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Theoretical analyses indicate that aggressive signals should positively correlate with the signallers' willingness and abilities to fight. Few experimental studies, however, have tested this prediction. In two experiments employing distinct, ecologically realistic protocols, we quantified the association between aggressive signals and fighting in fruit fly genotypes and found high positive genetic correlations between threat and fighting ( r G = 0.80 and 0.74). Our results add to the growing body of experimental work indicating that aggressive signals have relatively high informational value.

Female mate choice is a complex decision making process that involves many context-dependent factors. Understanding the factors that shape variation in female mate choice has important consequences for evolution via sexual selection. In many animals including fruit flies, Drosophila melanogaster, males often use aggressive mating strategies to coerce females into mating, but it is not clear if females’ experience with sexual aggression shapes their future behaviors. Here, we used males derived from lineages that were artificially selected to display either low or high sexual aggression toward females to determine how experience with these males shapes subsequent female mate choice. First, we verified that males from these lineages differed in their sexual behaviors. We found that males from high sexual aggression backgrounds spent more time pursuing virgin females, and had a shorter mating latency but shorter copulation duration compared with males from low sexual aggression backgrounds. Next, we tested how either a harassment by or mating experience with males from either a high or low sexual aggression backgrounds influenced subsequent female mate choice behaviors. We found that in both scenarios, females that interacted with high sexual aggression males were more likely and faster to mate with a novel male one day later, regardless of the male’s aggression level. These results have important implications for understanding the evolution of flexible polyandry as a mechanism that benefits females.

Male sexual aggression towards females is a form of sexual conflict that can result in increased fitness for males through forced copulations (FCs) or coercive matings at the cost of female lifetime fitness. We used male fruit flies (Drosophila melanogaster) as a model system to uncover the genomic contributions to variation in FC, both due to standing variation in a wild population, and due to plastic changes associated with variation in social experience. We used RNAseq to analyse whole-transcriptome differential expression (DE) in male head tissue associated with evolved changes in FC from lineages previously selected for high and low FC rate and in male flies with varying FC rates due to social experience. We identified hundreds of genes associated with evolved and plastic variation in FC, however only a small proportion (27 genes) showed consistent DE due to both modes of variation. We confirmed this trend of low concordance in gene expression effects across broader sets of genes significant in either the evolved or plastic analyses using multivariate approaches. The gene ontology terms neuropeptide hormone activity and serotonin receptor activity were significantly enriched in the set of significant genes. Of seven genes chosen for RNAi knockdown validation tests, knockdown of four genes showed the expected effect on FC behaviours. Taken together, our results provide important information about the apparently independent genetic architectures that underlie natural variation in sexual aggression due to evolution and plasticity.

When the reproductive interests of males and females conflict, males can evolve traits that are harmful to females, and females can coevolve traits to resist this harm. In the fruit fly, Drosophila melanogaster, there is genetic variation in female resistance traits, which can affect the pre- and post-mating success of males that try to mate with them. However, it is not clear to what extent the expression of these phenotypes can be modified by environmental factors such as sociosexual experience. Here, we tested how the genetic background of a female and her previous mating experience interact to affect the mating success of focal males. In the experience phase, we placed females from 28 distinct genetic backgrounds individually either with a single male (low conflict) or with three males (high conflict) for 48 hr. In the subsequent test phase, we measured the mating and post-mating fertilization success of focal males paired individually with each female. We found that focal males paired with females from the high-conflict treatment were less successful at mating, took longer to mate when they were successful, and had a lower proportion of paternity share. Furthermore, we identified significant female genetic variation associated with male mating success. These results indicate that female experience, along with intrinsic genetic factors, can independently influence different fitness components of her subsequent mates and has implications for our understanding of plastic female mating strategies and the evolution of sexually antagonistic traits in males and females.

Forced copulation is an extreme form of sexual aggression that can affect the evolution of sex-specific anatomy, morphology, and behavior. To characterize mechanistic and evolutionary aspects of forced copulation, we artificially selected male fruit flies based on their ability to succeed in the naturally prevalent behavior of forced matings with newly eclosed (teneral) females. The low and high forced copulation lineages showed rapid divergence, with the high lineages ultimately showing twice the rates of forced copulation as the low lineages. While males from the high lineages spent more time aggressively pursuing and mounting teneral females, their behavior toward non-teneral and heterospecific females was similar to that of males from the low lineages. Males from the low and high lineages also showed similar levels of male-male aggression. This suggests little or no genetic correlations between sexual aggression and non-aggressive pursuit of females, and between male aggression toward females and males. Surprisingly however, males from the high lineages had twice as high mating success than males from the low lineages when allowed to compete for consensual mating with mature females. In further experiments, we found no evidence for trade-offs associated with high forced mating rates: males from the high lineages did not have lower longevity than males from the low lineages when housed with females, and four generations of relaxed selection did not lead to convergence in forced mating rates. Our data indicate complex interactions among forced copulation success and consensual mating behavior, which we hope to clarify in future genomic work.

Cognition, defined as the processes concerned with the acquisition, retention and use of information, underlies animals’ abilities to navigate their local surroundings, embark on long-distance seasonal migrations, and socially learn information relevant to movement. Hence, in order to fully understand and predict animal movement, researchers must know the cognitive mechanisms that generate such movement. Work on a few model systems indicates that most animals possess excellent spatial learning and memory abilities, meaning that they can acquire and later recall information about distances and directions among relevant objects. Similarly, field work on several species has revealed some of the mechanisms that enable them to navigate over distances of up to several thousand kilometers. Key behaviors related to movement such as the choice of nest location, home range location and migration route are often affected by parents and other conspecifics. In some species, such social influence leads to the formation of aggregations, which in turn may lead to further social learning about food locations or other resources. Throughout the review, we note a variety of topics at the interface of cognition and movement that invite further investigation. These include the use of social information embedded in trails, the likely important roles of soundscapes and smellscapes, the mechanisms that large mammals rely on for long-distance migration, and the effects of expertise acquired over extended periods.

There has been extensive research on the ecology and evolution of social life in animals that live in groups. Less attention, however, has been devoted to apparently solitary species, even though recent research indicates that they also possess complex social behaviors. To address this knowledge gap, we artificially selected on sociability, defined as the tendency to engage in nonaggressive activities with others, in fruit flies. Our goal was to quantify the factors that determine the level of sociability and the traits correlated with this feature. After 25 generations of selection, the high-sociability lineages showed sociability scores about 50% higher than did the low-sociability lineages. Experiments using the evolved lineages indicated that there were no differences in mating success between flies from the low and high lineages. Both males and females from the low lineages, however, were more aggressive than males and females from the high lineages. Finally, the evolved lineages maintained their sociability scores after 10 generations of relaxed selection, suggesting no costs to maintaining low and high sociability, at least under our settings. Sociability is a complex trait, which we currently assess through genomic work on the evolved lineages.

Sexual conflict is common in nature and sometimes results in sexual aggression. An extreme case is forced copulation, where one individual forcibly mates with another individual who resists the mating. To understand what makes some males sexually aggressive, we established an experimental system that allowed us to quantify the characteristics that contribute to males' forced copulation success. In fruit flies (Drosophila melanogaster), sexually mature females can choose to accept or reject courting males; however, males can forcibly copulate with newly eclosed, sexually immature, teneral females. We tested males from 59 genotypes and found significant genetic variation in forced copulation success, with a broad-sense heritability of 0.16. We then chose three genotypes with the lowest and three genotypes with the highest forced copulation success rates and compared the behaviour of males from these two groups. Males from genotypes with high forced copulation success were more persistent in their pursuit of teneral females and mounted them more frequently than did males from the low-success genotypes. Males of the two categories, however, were similar in their attractiveness to both teneral and sexually mature females. Our results suggest that males vary in their pursuit strategies. Some males respond to female rejection signals by giving up and searching for receptive females, while other males persist in pursuit and coercion in spite of female objection. Our work highlights the practicality of using forced copulation in fruit flies as a model for further research on the mechanisms affecting variation in sexual coercion and forced copulation success and their evolutionary consequences.

To understand the prevalence and conditional use of aggression among animals, one has to know its costs and benefits. The obvious cost of aggression in animals that possess teeth, claws or other specialized weaponry is injury. Many species, however, do not have such body parts and thus cannot readily injure others. The cost of aggression in these animals is not well studied. We tested whether aggression has a fitness cost in fruit flies, which can serve as a model species for animals without weapons that engage in aggression. In three experiments employing distinct protocols, we allowed focal flies to fight for control of an attractive food patch over 4 days and then compared their survivorship to that of flies not engaged in conflict. In all three experiments, fly survivorship was lower in the aggression than no‐aggression treatments. Microscopic examination revealed no differences in wing damage between flies of the aggression and no‐aggression treatments. The two most likely, non‐mutually exclusive explanations for lower survivorship post‐fighting are physiological changes due to stress, and metabolic alterations associated with a life‐history strategy optimized for high‐conflict settings.

Expertise consists of the features that allow individuals with extensive experience on a given complex task to show superior performance on that task compared to novices. While expertise has been investigated mostly in humans, it is highly relevant for other species as well because it can have strong effects on fitness. Moreover, studying expertise in nonhumans can help us understand human expertise. Several features that distinguish experts within their domain of expertise from novices include (1) greater long-term memory, (2) larger capacity of working memory, (3) better ability to focus attention on the most relevant concurrent tasks, (4) superior ability to anticipate, perceive and comprehend the relevant elements in one's surroundings, (5) quicker and better decisions, and (6) faster and more coordinated motor movements. The development of expertise follows a characteristic pattern of gradual improvement in performance over extended periods devoted to practising a given complex task. Heritable variation in a few traits can affect the rate of expertise acquisition and its peak levels. These traits include motivation to practise, perseverance, basic cognitive abilities such as attention span, working memory capacity, learning rates and memory retention, and various physiological, anatomical and morphological features. Key environmental factors influencing expertise development are parental and social settings, which may encourage investment in the extended practice necessary for achieving superior performance on complex tasks. Future work on the evolutionary biology of expertise should focus on the yet unknown neurobiological mechanisms that underlie it, heritable variation in the traits that enable expertise and their genetic basis, further quantifications of expertise acquisition in natural settings, the fitness consequences of the traits that facilitate top expert performance, and the ecological and evolutionary consequences of expertise.

Social interactions are typically impaired in neuropsychiatric disorders such as autism, for which the genetic underpinnings are very complex. Social interactions can be modeled by analysis of behaviors, including social spacing, sociability, and aggression, in simpler organisms such as Drosophila melanogaster. Here, we examined the effects of mutants of the autism-related gene neuroligin 3 (nlg3) on fly social and non-social behaviors. Startled-induced negative geotaxis is affected by a loss of function nlg3 mutation. Social space and aggression are also altered in a sex- and social-experience-specific manner in nlg3 mutant flies. In light of the conserved roles that neuroligins play in social behavior, our results offer insight into the regulation of social behavior in other organisms, including humans.

Sociability, defined as individuals' propensity to participate in non-aggressive activities with conspecifics, is a fundamental feature of behavior in many animals including humans. However, we still have a limited knowledge of the mechanisms and evolutionary biology of sociability. To enhance our understanding, we developed a new protocol to quantify sociability in fruit flies (Drosophila melanogaster). In a series of experiments with 59 F1 hybrids derived from inbred lines, we documented, first, significant genetic variation in sociability in both males and females, with broad-sense heritabilities of 0.24 and 0.21 respectively. Second, we observed little genetic correlation in sociability between the sexes. Third, we found genetic variation in social plasticity among the hybrids, with a broad-sense heritability of ~0.24. That is, genotypes differed in the degree of sociability after experiencing the same relevant social experience. Our data pave the way for further research on the mechanisms that underlie sociability as well as its ecological and evolutionary consequences.

The outcomes of sexual selection often differ when mating success is determined by male contest rather than female choice. Many studies, however, inferred sexual selection driven by female choice without carefully assessing the role of subtle male aggression. Relying on close-up video analyses, we documented novel courtship interference between male fruit flies, a key model system in research on sexual selection, sexual conflict and speciation. In experiments comparing male mating success under choice (2 males + 1 female) and no-choice (1 male + 1 female) conditions, we found that, in some cases, courtship interference altered male mating success. Both choice and no-choice protocols have known weaknesses. Choice protocols do not control for male–male interactions while no-choice protocols do not allow females to compare and choose between males. To overcome these weaknesses, we developed a new protocol (true-choice), which allows females to freely visit and assess each of two males while preventing direct male–male interactions. Results from the true-choice protocol suggest that traits enhancing male aggression have a greater role in determining mating success in fruit flies. Furthermore, it is possible that the mating system of scramble competition observed in many species should be reclassified as subtle male contest, which can drive sexual selection for aggressive male features.

Indirect genetic effects (IGEs) are a major driver of social evolution, but much of the experimental work pertaining to IGEs on social behaviour has focused on the effect of stimulus individuals on single focal individuals. We extended IGE research to examine how stimulus individuals influence social interactions among several focal individuals. Specifically, we relied on recent work on social behaviour in fruit flies to examine whether IGEs cause 12 stimulus flies of distinct genotypes to alter social interactions within groups of six focal flies. The social behaviour of focals was significantly affected by the genotype of the stimulus flies. Focals were closer together when grouped with stimulus flies from genotypes that were close together than when grouped with stimulus flies from genotypes that were farther apart. A mechanism mediating this effect was the encounter rate between focal flies, which was lowest when the focal flies were grouped with stimulus flies of the more cohesive genotypes.

In many species, intense male-male competition for the opportunity to sire offspring has led to the evolution of selfish reproductive traits that are harmful to the females they mate with. In the fruit fly, Drosophila melanogaster, males modulate their reproductive behavior based on the perceived intensity of competition in their premating environment. Specifically, males housed with other males subsequently transfer a larger ejaculate during a longer mating compared to males housed alone. Although the potential fitness benefits to males from such plasticity are clear, its effects on females are mostly unknown. Hence, we tested the long-term consequences to females from mating with males with distinct social experiences. First, we verified that competitive experience influences male mating behavior and found that males housed with rivals subsequently have shorter mating latencies and longer mating durations. Then, we exposed females every other day for 20 days to males that were either housed alone or with rivals, and subsequently measured their fitness. We found that females mated to males housed with rivals produce more offspring early in life but fewer offspring later in life and have shorter lifespans but similar intrinsic population growth rates. These results indicate that plasticity in male mating behavior can influence female life histories by altering females' relative allocation to early versus late investment in reproduction and survival.

In many animals, the outcomes of competitive interactions can have lasting effects that influence an individual's reproductive success and have important consequences for the strength and direction of evolution via sexual selection. In the fruit fly, Drosophila melanogaster , males that have won previous contests are more likely to win in subsequent conflicts and losers are more likely to lose (winner–loser effects), but the direct fitness consequences and genetic underpinnings of this plasticity are poorly understood. Here, we tested how male genotype and the outcomes of previous male–male conflicts influence male pre- and post-copulatory success. We quantified pre-copulatory success in a choice and no-choice context, and post-copulatory success by quantifying ejaculate offensive and defensive ability. We found that winners have higher reproductive success compared to losers in both pre-copulatory scenarios. However, losers consistently mated for a longer duration, boosted female fecundity and had an increased paternity share when they were the first males to mate, suggesting increased investment into post-copulatory mechanisms. Finally, by using clonal hybrids from the Drosophila Genetic Reference Panel, we documented that genetic variation explained a sizeable proportion of the observed differences between lines, and of the interaction between line and winner and loser effects. Our results place the behavioural data on winner–loser effects in an evolutionary context by documenting the potential fitness gain to males from altering their reproductive strategy based on fighting experience. Our data may also explain the presence and maintenance of trade-offs between different male reproductive strategies.

Both maternal and offspring fitness would be higher if the offspring develop in a high-quality habitat than in a low-quality habitat. In animals without direct maternal care, it seems reasonable that either mothers or offspring should invest in finding the best habitat. Recent research, however, suggests extensive maternal and offspring exploration in fruit flies. We considered two hypotheses that could resolve this paradox, first that mothers do not choose oviposition sites that maximize larval success but rather sites that maximize their own fitness or egg survival, and, second, that the winged mothers make decisions over a larger spatial scale than the less mobile larvae are capable of. In a set of experiments, we found that larvae were more likely to explore when they hatched in poor patches lacking protective cavities and live yeast. Egg-laying females, however, also showed strong preferences for ovipositing in cavities with live yeast. These results provided no support for the first hypothesis. We then considered whether females are sensitive to larval travel costs between cavities and live yeast as suggested by the second hypothesis. We found no effect of the distance between the two patches on female oviposition choice, but we did find an effect of the intervening substrate. Females overwhelmingly preferred to lay in the cavity when the intervening substrate was an agar medium, but not when the intervening substrate was bare plastic that discourages larval travel. Therefore, we resolve the paradox of extensive exploration by both mothers and offspring by showing that larvae that hatch in habitats that are desirable to ovipositing females, but not to the larvae, can reasonably assume that there are better food patches within a safe travel distance. That is, there is an adaptive sharing of exploration between mothers and offspring. The exploration sharing hypothesis is pertinent for a large variety of species in which mothers oviposit in sites suboptimal for larval growth.

The traditional view of insects, as driven primarily by instinct, has changed dramatically in the past few decades. It begins with a brief review of insects’ sophisticated cognition, defined as the neuronal processes concerned with the acquisition, retention, and use of information. Three illuminating examples that illustrate adaptive aspects of cognitive traits in the context of night vision, memory and antipredatory decisions are given. Most insects possess good individual learning abilities and learning is positively associated with insect fitness. While social learning has been instrumental in social insects’ lives, its prevalence and importance in other insect taxa is still unknown. The chapter concludes by highlighting promising topics for future investigation, including research on heritable variation in insect cognitive traits and its association with fitness, expertise development, social learning in non-social insects, and the role of emotion in guiding insect decisions.

Lay Summary The adaptive decoupling hypothesis explains the prevalence of complex life cycles in animals by stating that antagonistic selection leads to the disruption of genetic correlations between juvenile and adult traits. We quantified the degree of sociality in larval and adult fruit flies. Although we found significant variation in social behavior among larvae and adults, both traits were decoupled between larvae and adults. Our results agree with the adaptive decoupling hypothesis.

Aggression is a central trait affecting fitness, which has been well studied in many animals. As a part of a research programme integrating mechanisms and fitness consequences of aggression, we examined the adaptive functions of antagonistic interactions in fruit flies, Drosophila melanogaster, a species in which aggression has been studied primarily in the context of territorial behaviour. In our experiments, males at an attractive food patch were more aggressive towards other males when they were in the presence of their recent mates than when they were in the presence of females mated with other males. Furthermore, while recently mated males accompanied by their mates were more aggressive than virgin males, recently mated males and virgin males showed similar levels of aggression in the presence of females mated with other males. When we allowed focal males to mate inside experimental arenas and then added intruder males, the intruder males spent less time on the food patch, remated with the resident females at lower frequencies and fathered a smaller proportion of offspring when the focals males remained in the arenas than when we removed the focal males. Our results reveal a novel adaptive function of aggression in fruit flies: in addition to fighting to defend attractive food sources that attract prospective mates, males rely on aggression to guard their mates, and such mate guarding enhances their fitness.

A critical question in the study of the evolution of cognition and the brain concerns the extent to which variation in cognitive processes and associated neural mechanisms is adaptive and shaped by natural selection. In order to be available to selection, cognitive traits and their neural architecture must show heritable variation within a population, yet heritability of cognitive and neural traits is not often investigated in the field of behavioral ecology. In this commentary, we outline existing research pertaining to the relative influences of genes and environment in cognitive and underlying neural trait variation, as well as what is known of their heritable genetic architecture by focusing on several cognitive traits that have received much attention in behavioral ecology. It is important to demonstrate that cognitive traits can respond to selection, and we advocate for an increased emphasis on investigating trait heritability for enhancing our understanding of the ecological, genetic and neurobiological mechanisms that have shaped interspecific and intraspecific variation in cognitive traits.

Mate choosiness by males has been documented in many taxa but we still do not know how it varies with age even though such variation can be important for our understanding of sexual selection on females. Theory provides conflicting predictions: young males, who are less attractive to females than older males, may be less choosy, or older males, who face fewer expected future mating opportunities, may be less choosy. In our experiments with fruit flies (Drosophila melanogaster), young (1-d-old) males spent relatively less time courting recently mated females than did mature (4-d-old) males. Overall, there was a gradual decline in male mate choosiness from age 1–7 d. As male age was correlated with the duration of deprivation from females, we tested for the effect of deprivation and found that same-age males previously exposed to females were choosier than female-deprived males. We also assessed key male parameters that could affect choosiness and found that, compared to mature males, young males were less attractive to females, less competitive in intramale interactions and less fertile. Although the lesser attractiveness and competitiveness should select for lesser mate choosiness in young males, their limited fertility and more expected future mating opportunities seem to override the other factors and lead to high mate choosiness in young males. Overall, our data indicate that young males just after reaching sexual maturity are choosy and that subsequent exposure to females can maintain high levels of male mate choosiness with age. Hence, males can contribute much more to sexual selection than previously appreciated.

Mate choice by males has been documented in many taxa including fruit flies (Drosophila spp.). It is still unclear, however, whether male mate choice varies much with age and one cannot readily predict the direction of change in male choosiness with age. We compared mate choice in young (1 day old) and mature (4 days old) male fruit flies (Drosophila melanogaster). Young males spent much less time courting heterospecific females than did mature males, but both male categories spent similar time courting conspecific females. We obtained similar results indicating higher selectivity of young than mature males in descendants of wild-caught flies, when males had an opportunity to learn to avoid heterospecific females and when males had a choice between courting conspecific and heterospecific females. The common methodology in the discipline has been to let virgin flies age for at least a few days prior to their use in experiments. Our experiments, which employed protocols sensitive to male age and experience, suggest that male fruit flies may be more choosy than previously thought and hence can contribute much more to sexual selection and incipient speciation than previously appreciated.

Selecting food items and attaining a nutritionally balanced diet is an important challenge for all animals including humans. We aimed to establish fruit fly larvae (Drosophila melanogaster) as a simple yet powerful model system for examining the mechanisms of specific hunger and diet selection. In two lab experiments with artificial diets, we found that larvae deprived of either sucrose or protein later selectively fed on a diet providing the missing nutrient. When allowed to freely move between two adjacent food patches, larvae surprisingly preferred to settle on one patch containing yeast and ignored the patch providing sucrose. Moreover, when allowed to move freely between three patches, which provided either yeast only, sucrose only or a balanced mixture of yeast and sucrose, the majority of larvae settled on the yeast-plus-sucrose patch and about one third chose to feed on the yeast only food. While protein (yeast) is essential for development, we also quantified larval success on diets with or without sucrose and show that larvae develop faster on diets containing sucrose. Our data suggest that fruit fly larvae can quickly assess major nutrients in food and seek a diet providing a missing nutrient. The larvae, however, probably prefer to quickly dig into a single food substrate for enhanced protection over achieving an optimal diet.

Learning and memory require the development, modification and maintenance of brain tissue, which cost time and energy. It may be adaptive for developing animals to adjust such investments based on environmental cues indicating the future utility of learning. The optimal learning ability that maximizes fitness will vary with the degree of complexity or difficulty of the environment, and developing animals may show an adaptive plastic modification of the extent of their learning ability based on early-life cues of environmental complexity. We tested whether fruit fly larvae reared in a ‘complex’ environment, where they had to search, sample and choose between three foods differing in flavour and bitterness subsequently possessed greater learning abilities than larvae reared in a simple environment with only one food type. We tested learning ability both at the larval stage and in young adults. Our results suggest that, despite theoretical and intuitive appeal, these environmental factors did not affect learning ability.

Although learned mate preferences are suspected to have important effects during speciation, theoretical models have largely neglected the effects on speciation and population divergence of within-generational learning, that is, learning based upon prior experience with potential mates. Here, we use population genetic models to address this deficit. Focusing on the situation of secondary contact between populations that still hybridize, we consider models of learning by females and by males under polygyny. We assess the effects of learning to prefer conspecifics from previous conspecific encounters, learning to avoid heterospecifics from previous heterospecific encounters, and learning to prefer familiar types. We examine the amount of population divergence that results from learning in these models. We also assess the effect of learning on the spread of an allele that strengthens assortative mating in both models. We find that learning can have counterintuitive, but logical and understandable effects that differ with the version of the model assessed. In general, population divergence is expected to increase most consistently when females learn to strengthen their preferences for conspecifics from previous encounters with conspecifics. Our results also suggest that within-generational learning will generally inhibit the spread of alleles strengthening assortative mating.

All animals are highly plastic and rely on the modulation of gene action, physiology and behaviour to continuously modify their phenotypes. Compared to other types of plasticity, learning, defined as the internal representation of novel information, allows animals to better exploit environmental features unique to certain times and places. This distinctive property of learning gives it an enormous potential to promote evolution through increased robustness, innovation and speciation rate. First, learning can enhance robustness because it allows individuals to adopt new resources and avoid novel threats. Empirical examples include the modification of egg-laying timing and nesting site selection in birds and of egg-laying substrate choice in insects. Second, learning can lead to innovation because it often has an exploratory stage that can lead to the discovery and refinement through trial and error of new, fitness-enhancing features. The best examples are cases of social learning that lead to the exploitation of novel food sources followed by genetic changes that optimize use of the new diet. Finally, learning can increase the levels of assortative mating that lead to population divergence either when young imprint on their parents or when individuals restrict their mate choice criteria based on interactions with prospective mates. While the notion that learning can have strong effects on evolution is backed by theory and some data, we currently lack broad experimental evidence to support that claim.

Neurogenetic research in fruit flies (Drosophila melanogaster) has established numerous protocols that illustrate flies' rich behavioural repertoire as well as excellent learning and memory abilities. To place that information in an evolutionary context, we followed up on earlier studies by evaluating the effect of experience with a variety of relevant female categories on males' courtship behaviour. We found, for the first time, that the experience of mating with conspecific females caused males to subsequently show lower levels of courtship towards heterospecific females compared to control males. These courtship levels, however, were higher than those of males that had experienced rejection by heterospecific females. Courtship reduction was selective: males that mated conspecifically did not subsequently show low levels of courting other conspecific females, and males that were rejected by recently mated conspecific females did not show low levels of courting heterospecific females. Interestingly, males that mated with virgin conspecifics and males that were rejected by virgin heterospecifics subsequently showed similar levels of low courtship towards recently mated conspecific females, suggesting that males find mated females unattractive after encountering virgin females. Males, however, showed higher levels of courtship towards mated females after mating with simulated mated females than after mating with control virgin females. Overall, our results indicate that adaptive use of learning by male fruit flies enhances mating success and reduces time and effort pursuing relatively less desirable or attainable females.

Male fruit flies (Drosophila melanogaster) force-copulate with females during the females' short vulnerable period following eclosion. Although sexually immature at that time, the females produce viable progeny from forced copulations. While the females could gain fitness from remating with their chosen male when reaching sexual maturity, mating in female fruit flies is typically followed by a long period of reduced attractiveness and receptivity. To test whether forcibly mated females can overcome the typical effects of mating, we quantified the effects of consensual versus forced matings on female attractiveness and receptivity. Forcibly mated females were as attractive to males as same-age virgin females and more attractive than consensually mated females. The forcibly mated females, however, remated at lower frequencies than same-age virgin females but at higher frequencies than consensually mated females. Our results suggest an intriguing outcome of sexual conflict in which males can sire offspring with and reduce the receptivity of forcibly mated females, but these females can retain their attractiveness and partial receptivity to males.

Forced copulation, which is perhaps the most extreme form of sexual conflict, is ubiquitous among many species including humans. To better understand the evolution and maintenance of forced copulations, it is imperative to assess their costs and benefits. We followed up on recent studies indicating frequent forced copulations in two wild populations of fruit flies, Drosophila melanogaster, and quantified their effects on males and females under controlled laboratory settings. Compared to females that mated consensually, females that were forcibly mated had fewer progeny, higher mortality rates and higher frequencies of wing damage that prevented flight. Males that forcibly copulated fathered much fewer progeny than did males that mated consensually. The reasons for the relatively small reproductive gains to males from forced copulations were the lower female fertility and higher female mortality from forced than consensual copulations as well as the higher frequencies of rematings by females that were forcibly copulated. It is likely that males attempt to force-copulate in spite of the low potential reproductive gain because of the scarcity of sexually receptive females and the consequent low probability of attaining the high fitness associated with consensual matings.

As a part of our research on the evolution of social learning in insects, we examined socially influenced behaviour and social learning in desert locust (Schistocerca gregaria) nymphs and adults. In the nymphs, the only positive effect we documented was an increased tendency to feed while in the company of another locust than alone. The adults, on the other hand, showed significant preference for joining others (local enhancement) in both the contexts of feeding and egg laying. Neither nymphs nor adults, however, showed social learning. Our preliminary analyses pointed to locusts as a likely insect that might possess social learning. Our research, when taken together with research on phase-shifts and swarm ⁄marching behaviour of gregarious locusts, suggests that the behavioural dynamics of gregarious locusts may make local enhancement but not social learning beneficial. The possible difference we documented between the nymphs and adults could enable us to further explore the proximate and ultimate mechanisms that underlie socially influenced behaviour.

Learning in the context of mate choice is important because it can influence sexual selection and incipient speciation. While fruit flies (Drosophila spp.) have been a key model system for research on sexual selection, speciation and learning, much of the research on fruit fly learning in the context of sexual behaviour has focused on males even though females typically control mating decisions. In a series of experiments, we found no evidence that early experience with either only conspecific males or both conspecific and heterospecific males affected the frequency of heterospecific matings by female Drosophila pseudoobscura. We conducted further experiments to place our results in perspective. First, we tested whether heterospecific matings do not induce female unreceptivity and thus have little cost, in which case learning would be of little benefit. Contrary to our prediction, we found that females that had initially mated heterospecifically remated conspecifically at a lower frequency than females that had first mated conspecifically. Second, we replicated earlier data indicating that male D. pseudoobscura that are rejected by heterospecific females later selectively reduce courtship of heterospecific females. Finally, we tested whether females can learn as well as males in a nonsexual context involving learning to avoid odours associated with danger and found similar learning scores in females and males. Our results indicate that, in spite of the potential benefits from learning in the context of mate choice and possessing a good learning ability in another domain, female D. pseudoobscura either do not learn about potential mates or such learning is not as robust as it is in the males.

Nonrepairable body damage such as tooth and wing wear commonly occur in animals and can dramatically alter their behaviour. We critically examined the effects of nonrepairable damage in a model system that enabled us to separate the effects of damage from other correlated effects of senescence. Compared to sham controls, honeybees with 20% of their front wings trimmed continued to forage at similar rates and reduced their net rate of food delivery by approximately 20%. The changes in flight behaviour allowing the foragers to cope with the substantial wing damage probably occurred immediately following wing trimming. Bees showed no increase in foraging performance either in successive trips or during the 2 days following wing trimming. The cost of maintaining relatively high foraging performance after sustaining severe wing damage was approximately a 20% increase in mortality rate, most likely owing to predation. Our results illustrate a remarkable versatility of honeybees’ flight behaviour, which allows them to handle the inevitable nonrepairable body damage that naturally occurs with ageing.

Extensive research indicates that sexually mature female fruit flies typically choose with whom to mate, a process that is crucial for the operation of sexual selection and population divergence via female choice. We followed up on field data suggesting that male fruit flies (Drosophila melanogaster) force copulate with teneral females, which are recently eclosed females characterized by their folded wings and soft, light coloured bodies. Our results indicated that males succeeded in mating with about 20% of the teneral females from our Canton-S population and 15% of the teneral females from a local, wild-caught D. melanogaster population. Males were most likely to mate with recently eclosed females and failed to mate with females older than 1 h posteclosion. Close behavioural observations indicated coercion by the males and resistance by the teneral females. The teneral females continued to fight off males throughout copulation and this probably contributed to the shorter mating duration of teneral females relative to that of mature females. Although teneral females failed to foil some forced copulation attempts, they could reduce the impact of such copulations by subsequently remating with a male of their choosing. Indeed, tenerally mated females were six times more likely to remate than were control females that had mated when mature. Our results substantiate a novel aspect of sexual conflict in fruit flies, which could counteract processes driven by female mate choice.

Honeybees in natural settings show a gradual increase in foraging performance similar to the general pattern of lifetime performance seen in a wide variety of animals including humans. To quantify the factors contributing to such gradual increase in foraging success, we studied bumblebees foraging on pepper plants inside a greenhouse. This allowed us to combine the global measure of the net rate of food delivery to the hive with a detailed examination of bees’ performance at flowers over time. Although bees exhibited short-term improvements in foraging ability during their first few foraging trips, we did not observe the predicted long-term increase in performance over days. Our results suggest that a variety of flower-handling tasks, flower choice and movements between plants can be learned quickly under the simple greenhouse settings. The long-term increase in performance under natural settings may be caused by factors including spatial orientation and locating the best plant species, flower patches and individual plants over a large area.

The mechanisms maintaining homosexual behaviour in animals are not well understood. In fruit flies, where male–male courtship is prevalent, it has been suggested that young males gain from being courted by mature males, perhaps through learning. I conducted two series of experiments to critically examine why mature males court immature males and what immature males may gain from such courtship. The results indicate that mature males do not identify the sex of the sexually ambiguous immature males and find them attractive even after substantial experience. These findings agree with recent research indicating that males initially court a broad range of potential mating targets and then narrow their courtship focus based on their experience of being rejected by classes of flies such as recently mated females or heterospecific females, which are clearly identified by their distinct pheromonal profiles. Compared to inexperienced males, males that either had received courtship when immature or had been housed with mature males when young did not have either higher mating frequencies or shorter mating latencies but spent more time courting females. Such higher courtship intensities may translate into a mating advantage in some settings. It appears that young males that interact with mature males develop into a sexually aggressive phenotype, which could better prepare them to compete for females.

Social learning, defined as learning from other individuals, has had dramatic effects on some species, including humans, in whom it has generated a rich culture. As a first step in examining the evolution of and mechanisms underlying social learning in insects, we tested for social learning in fruitflies ( Drosophila melanogaster ). Focal females (observers) that experienced novel food together with mated females (models), who had laid eggs on that food, subsequently exhibited a stronger preference for laying eggs on that food over another novel food compared with focal females that experienced the food alone. We observed no social learning, however, when observers experienced food with potentially more ambiguous social information provided by the presence of either virgin models or aggregation pheromone. This first documentation of social learning about egg-laying substrates in fruitflies builds on recent data indicating intricate use of social information by fruitflies and opens up exciting avenues for research on the evolution and neurogenetics of social learning using biology's major model system.

Socially influenced learning is important because it can drive the spread of novel behaviours among individuals within and between generations. While work on a few vertebrates suggests the conditions favouring the use of social over individual learning, we know little about the evolution of social learning. As a part of an ongoing examination of the evolutionary roots of social learning in insects, we tested for social learning in locusts, Locusta migratoria. Locusts showed rapid individual learning, preferring a diet they ate for a single meal of only 20 min over another diet of equal nutritional quality. Locusts, however, did not show stronger preference for novel food that they had previously consumed while in the presence of a conspecific experienced with that food. Furthermore, focal locusts did not learn about novel food from (1) experienced conspecifics that were observable through a screen, (2) interactions with conspecifics that had previously fed on and gave off odours from novel food and (3) cannibalizing conspecifics that had recently fed on novel food. Whereas our results extend previous work indicating excellent individual learning in locusts, they provide no evidence for socially influenced learning in a species that, in its gregarious form, has the opportunity for social learning and could benefit from such an ability.

We compared the performance of Bayesian learning strategies and approximations to such strategies, which are far less computationally demanding, in a setting requiring individuals to make binary decisions based on experience. Extending Bayesian updating schemes, we compared the different strategies while allowing for various implementations of memory and knowledge about the environment. The dynamics of the observable variables was modeled through basic probability distributions and convolution. This theoretical framework was applied to the problem of male fruit flies who have to decide which females they should court. Computer simulations indicated that, for most parameter values, approximations to the Bayesian strategy performed as well as the full Bayesian one. The linear approximation, reminiscent of the linear operator, was notably successful, and, without innate knowledge, the only successful learning strategy. Besides being less demanding in computation and thus realistic for small brains, the linear approximation was also successful at limited memory, which would translate into robustness in rapidly changing environments. Knowledge about the environment boosted the performance of the various learning strategies with maximal performance at large utilization of memory. Only for limited memory capacities, intermediate knowledge was most successful. We conclude that many animals may rely on algorithms that involve approximations rather than full Bayesian calculations because such approximations achieve high levels of performance with only a fraction of the computational requirements, in particular for extensions of Bayesian updating schemes, which can represent universal and realistic environments.

Recent research indicating learning in the context of sexual behaviour in fruit flies suggests that learning could increase levels of assortative mating between partially diverged populations. We present a graphic model examining the role of learning and a series of experiments evaluating assumptions and predictions of the model. We found that male Drosophila persimilis that previously succeeded in mating with females of the sibling species, D. pseudoobscura, did not have a higher heterospecific mating success than males that were either virgin or previously mated with conspecific females. On the other hand, female D. pseudoobscura with apparently strict mating criteria, which rejected heterospecific males, were also more likely to reject conspecific males than were females inexperienced with males. Finally, D. persimilis males previously rejected by heterospecific females courted significantly less and had half as much heterospecific mating success as males previously accepted by heterospecific females. These results, combined with previous evidence demonstrating that males rejected by heterospecific females learn to avoid courting such females, indicate that learning can increase phenotypic divergence between populations with partial pre-mating isolation.

Honeybees, Apis mellifera, who show temporal polyethism, begin their adult life performing tasks inside the hive (hive bees) and then switch to foraging when they are about 2–3 weeks old (foragers). Usually hive tasks require little or no flying, whereas foraging involves flying for several hours a day and carrying heavy loads of nectar and pollen. Flight muscles are particularly plastic organs that can respond to use and disuse, and accordingly it would be expected that adjustments in flight muscle metabolism occur throughout a bee’s life. We thus investigated changes in lifetime flight metabolic rate and flight muscle biochemistry of differently aged hive bees and of foragers with varying foraging experience. Rapid increases in flight metabolic rates early in life coincided with a switch in troponin T isoforms and increases in flight muscle maximal activities (V max) of the enzymes citrate synthase, cytochrome c oxidase, hexokinase, phosphofructokinase, and pyruvate kinase. However, further increases in flight metabolic rate in experienced foragers occurred without additional changes in the in vitro V max of these flight muscle metabolic enzymes. Estimates of in vivo flux (v) compared to maximum flux of each enzyme in vitro (fractional velocity, v/V max) suggest that most enzymes operate at a higher fraction of V max in mature foragers compared to young hive bees. Our results indicate that honeybees develop most of their flight muscle metabolic machinery early in life. Any further increases in flight metabolism with age or foraging experience are most likely achieved by operating metabolic enzymes closer to their maximal flux capacity.