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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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Recent data indicating that male fruit flies adaptively reduce courtship of heterospecific females, which typically reject them, suggest that learning could contribute to reduced levels of matings between individuals from diverging populations with partial premating isolation. To further examine the robustness of learning in the context of courtship in fruit flies, I wished to broaden the types of experience provided to males prior to testing. In both Drosophila persimilis and D. pseudoobscura, alternating trials of mating with conspecific females and rejection by heterospecific females produced the strongest reduction in heterospecific courtship. Trials of rejection by heterospecific females produced equally strong reduction in heterospecific courtship in D. persimilis but not in D. pseudoobscura, whereas trials of mating with conspecific females did not reduce heterospecific courtship at all. The pattern of strong reduction in heterospecific courtship was also replicated when I simulated the likely natural scenario in which males interact with conspecific females since eclosion and later encounter and experience rejection by heterospecific females. The results indicate that a variety of relevant experiences cause a rapid decrease in the time that male fruit flies spend courting heterospecific females. Such learning in partially reproductively isolated populations could contribute to speciation.

Life history research has mostly neglected learning even though it is probably a major contributor to lifetime performance in a variety of animals. As part of an ongoing project evaluating the relative contribution of learning, physiology and effort to performance throughout the life span, I quantified lifetime performance of honeybees, Apis mellifera, foraging at a feeder. Unlike natural foraging, where bees may learn a variety of features that contribute to increased performance, food collection from a feeder requires little learning. Foragers showed no long-term change in the rate of food delivery, a pattern that was different from published data indicating a long-term gradual increase in foraging performance in honeybees under natural settings. The discrepancy between bees' lifetime performance in the artificial versus natural settings suggests that learning is the key component contributing to the increase in performance throughout a forager's life as observed in the field.

Experiments indicating learning in the context of courtship in fruit flies challenge the prevailing views that male insects are either indiscriminate or rely on innate rules for courtship. We investigated the conditions favouring learning during courtship in insects by using a model that compared a learning strategy to two alternatives, indiscriminate courtship and innate selectivity. Our analyses indicated that, under the two conditions of high encounter rates with females and long courtship durations, indiscriminate courtship resulted in much lower lifetime mating success than either selectivity or learning. Learning had moderate advantages over selectivity when encounter rates with females were high, when a large proportion of females were sexually receptive, and when acceptance rates by sexually receptive females were high. We predict that species in which such conditions commonly occur are most likely to show learning in the context of male courtship.

Much of the research on learning in fruit flies has focused on the genetic and cellular basis of learning. The evolutionary relevance of learning in these tiny, short-lived insects is not well understood. Relying on the knowledge that male fruit flies learn in the context of courtship, I tested whether such learning improves male courtship. I found, first, that compared with inexperienced males, males with experience courting recently mated, unreceptive females were slower to begin courtship of novel recently mated females and spent less time courting such females. The experienced males, however, began courting virgin females sooner than did inexperienced males and courted such females as long as did inexperienced males. Second, compared with males experienced with recently mated females, males experienced with immature, unreceptive females were faster to approach either virgin or recently mated females and courted virgin females longer. These results indicate that courting experience permits male fruit flies to refine their courtship behaviour in a way that could increase their mating success.

Like most animals, honeybees, Apis mellifera, possess a suite of antipredatory adaptations used to defend their colony against intruders and to avoid flowers associated with predation risk. Honeybees also possess a remarkable ability to communicate the direction, distance and relative profitability of flower patches to hivemates using the well-studied waggle dance. Here we show that honeybees returning from foraging on dangerous flowers are less likely to perform the waggle dance and engage in fewer waggle runs than foragers returning from equally rewarding, safe flowers. Our results indicate that experienced foragers effectively steer naive recruits away from dangerous flowers and raise interesting questions as to how information about the reward and risk properties of patches are integrated into the waggle dance.

The types of interactions between learning events can significantly affect the value of learning. Learning one task may enhance the learning of a subsequent task (transfer), but the learning of a new task may also interfere with the memory of a previously learned task. Bumblebees, Bombus occidentalis, were tested for the magnitudes of transfer and interference between two related learning events. On the one hand, bees showed no evidence for positive transfer from one learning task to another. On the other hand, bees showed an initial reduction in performance after switching from task 2 back to task 1. However, after being trained to switch back and forth between two tasks, bees no longer showed an initial reduction in performance after switching. The results suggest first, that bees cannot generalize from one learning incident to another in the manner required in this experiment, and second, that bees can learn to alternate between certain distinct tasks with no reduction in performance.

Psychological studies have established that the central nervous system cannot sustain vigilance for an extended period of time. The consequent vigilance decrement implies a gradual reduction in the ability to process information effectively. This may result in a reduced ability to detect hidden predators, locate cryptic food items or make successful behavioural decisions. A model incorporating parameters of vigilance decrement during foraging and vigilance recovery during rest predicts first, the optimal allocation of time between foraging activity and rest, and second, the optimal length of each foraging episode. For a given rate of vigilance recovery, the model predicts that both the optimal proportion of time devoted for foraging activity and the optimal length of a foraging bout should be decreasing functions of the rate of vigilance decrement. Because the rate of vigilance decrement is larger for more difficult tasks, both the total time spent foraging and the duration of each foraging episode should be smaller for more demanding foraging activities. It is suggested that vigilance decrement is a dominant factor determining temporal patterns of animal behaviour.