Introduction
Many animals exhibit plasticity in their reproductive behaviour and / or
reproductive investment in response to the other organisms around them,
allowing them to allocate resources across mating opportunities in order
to maximise lifetime reproductive success (Dewsbury 1982; Parker 1982;
Gage 1995; Wedell et al. 2002; Kokko and Rankin 2006; Rodriguez et al.
2013). However, in order for plasticity to be adaptive, cues that confer
accurate, reliable, and robust information on the current conditions
must be received (DeWitt et al. 1998; Auld et al. 2010). One way in
which the information conferred by environmental cues may be made more
robust is through the receipt of multi-component (complex) cues.
Redundancy among cue components can mean that even if one component is
lost or compromised, the overall information within any message can
remain intact (Johnstone 1996; Bro-Jorgensen 2010). This suggests that
receiving alternative combinations of cue components should elicit
equivalent phenotypic changes and equivalent associated fitness
benefits. However, redundancy among cue components may also be
incomplete, whereby separate cue components relay partially overlapping,
but not identical, information about the environment (Bretman et al.
2011b; Dore et al. 2018). In this scenario, altering the combination of
cue components to which an individual is exposed may result in subtle
effects on subsequent phenotypes, with associated fitness consequences.
Male Drosophila melanogaster express behavioural plasticity,
whereby individuals exposed to rival males will subsequently mate for
longer and increase their transfer of some seminal fluid proteins, in
comparison to males housed alone (Bretman et al. 2009; Wigby et al.
2009a). Extended matings following exposure to rivals are reported to be
associated with increased paternity share (Bretman et al. 2009).
However, exposure to rivals over a male’s whole lifetime results in the
expression of reproductive costs later in life (Bretman et al. 2009;
Bretman et al. 2013b). The behavioural response of male D.
melanogaster to rival males is highly sensitive to the level of
competition and can rapidly be reversed upon the removal of competition
(Bretman et al. 2012). Drosophila offers excellent potential for
studying how redundancy in cue components can affect plastic behaviour.
For example, Bretman et al. (2011b) found that male D.
melanogaster can detect rival males via three sensory cues: tactile,
olfactory and auditory. Males exposed to any two of these cues in
combination, or all three, responded with equivalent extensions to
subsequent mating duration. The finding that removing any one cue of
rival presence does not prevent the male from responding suggests that
there is redundancy in how these cues are processed. This redundancy may
confer robustness in responses to the social environment, which can be
complex and rapidly variable (Kasumovic et al. 2008; Bretman et al.
2011a; Greenspan 2012; Dore et al. 2018). Although male D.
melanogaster with one sensory cue removed were able to respond to
rivals, a longer period of exposure was required to elicit the longer
mating response, compared to males with all cues intact (Rouse and
Bretman 2016). Furthermore, the combination of cues a male is exposed to
has been found to have a role in species recognition of rivals (Bretman
et al. 2017). This suggests that there may be incomplete redundancy in
how the cues of rival presence are processed in order to produce the
behavioural response.
In addition to eliciting equivalent behavioural responses, perceiving
any two of the three rival cues appears to result in comparable
increases in the number of offspring fathered (Bretman et al. 2011b).
However, thus far this has only been tested in the absence of realised
sperm competition; hence, an important facet of the fitness consequences
of responding to rival males is not yet known. This is the omission we
tackle in this study. Determining whether males that have any one
sensory cue systematically removed achieve equivalent success in sperm
competition is important as it is expected to increase our understanding
of the fitness benefits and potential costs of redundancy in general.
We explicitly tested the fitness equivalence of receiving alternative
cues of rival presence under sperm competition, to investigate further
whether these cues show complete redundancy. Male D. melanogasterwere exposed to intact rivals or those subjected to a physical
manipulation that removed the auditory cue of rival presence. We focused
on testing auditory cue removal as this could be fully controlled,
(removal of tactile and olfactory cues produced off-target effects on
male behaviour; Supplementary information 1, 2; Figure S1, S2). Our
rationale for focusing our experiments on just this single cue removal
as the exemplar was that previous tests reported that all cues were
equivalent with respect to the subsequent behavioural and fitness
outcomes (Bretman et al. 2011b). Thus, the effects of removing the
auditory cue can inform our understanding of the redundancy of all three
key cues.
Males exposed to the full repertoire of cues (auditory + tactile +
olfactory) and those with one cue removed (tactile + olfactory) were
both predicted to show equivalent extension in mating duration and
increase in non-competitive paternity compared to males that had no
rival exposure, as identified by Bretman et al. (2011b). In addition, we
predicted that males exposed to either of the above combinations of
rival cues would achieve an equivalent increase in competitive paternity
when the female subsequently remated, relative to males kept without
rivals. This would support the idea that the cues of rival presence
perceived by male D. melanogaster are redundant.