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The diversity of sexual traits favoured by females is enormous and, curiously, includes preferences for males with rare or novel phenotypes. We modelled the evolution of a preference for rarity that yielded two surprising results. First, a Fisherian ‘sexy son’ effect can boost female preferences to a frequency well above that predicted by mutation–selection balance, even if there are significant mortality costs for females. Preferences do not reach fixation, however, as they are subject to frequency-dependent selection: if choosy females are too common, then rare genotypes in one generation become common, and thus unattractive, in the offspring generation. Nevertheless, even at relatively low frequency, preferences maintain polymorphism in male traits. The second unexpected result is that the preferences can evolve to much higher frequencies if choice is hindered, such that females cannot always express their preferences. Our results emphasize the need to consider feedback where preferences determine the dynamics of male genotypes and vice versa. They also highlight the similarity between the arbitrariness of behavioural norms in models of social evolution with punishment (the so-called ‘folk theorem’) and the diversity of sexual traits that can be preferred simply because deviating from the norm produces unattractive offspring and is, in this sense, ‘punished’.

An increasing number of studies find females to base their mate choice on several cues. Why this occurs is debated and many different hypotheses have been proposed. Here I review the hypotheses and the evidence in favour of them. At the same time I provide a new categorisation based on the adaptiveness of the preferences and the information content of the cues. A few comparative and empirical studies suggest that most multiple cues are Fisherian attractiveness cues or uninformative cues that occur alongside a viability indicator and facilitate detection, improve signal reception, or are remnants from past selection pressures. However, much evidence exists tor multiple cues providing additional information and serving as multiple messages that either indicate general mate quality or enable females that differ in mate preferences to choose the most suitable male. Less evidence exists for multiple cues serving as back-up signals. The importance of receiver psychology, multiple sensory environments and signal interaction in the evolution of multiple cues and preferences has received surprisingly little attention but may be of crucial importance. Similarly, sexual conflict has been proposed to result in maladaptive preferences for manipulative cues, and in neutral preferences for threshold cues, but no reliable evidence exists so far. An important factor in the evolution of multiple preferences is the cost of using additional cues. Most theoretical work assumes that the cost of choice increases with the number of cues used, which restricts the conditions under which preferences for multiple cues are expected to evolve. I suggest that in contrast to this expectation, the use of multiple cues can reduce mate choice costs by decreasing the number of mates inspected more closely or the time and energy spent inspecting a set of mates. This may be one explanation for why multiple cues are more common than usually expected. Finally I discuss the consequences that the use of multiple cues may have for the process of sexual selection, the maintenance of genetic variation, and speciation.

Fitness costs of signalling are essential in order for reliable sexual signalling to prevail when the interests of the sexes conflict. This means that signalling can be subjected to a life history trade-off between present and future signalling effort. Here, I show that three-spined stickleback males (Gasterosteus aculeatus), who have a single breeding season during which they breed repeatedly, change their red nuptial coloration over the season depending on their body size at the start of breeding. Large males that completed several breeding cycles increased their red coloration over the season, whereas small males, who completed only a few cycles, did not. The increase in coloration was accompanied by an increase in parental success when males were energy constrained, but not when they had access to an unlimited food supply. Red coloration was thus an honest signal of male parental ability despite changes in signal expression when both signalling and parental care were costly and the investments in them changed simultaneously over the reproductive lifetime. However, the honesty of the signal varied over a lifetime. At the penultimate cycle, bright males cannibalized some of their eggs, probably to increase survival to the last cycle, whereas males cared for their offspring independent of coloration at the ultimate cycle.

Adaptation does not necessarily lead to traits which are optimal for the population. This is because selection is often the strongest at the individual or gene level. The evolution of selfishness can lead to a ‘tragedy of the commons’, where traits such as aggression or social cheating reduce population size and may lead to extinction. This suggests that species-level selection will result whenever species differ in the incentive to be selfish. We explore this idea in a simple model that combines individual-level selection with ecology in two interacting species. Our model is not influenced by kin or trait-group selection. We find that individual selection in combination with competitive exclusion greatly increases the likelihood that selfish species go extinct. A simple example of this would be a vertebrate species that invests heavily into squabbles over breeding sites, which is then excluded by a species that invests more into direct reproduction. A multispecies simulation shows that these extinctions result in communities containing species that are much less selfish. Our results suggest that species-level selection and community dynamics play an important role in regulating the intensity of conflicts in natural populations.

Many hypotheses have been proposed to explain multiple mating in females. One of them is bet hedging, that is avoiding having no or very few offspring in any given generation, rather than maximizing the expected number of offspring. However, within-generation bet hedging is generally believed to be an unimportant evolutionary force, except in very small populations. In this study, we derive predictions of the bet-hedging hypothesis for a case in which local insect populations are often small, offspring performance varies, for example, due to inbreeding depression, and the groups of gregarious larvae have to exceed a threshold size before they are likely to survive throughout the larval stage. These conditions exist for populations of the Glanville fritillary butterfly (Melitaea cinxia), potentially making bet-hedging benefits larger than usual. We observed matings in a field cage, which allowed detailed observations under practically natural conditions, and analyzed genetic paternity of egg clutches laid by females under direct observation. The egg-laying and survival patterns are in line with the predictions, supporting the hypothesis that multiple mating in M. cinxia presents a rare case of within-generation bet hedging.

Divorce in socially monogamous species can result from different mechanisms, for example, chance events, active desertion of the partner, or the intrusion of a third individual ousting the partner. We compared the predictions associated with such mechanisms with data from common guillemots (Uria aalge) breeding on the Isle of May, Scotland. The data cover the years 1982--2005 and show a yearly divorce rate of 10.2%. In most divorces (86%), one of the original partners moved to another breeding site, whereas the other bird stayed and bred with a new partner. On average, movers had a significantly lower breeding success after divorce, stayers were largely unaffected, whereas the incoming birds benefited significantly from the change. This pattern fits best the predictions of the "forced-divorce" hypothesis, suggesting that many divorces were caused by incoming birds rather than the original partners or chance events. Although we are unable to document the precise behavioral sequence that led to divorces, our interpretation is supported by observations of frequent fights over breeding-site ownership. Our data also indicate within-population diversity of divorce mechanisms: some divorces were apparently accidental, others desertion of partners and sites if the latter were of low quality. Our study finally illustrates that a negative correlation between breeding success and probability of divorce (which our data show) need not indicate the adaptiveness of divorce for the original partners. Because such a connection has often been made, adaptive divorce may in general be less common than usually assumed. Copyright 2007, Oxford University Press.

Models of population dynamics generally neglect the presence of males. While this assumption holds under many circumstances, behavioural ecology increasingly tells that the presence (or absence) of males may have an impact on female fitness, and hence population sizes. Here we ask the question of whether males matter to population dynamics, operationally defined as a dependency of population growth on the relative density of males. We provide simple models, and evaluate the current 8 empirical evidence for them, that illustrate various mechanisms of such male influence: mate searching behavior, male resource use (including effects of sexual dimorphism), sexual harassment and sexual segregation. In each case, theory predicts that males can have an effect on population densities, and in some extreme cases a positive feedback between an increasingly male-biased sex ratio and the effects on female harassment may theoretically even bring about population extinction. The results of this study, and the literature reviewed, show that the males can have a substantial effect on population dynamics, particularly so when human influences result in biased sex ratios.

In a seminal paper, Hammerstein and Parker (1987) described how sex roles in mate searching can be frequency dependent: the need for one sex to perform mate searching is diminished when the opposite sex takes on the greater searching effort. Intriguingly, this predicts that females are just as likely to search as males, despite a higher potential reproductive rate by the latter sex. This prediction, however, is not supported by data: male mate searching prevails in nature. Counterexamples also exist in the empirical literature. Depending on the taxon studied, female mate searching can arise in either low- or high-density conditions, and suggested explanations differ accordingly. We examine these puzzling observations by building two models (with and without sperm competition). When sperm competition is explicitly included, male mate searching becomes the dominant pattern; when it is excluded, male mate searching predominates only if we assume that costs of searching are higher for females. Consequently, two hypotheses emerge from our models. The multiple-mating hypothesis explains male searching on the basis of the ubiquity of sperm competition, and predicts that female searching can arise in low-density situations in which sperm can become limiting. It can also explain cases of female pheromone production, where males pay the majority of search costs. The sex-specific cost hypothesis predicts the opposite pattern of female searching in high-density conditions, and it potentially applies to some species in which sperm limitation is unlikely.

Female mate choice influences the maintenance of genetic variation by altering the mating success of males with different genotypes. The evolution of preferences themselves, on the other hand, depends on genetic variation present in the population. Few models have tracked this feedback between a choice gene and its effects on genetic variation, in particular when genes that determine offspring viability and attractiveness have dominance effects. Here we build a population genetic model that allows comparing the evolution of various choice rules in a single framework. We first consider preferences for good genes and show that focused preferences for homozygotes evolve more easily than broad preferences, which allow heterozygous males high mating success too. This occurs despite better maintenance of genetic diversity in the latter scenario, and we discuss why empirical findings of superior mating success of heterozygous males consequently do not immediately lead to a better understanding of the lek paradox. Our results thus suggest that the mechanisms that help maintain genetic diversity also have a flipside of making female choice an inaccurate means of producing the desired kind of offspring. We then consider preferences for heterozygosity per se, and show that these evolve only under very special conditions. Choice for compatible genotypes can evolve but its selective advantage diminishes quickly due to frequency-dependent selection. Finally, we show that our model reproduces earlier results on selfing, when the female choice strategy produces assortative mating. Overall, our model indicates that various forms of heterozygote-favouring (or variable) female choice pose a problem for the theory of sexual ornamentation based on indirect benefits, rather than a solution.

Game theory models of sperm competition predict that within species, males should increase their sperm expenditure when they have one competitor, but decrease expenditure with increasing numbers of competitors. So far, there have been few tests or support for this prediction. Here, we show that males of a freshwater fish, the European bitterling, Rhodeus sericeus, do indeed adjust their ejaculation rate to the number of male competitors by first increasing and then decreasing their ejaculation rates as the number of competitors increases. However, this occurred only under restricted conditions. Specifically, the prediction was upheld as long as no female had deposited eggs in the live mussels that are used as spawning sites. After one or more females had spawned, males did not decrease their ejaculation rates with the number of competitors, but instead they became more aggressive. This indicates that decreased ejaculation rate and increased aggression are alternative responses to increased risk of sperm competition.

Experiments are often carried out in the laboratory under arti®cial conditions. Although this can control for confounding factors, it may eliminate important factors that under natural conditions mediate the interaction under investigation. Here, we show that different results can be gained in the ®eld and in the laboratory regarding host±parasite interaction. In the ®eld, courting three-spined stickleback males, Gasterosteus aculeatus, were less often infected with plerocercoids of a cestode tapeworm, Schistocephalus solidus, than shoaling males. However, when a random sample of males was allowed to nest and court females in individual aquaria in the laboratory, both uninfected and infected males built nests and courted females. Moreover, while the few infected males that courted females in the ®eld expressed less red nuptial coloration than uninfected courting males, there was no difference in redness between infected and uninfected males in the laboratory. We argue that the different results gained in the ®eld and in the laboratory are due to differences in the cost of reproduction, due to differences in the resource pool of the males. The favourable conditions in the laboratory exclude factors such as predation risk, social interactions, and ¯uctuating environmental conditions that may use up resources in the ®eld and mediate the effect of the parasite.

For signalling to be honest the handicap principle claims that signals must impose fitness costs so that only the best individuals can afford the most exaggerated signals. The cost of signalling in terms of reduced survival decreases, however, towards the end of an individual’s lifetime, which can induce an increase in signalling effort as a terminal effort. I show for the three-spined stickleback, Gasterosteus aculeatus, that a decrease in survival prospects through impaired condition leads to an increase in red nuptial coloration that makes the signal less reliable as an indicator of male parental ability. Males in poor condition with a large signal sometimes cannibalized all the eggs they received, probably to start a new breeding cycle with a higher energy reserve. However, the inclusion of socially imposed costs of signalling through male–male competition during courtship increased the honesty of the signal, as some males in poor condition and of poor parental ability decreased their signal expression. Some cheaters still occurred, but the signalling system was honest on average. This implies that socially imposed costs are important in the maintenance of honest sexual signalling. Dishonesty may occur under favourable conditions when the cost of signalling is reduced. This emphasizes the importance of considering the environmental conditions experienced by individuals when investigating the evolution and maintenance of honest sexual signals.

In many species, secondary sexual characteristics are used in both male-male competition and in attracting females. This suggests that social control of deception could contribute to the maintenance of honest sexual signalling. In the three-spined stickleback Gasterosteus aculeatus, male red breeding coloration plays a dual role in sexual selection by functioning as both a threat signal in male-male competition and as a cue for female choice. To investigate whether male competition determines the level of signalling, the expression of red coloration and courtship activity were recorded both before and after male interactions. The results show that male competition influences signal expression by increasing the difference between males in signalling level. This in turn facilitates female choice and induces a preference for dominant males. Since a preference for dominant males may benefit females both directly and indirectly in this species with exclusively paternal care, male-male competition seems to increase the honesty of signalling and, thus, facilitates female choice in relation to male quality. This may increase the intensity of sexual selection and promote the evolution of breeding aggregations.

Reproductive activities often increase the susceptibility of individuals to predators. Individuals may be able to reduce this risk of predation, however, by their choice of breeding habitat, as the structural complexity of habitats is known to affect predator foraging success. Here we show that the presence of predators induces a preference for structurally complex nest sites over open ones in male three-spined sticklebacks, Gasterosteus aculeatus. To investigate whether this predator-induced nest site preference can decrease the known negative effect of predators on courtship activity, we recorded the reduction in courtship activity during predator presentations for males in vegetated and open nest sites. Habitat structure affected the response to a predator when males were in competition. A male in a vegetated site reduced courtship activity less than amale in an open site. Habitat had no effect on courtship when males were solitary, however. This suggests that male–male competition and the possibility of losing mating opportunities to other males affect risk taking. Females, who were unaware of the predator, preferred the male in the vegetated site, which showed less reduction in courtship, when the males were exposed to a predator, but chose randomly between the males when the predator was absent. Thus, a preference for vegetated nest sites under predation risk may be beneficial not only by increasing the probability of survival, but also by reducing the negative impact of predators on courtship activity and mating probability.

An increasing number of studies show that animals adjust their reproductive effort to the risk of predation. However, to maximize lifetime reproductive success this adjustment should depend on the animal9s current and future reproductive potential. Here I tested this hypothesis by allowing threespine stickleback males ( Gasterosteus aculeatus ), differing in current and future mating probabilities, to reproduce in pools in both the presence and absence of predators. As expected, males adjusted their reproductive effort to the risk of predation. Fewer males bred, and all males developed less nuptial coloration in the presence of predators. However, males with a low current mating probability took less risk than males with a higher mating probability, whereas all males increased risk taking when future reproductive opportunities decreased. The results thus support the hypothesis that males are able to assess both the risk of predation and their current versus future mating probability, and adjust their reproductive decisions accordingly. The study further suggests that predation risk may have less effect on sexual selection than previously assumed, as the males which refrained from reproducing in the presence of predators were mainly males with a low mating probability.