This is a repository copy of Exposure time to rivals and sensory cues affect how quickly males respond to changes in sperm competition threat.White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/104720/ Version: Accepted Version Article:Rouse, J orcid.org/0000-0001-8457-4623 and Bretman, AJ orcid.org/0000-0002-4421-3337 (2016) Exposure time to rivals and sensory cues affect how quickly males respond to changes in sperm competition threat. Animal Behaviour, 122. pp. 1-8.

Phenotypic plasticity can be a key determinant of fitness. The degree to which the expression of plasticity is adaptive relies upon the accuracy with which information about the state of the environment is integrated. This step might be particularly beneficial when environments, e.g. the social and sexual context, change rapidly. Fluctuating temporal dynamics could increase the difficulty of determining the appropriate level of expression of a plastic response. In this review, we suggest that new insights into plastic responses to the social and sexual environment (social and reproductive plasticity) may be gained by examining the role of complex cues (those comprising multiple, distinct sensory components). Such cues can enable individuals to more accurately monitor their environment in order to respond adaptively to it across the whole life course. We briefly review the hypotheses for the evolution of complex cues and then adapt these ideas to the context of social and sexual plasticity. We propose that the ability to perceive complex cues can facilitate plasticity, increase the associated fitness benefits and decrease the risk of costly ‘mismatches’ between phenotype and environment by (i) increasing the robustness of information gained from highly variable environments, (ii) fine-tuning responses by using multiple strands of information and (iii) reducing time lags in adaptive responses. We conclude by outlining areas for future research that will help to determine the interplay between complex cues and plasticity.

Article:Rouse, J orcid.org/0000-0001-8457-4623, Watkinson, K and Bretman, A orcid.org/0000-0002- 4421-3337 (2018) AbstractMales of many species use social cues to predict sperm competition and tailor their reproductive strategies, such as ejaculate or behavioural investment, accordingly. Whilst these plastic strategies are widespread, the underlying mechanisms remain largely unknown. Plastic behaviour requires individuals to learn and memorise cues associated with environmental change before using this experience to modify behaviour. Drosophila melanogaster respond to an increase in sperm competition threat by extending mating duration after exposure to a rival male. This behaviour shows lag times between environmental change and behavioural response suggestive of acquisition and loss of memory. Considering olfaction is important for a male's ability to assess the sperm competition environment, we hypothesised that an olfactory learning and memory pathway may play a key role in controlling this plastic behaviour. We assessed the role of genes and brain structures known to be involved in learning and memory. We show that sperm competition responses depend on anaesthesia sensitive memory, specifically the genes rut and amn. We also show that the lobes of the mushroom bodies are integral to the control of plastic mating behaviour. These results reveal the genetic and neural properties required for reacting to changes in the sperm competition environment.

The social environment provides males with information about the likelihood of reproductive competition. However, social context can be highly variable, and males must track their environment in order to alter reproductive investment appropriately. In addition to using information gained as adults to adjust reproductive strategies, males can use cues in early life to anticipate future mating competition and alter development of reproductive tissue. As responding to variable levels of competition may be cognitively challenging, and early life environments could influence neural development, cues of future competition during development could influence adult cognitive capacity. Male Drosophila melanogaster fruit flies reared with cues of future reproductive competition, high larval density or in the presence of adult males, develop larger accessory glands. We examined whether these early life conditions affect adult male learning ability. We assessed the learning ability of adults reared under different larval social conditions in a non-sexual and sexual context. We also measured gene expression in learning, memory and synapse-related genes previously found to respond to the adult social environment. The presence of adult males during development had no effect. Males from low larval densities, however, had better learning ability in the sexual-context assay and showed relatively higher gene expression compared to flies from high larval densities. This could suggest a trade-off between reproductive investment into accessory gland growth or an increased investment into neural plasticity at low density.

Complex sets of cues can be important in recognizing and responding to conspecific mating competitors and avoiding potentially costly heterospecific competitive interactions. Within Drosophila melanogaster, males can detect sensory inputs from conspecifics to assess the level of competition. They respond to rivals by significantly extending mating duration and gain significant fitness benefits from doing so. Here, we tested the idea that the multiple sensory cues used by D. melanogaster males to detect conspecifics also function to minimize “off‐target” responses to heterospecific males that they might encounter (Drosophila simulans, Drosophila yakuba, Drosophila pseudoobscura, or Drosophila virilis). Focal D. melanogaster males exposed to D. simulans or D. pseudoobscura subsequently increased mating duration, but to a lesser extent than following exposure to conspecific rivals. The magnitude of rivals’ responses expressed by D. melanogaster males did not align with genetic distance between species, and none of the sensory manipulations caused D. melanogaster to respond to males of all other species tested. However, when we removed or provided “false” sensory cues, D. melanogaster males became more likely to show increased mating duration responses to heterospecific males. We suggest that benefits of avoiding inaccurate assessment of the competitive environment may shape the evolution of recognition cues.