate.