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The social environment has myriad effects on individuals, altering reproduction, immune function, cognition, and aging. Phenotypic plasticity enables animals to respond to heterogeneous environments such as the social environment but requires that they assess those environments accurately. It has been suggested that combinations of sensory cues allow animals to respond rapidly and accurately to changeable environments, but it is unclear whether the same sensory inputs are required in all traits that respond to a particular environmental cue. Drosophila melanogaster males, in the presence of rival males, exhibit a consistent behavioral response by extending mating duration. However, exposure to a rival also results in a reduction in their lifespan, a phenomenon interpreted as a trade-off associated with sperm competition strategies. D. melanogaster perceive their rivals by using multiple sensory cues; interfering with at least two olfactory, auditory, or tactile cues eliminates the extension of mating duration. Here, we assessed whether these same cues were implicated in the lifespan reduction. Removal of combinations of auditory and olfactory cues removed the extended mating duration response to a rival, as previously found. However, we found that these manipulations did not alter the reduction in lifespan of males exposed to rivals or induce any changes in activity patterns, grooming, or male–male aggression. Therefore, our analysis suggests that lifespan reduction is not a cost associated with the behavioral responses to sperm competition. Moreover, this highlights the trait-specific nature of the mechanisms underlying plasticity in response to the same environmental conditions. [ABSTRACT FROM AUTHOR]

Plasticity in developmental processes gives rise to remarkable environmentally induced phenotypes. Some of the most striking and well-studied examples of developmental plasticity are seen in insects. For example, beetle horn size responds to nutritional state, butterfly eyespots are enlarged in response to temperature and humidity, and environmental cues also give rise to the queen and worker castes of eusocial insects. These phenotypes arise from essentially identical genomes in response to an environmental cue during development. Developmental plasticity is taxonomically widespread, affects individual fitness, and may act as a rapid-response mechanism allowing individuals to adapt to changing environments. Despite the importance and prevalence of developmental plasticity, there remains scant mechanistic understanding of how it works or evolves. In this review, we use key examples to discuss what is known about developmental plasticity in insects and identify fundamental gaps in the current knowledge. We highlight the importance of working towards a fully integrated understanding of developmental plasticity in a diverse range of species. Furthermore, we advocate for the use of comparative studies in an evo-devo framework to address how developmental plasticity works and how it evolves. [ABSTRACT FROM AUTHOR]

Individuals can respond plastically to variation in their social environment. However, each sex may respond to different cues and contrasting aspects of competition. Theory suggests that the plastic phenotype expressed by one sex can influence evolutionary dynamics in the other, and that plasticity simultaneously expressed by both sexes can exert sex‐specific effects on fitness. However, data are needed to test this theory base. Here, we examined whether the simultaneous expression of adaptive plasticity by both sexes of Drosophila melanogaster fruit flies in response to their respective social environments interacts to determine the value of key reproductive traits (mating latency, duration, and fecundity). To vary social environments, males were kept alone, or with same sex rivals, and females were kept alone, in same‐sex, or mixed‐sex groups. Matings were then conducted between individuals from all of these five social treatments in all combinations, and the resulting reproductive traits measured in both "choice" and "no‐choice" assays. Mating latency was determined by an interaction between the plastic responses of both sexes to their social environments. Interestingly, the mating latency response occurred in opposing directions in the different assays. In females exposed to same‐sex social treatments, mating latency was more rapid with rival treatment males in the choice assays, but slower with those same males in no‐choice assays. In contrast, mating duration was determined purely by responses of males to their social environments, and fecundity purely by responses of females. Collectively, the results show that plastic responses represent an important and novel facet of sexual interactions. [ABSTRACT FROM AUTHOR]

Phenotypic plasticity can allow animals to adapt their behavior, such as their mating effort, to their social and sexual environment. However, this relies on the individual receiving accurate and reliable cues of the environmental conditions. This can be achieved via the receipt of multimodal cues, which may provide redundancy and robustness. Male Drosophila melanogaster detect presence of rivals via combinations of any two or more redundant cue components (sound, smell, and touch) and respond by extending their subsequent mating duration, which is associated with higher reproductive success. Although alternative combinations of cues of rival presence have previously been found to elicit equivalent increases in mating duration and offspring production, their redundancy in securing success under sperm competition has not previously been tested. Here, we explicitly test this by exposing male D. melanogaster to alternative combinations of rival cues, and examine reproductive success in both the presence and absence of sperm competition. The results supported previous findings of redundancy of cues in terms of behavioral responses. However, there was no evidence of reproductive benefits accrued by extending mating duration in response to rivals. The lack of identifiable fitness benefits of longer mating under these conditions, both in the presence and absence of sperm competition, contrasted with some previous results, but could be explained by (a) damage sustained from aggressive interactions with rivals leading to reduced ability to increase ejaculate investment, (b) presence of features of the social environment, such as male and female mating status, that obscured the fitness benefits of longer mating, and (c) decoupling of behavioral investment with fitness benefits. [ABSTRACT FROM AUTHOR]

Sperm competition favors large, costly ejaculates, and theory predicts the evolution of allocation strategies that enable males to plastically tailor ejaculate expenditure to sperm competition threat. While greater sperm transfer in response to a perceived increase in the risk of sperm competition is well-supported, we have a poor understanding ofwhether males (i) respond to changes in perceived intensity of sperm competition, (ii) use the same allocation rules for sperm and seminal fluid, and (iii) experience changes in current and future reproductive performance as a result of ejaculate compositional changes. Combining quantitative proteomics with fluorescent sperm labeling, we show that Drosophila melanogaster males exercise independent control over the transfer of sperm and seminal fluid proteins (SFPs) under different levels of male-male competition. While sperm transfer peaks at low competition, consistent with some theoretical predictions based on sperm competition intensity, the abundance of transferred SFPs generally increases at high competition levels. However, we find that clusters of SFPs vary in the directionality and sensitivity of their response to competition, promoting compositional change in seminal fluid. By tracking the degree of decline inmale mating probability and offspring production across successive matings, we provide evidence that ejaculate compositional change represents an adaptive response to current spermcompetition, but one that comes at a cost to future mating performance. Our work reveals a previously unknown divergence in ejaculate component allocation rules, exposes downstream costs of elevated ejaculate investment, and ultimately suggests a central role for ejaculate compositional plasticity in sexual selection. [ABSTRACT FROM AUTHOR]

Phenotypic plasticity can increase fitness in rapidly changeable environments, but may be limited if the underlying mechanisms cause a lag between environmental change and individual response or if the information individuals receive is unreliable. Hence to understand the evolution of plasticity we need to assess whether individuals respond to fine-scale variation in environmental cues. In this study we used a Drosophila melanogaster fruit fly model to investigate factors that determine how quickly males alter their behaviour in response to changes in sperm competition cues. Male D. melanogaster respond to exposure to rival males prior to mating by extending mating duration and increasing ejaculate investment. We have previously shown that to build-up the response, males need about 24 h exposure to a rival. We reasoned that this time lag was necessary to increase ejaculate production, but this physiological limitation should not apply when moving from high- to low-competition environments; hence we predicted that males should immediately decrease their investment when competition is removed. Here we tested this by measuring how long rival-exposed males maintained an extended mating duration after removal of the rival. We assessed how exposure time and sensory information affected the speed of change in behavioural state. Males maintained extended mating duration for hours after a rival was removed, but this was dependent on time of exposure to a rival. Furthermore, although sensory-impaired males were able to respond to rivals, the time required for the response to build and diminish depended on males possessing their full sensory repertoire. Our results suggest that males use exposure time and multiple sensory cues to assess whether the threat of sperm competition is transient (so unlikely to translate into realized competition) or sustained (requiring a response). Therefore, time lags between environmental changes and responses may buffer animals against making hasty decisions in fluctuating environments. [ABSTRACT FROM AUTHOR]

Phenotypic plasticity will be favored whenever there are significant fitness benefits of responding to environmental variation. The extent and nature of the plasticity that evolves depends on the rate of environmental fluctuations and the capacity to track and respond to that variability. Reproductive environments represent one arena in which changes can be rapid. The finding that males of many species show morphological, physiological, and behavioral plasticity in response to premating and postmating reproductive competition (RC) suggests that plasticity is broadly beneficial. The developmental environment is expected to accurately predict the average population level of RC but to be a relatively poor indicator of immediate RC at any particular mating. Therefore, we predict that manipulation of average RC during development should cause a response in plasticity "set" during development (e.g., size of adult reproductive structures), but not in flexible plasticity determined by the immediate adult environment (e.g., behavioral plasticity in mating duration). We tested this prediction in Drosophila melanogaster males by manipulating 2 independent cues of average RC during development: 1) larval density and 2) the presence or absence of adult males within larval culture vials. Consistent with the prediction, both manipulations resulted in the development of males with significantly larger adult accessory glands (although testis size decreased when males were added to culture vials). There was no effect on adult plasticity (mating duration, extended mating in response to rivals). The results suggest that males have evolved independent responses to long- and short-term variation in RC. [ABSTRACT FROM AUTHOR]

Phenotypic plasticity is a key mechanism by which animals can cope with rapidly changeable environments, but the evolutionary lability of such plasticity remains unclear. The socio-sexual environment can fluctuate very rapidly, affecting both the frequency of mating opportunities and the level of competition males may face. Males of many species show plastic behavioural responses to changes in social environment, in particular the presence of rival males. For example, Drosophila pseudoobscura males respond to rivals by extending mating duration and increasing ejaculate size. Whilst such responses are predicted to be adaptive, the extent to which the magnitude of response is heritable, and hence selectable, is unknown. We investigated this using isofemale lines of the fruit fly D. pseudoobscura, estimating heritability of mating duration in males exposed or not to a rival, and any genetic basis to the change in this trait between these environments (i.e. degree of plasticity). The two populations differed in population sex ratio, and the presence of a sex ratio distorting selfish chromosome. We find that mating duration is heritable, but no evidence of population differences. We find no significant heritability of plasticity in mating duration in one population, but borderline significant heritability of plasticity in the second. This difference between populations might be related to the presence of the sex ratio distorting selfish gene in the latter population, but this will require investigation in additional populations to draw any conclusions. We suggest that there is scope for selection to produce an evolutionary response in the plasticity of mating duration in response to rivals in D. pseudoobscura, at least in some populations. [ABSTRACT FROM AUTHOR]

Theory predicts that males should evolve mechanisms to assess competition and allocate resources accordingly. This requires phenotypic plasticity, to accurately match responses to the environment. Plastic responses in males to sexual competition are diverse and widespread. However, our ability to understand and predict how they evolve is limited because their benefits are rarely measured, and costs are, as yet, entirely unquantified. In the fruit fly Drosophila melanogaster, males that anticipate strong competition for matings or fertilizations subsequently mate for longer and transfer more of two key seminal fluid proteins. This results in significantly elevated reproductive output. In this study, we examined the fitness effects of male responses to rivals across the entire male life span. Males were exposed to rivals or not throughout life while controlling mating opportunities. Males showed significant responses to rivals throughout their lifetimes, associated with significant early-life fitness benefits. However, these disappeared after the third mating. There were also significant costs-males exposed to rivals took significantly fewer mating opportunities in later life and had significantly shorter life spans than controls. The data suggest that there are substantial costs for males of mounting plastic responses to the threat of sexual competition. [ABSTRACT FROM AUTHOR]

Plasticity in behaviour is of fundamental significance when environments are variable. Such plasticity is particularly important in the context of rapid changes in the socio-sexual environment. Males can exhibit adaptive plastic responses to variation in the overall level of reproductive competition. However, the extent of behavioural flexibility within individuals, and the degree to which rapidly changing plastic responses map onto fitness are unknown. We addressed this by determining the behaviour and fitness profiles of individual Drosophila melanogaster males subjected to up to three episodes of exposure to rivals or no rivals, in all combinations. Behaviour (mating duration) was remarkably sensitive to the level of competition and fully reversible, suggesting that substantial costs arise from the incorrect expression of even highly flexible behaviour. However, changes in mating duration matched fitness outcomes (offspring number) only in scenarios in which males experienced zero then high competition. Following the removal of competition, mating duration, but not offspring production, decreased to below control levels. This indicates that the benefit of increasing reproductive investment when encountering rivals may exceed that of decreasing investment when rivals disappear. Such asymmetric fitness benefits and mismatches with behavioural responses are expected to exert strong selection on the evolution of plasticity. [ABSTRACT FROM AUTHOR]

Abstract: Male responses to risk of sperm competition play an important role in sexual selection, sexual conflict, and the evolution of mating systems. Such responses can combine behavioural and physiological processes, and can be mediated through different components of the ejaculate such as sperm numbers and seminal proteins. An additional level of ejaculate complexity is sperm heteromorphism, with the inclusion of non-fertilising parasperm in the ejaculate. We now test the response to rivals in a sperm heteromorphic species, Drosophila pseudoobscura, measuring the behavioural response and sperm transfer and, crucially, relating these to short-term fitness. Males respond to exposure to conspecific rivals by increasing mating duration, but do not respond to heterospecific rivals. In addition, after exposure to a conspecific rival, males increased the transfer of fertilising eusperm, but not non-fertilising parasperm. Males exposed to a conspecific rival also achieve higher offspring production. This suggests that the evolution of parasperm in flies was not driven by sperm competition and adds to the increasing evidence that males can make extremely sophisticated responses to mating competition. [Copyright &y& Elsevier]