Roger Härdling

Female Polymorphism, Frequency Dependence, and Rapid Evolutionary Dynamics in Natural Populations

Rapid evolutionary change over a few generations has been documented in natural populations. Such changes are observed as organisms invade new environments, and they are often triggered by changed interspecific interactions, such as differences in predation regimes. However, in spite of increased recognition of antagonistic male‐female mating interactions, there is very limited evidence that such intraspecific interactions could cause rapid evolutionary dynamics in nature. This is because ecological and longitudinal data from natural populations have been lacking. Here we show that in a color‐polymorphic damselfly species, male‐female mating interactions lead to rapid evolutionary change in morph frequencies between generations. Field data and computer simulations indicate that these changes are driven by sexual conflict, in which morph fecundities are negatively affected by frequency‐ and density‐dependent male mating harassment. These frequency‐dependent processes prevent population divergence by maintaining a female polymorphism in most populations. Although these results contrast with the traditional view of how sexual conflict enhances the rate of population divergence, they are consistent with a recent theoretical model of how females may form discrete genetic clusters in response to male mating harassment.

Male mating constraints affect mutual mate choice: prudent male courting and sperm-limited females.

Costs of sperm production may lead to prudence in male sperm allocation and also to male mate choice. Here, we develop a life history–based mutual mate choice model that takes into account the lost‐opportunity costs for males from time out in sperm recovery and lets mate competition be determined by the prevailing mate choice strategies. We assume that high mating rate may potentially lead to sperm depletion in males, and that as a result, female reproduction may be limited by the availability of sperm. Increasing variation in male quality leads, in general, to increased selective mate choice by females, and vice versa. Lower‐quality males may, however, gain access to more fecund higher‐quality females by lowering their courting rate, thus increasing their sperm reserves. When faced with strong male competition for mates, low‐quality males become less choosy, which leads to assortative mating for quality and an increased mating rate across all males. With assortative mating, the frequency of antagonistic interactions (sexual conflict) is reduced, allowing males to lower the time spent replenishing sperm reserves in order to increase mating rate. This in turn leads to lower sperm levels at mating and therefore could lead to negative effects on female fitness via sperm limitation.

The evolution of repeated mating under sexual conflict

In insects, repeated mating by females may have direct effects on female fecundity, fertility, and longevity. In addition, a females remating rate affects her fitness through mortality costs of male harassment and ecological risks of mating such as predation. We analyse a model where these female fitness factors are put into their life‐history context, and traded against each other, while accounting for limitations because of mate availability. We solve analytically for the condition when female multiple mating will evolve. We show that the probability that a female mates with a courting male decreases with increases in population density. The extent of conflict between the sexes thus automatically becomes larger at higher densities. However, because at higher densities females meet males at a higher rate, the resulting ESS female remating rate is independent of population density. The female remating probability is in conflict with male adaptations that increase male mating rate by persuading or forcing females to mate, and also in conflict with male adaptations for protecting the own sperm from being removed by future female mates. We show that the relative importance of these conflicts depends on population density.

Nonrandom mating preserves intrasexual polymorphism and stops population differentiation in sexual conflict

Evolutionary conflict between the sexes is predicted to lead to sexual arms races in which male adaptations for acquiring mates (“offense” traits) are met by female counteradaptations—for example, to reduce mating rate (“defense” traits). Such coevolutionary chases may be perpetual. However, we show here that the coevolutionary process may also lead to a stable state in which multiple offense‐defense trait pairs are maintained. This type of polymorphism below the species level is a result of sexual conflict in combination with nonrandom mating. Our results show that if nonrandom mating occurs with respect to male and female conflict traits, genetic correlations will act to stabilize the trait frequencies so that all morphs are maintained. We discuss the results in special relation to the evolution of female polymorphism in diving beetles and argue that the process we describe may be a general force that maintains polymorphism in other taxa as well.

Priority versus Brute Force: When Should Males Begin Guarding Resources?

When should males begin guarding a resource when both resources and guarders vary in quality? This general problem applies, for example, to migrant birds occupying territories in the spring and to precopula in crustaceans where males grab females before they molt and become receptive. Previous work has produced conflicting predictions. Theory on migrant birds predicts that the strongest competitors should often arrive first, whereas some models of mate guarding have predicted that the strongest competitors wait and then simply usurp a female from a weaker competitor. We build a general model of resource guarding that allows varying the ease with which takeovers occur. The model is phrased in terms of mate‐guarding crustaceans, but the same logic can be applied to other forms of resource acquisition where priority plays a role but takeovers might be possible too. The race to secure breeding positions can lead to strong competitors (large males) taking females earliest, even though this means accepting a lower‐quality female. Paradoxically, this means that small males, which have fewer breeding opportunities, are more choosy than larger ones. Such solutions are found when takeovers are impossible. The easier the takeovers and the higher the rate of finding guarded resources, the more likely are solutions where guarding durations are short, where strong competitors begin guarding only just before breeding, and where they do this by usurping the resource. The relationship between an individual’s competitive ability and its timing of resource acquisition can also be nonlinear if takeovers are moderately common; if this is the case, then males of intermediate size guard the longest.

Dynamics of the Caring Family

When several individuals simultaneously provide for offspring, as in families, the effort of any one individual will depend on the efforts of the other family members. This conflict of interest among family members is made more complicated by their relatedness because relatives share genetic interest to some degree. The conflict resolution will also be influenced by the differences in reproductive value between breeders and helpers. Here, we calculate evolutionarily stable provisioning efforts in families with up to two helpers. We explicitly consider that the behavioral choices are made in a life‐history context, and we also consider how group sizes change dynamically; this affects, for example, average relatedness among group members. We assume two different scenarios: intact families in which the breeder is 100% monogamous and stepfamilies in which the breeder shifts mate between breeding events. The average relatedness among family members is allowed to evolve in concert with changes in provisioning effort. Our model shows that an individual’s provisioning effort is not easy to predict from either its relatedness to the offspring or its reproductive value. Instead, it is necessary to consider the inclusive fitness effect of provisioning, which is determined by a combination of relatedness, reproductive value, and the reproductive value of the offspring.

Parallel divergence in mate guarding behaviour following colonization of a novel habitat

Ecological factors can have profound effects on mating system and mating behaviour. We investigated the effect of altered ecological conditions, following colonization of a novel habitat, on precopulatory mate guarding in a freshwater isopod (Asellus aquaticus). This isopod occurs in two different ecotypes, which coexist within several different lakes in Sweden but which utilize different habitats. These ecotypes have rapidly (ca. 40 generations) diverged in parallel among lakes in several phenotypic characters, presumably as a response to different predatory pressures. Here, we demonstrate that also mate guarding characteristics have diverged in parallel between the ecotypes in different lakes. This is one of the few studies reporting parallel evolution of mating behaviour. Furthermore, our results also indicate a potential sexual conflict, as the length of mate guarding appears to lower components of female fitness. We discuss how novel environments might have strong and rapid effects on mate guarding dynamics and mating behaviour.

The dynamics of sexually antagonistic coevolution and the complex influences of mating system and genetic correlation.

Sexual conflict has been proposed to be a mediator of speciation but recent theoretical work, as well as empirical studies, suggests that sexual conflict may also be able to prevent speciation and to preserve genetic polymorphism within a species. Here, we develop a population genetic model and study the effects of sexual conflict in a polymorphic population. The morphs mate assortatively based on different sexually antagonistic traits and females are assumed to suffer a cost when the proportion of matching males is high. We consider the model in two different mating systems; promiscuity and polygyny. Our results show that genetic polymorphism may be maintained through negative frequency dependent selection established by assortative mating and female conflict costs. However, the outcome significantly differs between mating systems. Furthermore, we show that indirect selection may have profound effects on the evolutionary dynamics of a sexual conflict.

The interplay between local ecology, divergent selection and genetic drift in population divergence of a sexually antagonistic female trait

Genetically polymorphic species offer the possibility to study maintenance of genetic variation and the potential role for genetic drift in population divergence. Indirect inference of the selection regimes operating on polymorphic traits can be achieved by comparing population divergence in neutral genetic markers with population divergence in trait frequencies. Such an approach could further be combined with ecological data to better understand agents of selection. Here, we infer the selective regimes acting on a polymorphic mating trait in an insect group; the dorsal structures (either rough or smooth) of female diving beetles. Our recent work suggests that the rough structures have a sexually antagonistic function in reducing male mating attempts. For two species (Dytiscus lapponicus and Graphoderus zonatus), we could not reject genetic drift as an explanation for population divergence in morph frequencies, whereas for the third (Hygrotus impressopunctatus) we found that divergent selection pulls morph frequencies apart across populations. Furthermore, population morph frequencies in H. impressopunctatus were significantly related to local bioclimatic factors, providing an additional line of evidence for local adaptation in this species. These data, therefore, suggest that local ecological factors and sexual conflict interact over larger spatial scales to shape population divergence in the polymorphism.

Antagonistic Coevolution Under Sexual Conflict

The theory of sexual conflict predicts that sexual coevolution will be very dynamic, with in principle perpetual evolutionary arms races and chases. These arms races are expected to stop once the costs of conflict adaptations become too high. We argue that this prediction is contingent on specific assumptions about the sexual interaction and the adaptations involved in the arms race. More generally, evolutionary arms races stop when the fitness benefit of further escalations is outweighed by the fitness costs. For this it is not necessary that the absolute costs of conflict must be high at the stable state, or that the population fitness must be decreased at equilibrium. We expect the outcome of sexual antagonistic coevolution to be determined by the possibility to reach compromises and by the relative ability of each sex to control the outcome of the interaction. We exemplify with a theoretical conflict model, which leads to population extinction when conflict is settled by armaments with expression-level determined costs. The model predicts a compromise with small conflict costs for the population, if costs are in addition determined by the extent of conflict between the sexes, which may be the case when the cost depends on behavioural antagonism.