Assessment of Rival Males through the Use of Multiple Sensory Cues in the Fruitfly Drosophila pseudoobscura

April Assessment of Rival Males through the Use of Multiple Sensory Cues in the Fruitfly Drosophila pseudoobscura Chris P. Maguire 0 1 2 Anne Liz 0 1 2 Tom A. R. Price 0 1 2 0 1 Institute of Integrative Biology, University of Liverpool , Liverpool , United Kingdom , 2 UMR 6553 ECOBIO , Universite de Rennes 1 , Rennes , France 1 Funding: This work was funded by the Natural Environment Research Council (www.nerc.ac.uk), which was not directly involved in the work in any way (grant NE/H015604/1 to TP). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript 2 Academic Editor: Alex Cordoba-Aguilar, Universidad Nacional Autonoma de Mexico , MEXICO Environments vary stochastically, and animals need to behave in ways that best fit the conditions in which they find themselves. The social environment is particularly variable, and responding appropriately to it can be vital for an animal's success. However, cues of social environment are not always reliable, and animals may need to balance accuracy against the risk of failing to respond if local conditions or interfering signals prevent them detecting a cue. Recent work has shown that many male Drosophila fruit flies respond to the presence of rival males, and that these responses increase their success in acquiring mates and fathering offspring. In Drosophila melanogaster males detect rivals using auditory, tactile and olfactory cues. However, males fail to respond to rivals if any two of these senses are not functioning: a single cue is not enough to produce a response. Here we examined cue use in the detection of rival males in a distantly related Drosophila species, D. pseudoobscura, where auditory, olfactory, tactile and visual cues were manipulated to assess the importance of each sensory cue singly and in combination. In contrast to D. melanogaster, male D. pseudoobscura require intact olfactory and tactile cues to respond to rivals. Visual cues were not important for detecting rival D. pseudoobscura, while results on auditory cues appeared puzzling. This difference in cue use in two species in the same genus suggests that cue use is evolutionarily labile, and may evolve in response to ecological or life history differences between species. - Competing Interests: The authors have declared that no competing interests exist. Animals often show rapid behavioural and physiological changes to survive and reproduce in a changeable environment [1, 2]. In particular, the socio-sexual environment can change very quickly, and is therefore extremely important for male mating success [1]. Competition between males for access to females is known to generate aggressiveness between males in many animals such as mice [3], birds [4], fish [5], spiders [6], and flies [7, 8]). Expressing aggressiveness toward a conspecific depends on the ability to recognize and identify individuals within a social context [9]. For example, a male that is unable to recognize other males or distinguish them from females may waste energy by attempting to court both males and females alike. In recognition systems (social, mate, kin or family, predatory etc.), an individual has to express or bear a cue that will be perceived and processed by receivers, who will respond (or not) to it appropriately. Recognition systems are costly as any errors may lead to reduced fitness both for the emitter and the receiver of the cue [1012]. Therefore recognition systems are generally very specific and sometimes highly complex. In some species, single environmental cues are used as key indicators of sperm competition risk [13]. For example, the male meadow vole (Microtus pennsylvanicus) will increase its sperm investment after detecting the risk of sperm competition through the odour of conspecific males [14]. However, in many systems multiple cues are likely to be used, and how multiple cues are perceived and integrated by the receiver to generate a response is poorly understood. Indeed, understanding how multiple cues are integrated over both behavioural and evolutionary time is a key area of research in behavioral ecology, in behaviors including mate choice and struggles for dominance [15,16], investment in offspring and rejection of brood parasites [17] and habitat selection [18]. As experiments on detection of rivals and responses to them can be carried out in the laboratory [1], they provide a potentially enlightening area in which to examine the integration of cues. However, at present, there are few studies that assess the use of multiple cues to effectively respond to rivals [1]. In addition, the fitness consequences of such physiological and behavioural responses have received very little attention in the literature [1]. In light of this significant gap in knowledge, two studies using Drosophila, have tried to identify the potential multiple cues that males use to assess the risk of sperm competition and to examine the fitness effects of the resultant plastic behaviours [13, 19]. However, recognizing a competitor, a mate or a potential predator does not necessarily mean that the individual will express a response. In fact, we can only behaviorally detect recognition systems and assess them when the receiver expresses a response to the emitter (i.e. when an interaction occurs). This notion suggests that an absence of behaviour as a response does not necessarily mean that recognition did not occur. This is particularly difficult to deal with as we cannot ascertain that recognition was absent when there is no interaction between individuals. Deciphering the cues used, and how they are processed by receivers, is essential as it allows us to some extent to study recognition systems. Male behavioural plasticity has been shown in numerous Drosophila species, as a response to the threat of sperm competition [1921]. In the presence of rivals, males will undergo prolonged copulation and show an increase in a latency to copulate [21]. D. pseudoobscura has been shown to effectively alter the proportion of eusperm (fertilising) and parasperm (nonfertilising) in their ejaculate [22]. Additionally, D. melanogaster have been shown to strategically allocate the proportions of their seminal fluid proteins, in response to the risk of sperm competition [23], and to increase the number of sperm in their ejaculate after exposure to a rival male [24]. These variable responses made to rivals have subsequently been shown to cause a gain in fitness in both D. melanogaster and D. pseudoobscura, through a direct increase in offspring [20, 22]. However, in D. melanogaster this response to potential rivals has fitness costs in terms of male survival and mating success later in life, making it important that males respond appropriately to rivals [25]. The ability to assess potential rivalry in male Drosophila suggests a highly accurate mechanism for perception, allowing behavioural plasticity to be performed to a high de (...truncated)