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.