Sebastian Wacker

Do operational sex ratio and density affect mating behaviour? An experiment on the two-spotted goby

Males generally compete for females through courtship and aggression (conventional sex roles). However, sex roles are reversed in some species and can even vary between populations or over time within a single species. The operational sex ratio (OSR), the sex ratio of ready-to-mate individuals, is a central factor proposed to explain the strength and direction of mating competition. Density can both act as a cue for OSR and have its own effects on competition. In the two-spotted goby, Gobiusculus flavescens, a seasonal switch in sex roles coincides with a change in OSR from male to female biased and a decrease in male density. This dynamic system provides an ideal opportunity to test the effects of OSR and density on competitive behaviour experimentally. In an aquarium experiment, we created two different sex ratios at two different densities and observed courtship and agonistic behaviour in both sexes. We changed sex ratio to equality after 4 days of treatment, to test for a lag in the behavioural response. Contrary to our predictions, males courted more after prolonged exposure to a female-biased sex ratio, although we also found a tendency for a positive effect of male density on male courtship frequency. We did not find any other effects of treatment on either male or female behaviour. Furthermore, we did not find evidence for a lag in the response to a change in density or sex ratio. We conclude that OSR and density did not affect individual frequencies of behaviour in the expected direction.

Operational sex ratio but not density affects sexual selection in a fish

The operational sex ratio (OSR) and density are considered important factors affecting the strength of sexual selection. Although there is increasing evidence that OSR and density affect the potential for sexual selection, few studies have addressed whether this is realized in phenotypic selection and how the two factors interact. We manipulated OSR (three levels) and male density (two levels) in 36 experimental breeding populations of Gobiusculus flavescens—a fish with paternal care. We measured mating competition behavior, the opportunity for selection (I), and selection on four morphological traits in males. We found sexual selection on two male traits, with the strongest selection being 20% of I. As predicted from OSR theory, increasing female scarcity caused males to become more competitive, concomitant with an increase in I and selection on morphological traits. Model simulations of I based on random mating (Imin) and maximum mate monopolization (Imax) demonstrated that the potential for sexual selection was close to its theoretical maximum across the range of OSRs. However, male density and its interaction with the OSR did not affect sexual selection. We argue that a multifaceted approach, combining mating behavior and selection analyses, can help us to understand how ecological factors affect sexual selection.

OPERATIONAL SEX RATIO BUT NOT DENSITY AFFECTS SEXUAL SELECTION IN A FISH: EFFECTS OF OSR AND DENSITY ON SEXUAL SELECTION

The operational sex ratio (OSR) and density are considered important factors affecting the strength of sexual selection. Although there is increasing evidence that OSR and density affect the potential for sexual selection, few studies have addressed whether this is realized in phenotypic selection and how the two factors interact. We manipulated OSR (three levels) and male density (two levels) in 36 experimental breeding populations of Gobiusculus flavescens—a fish with paternal care. We measured mating competition behavior, the opportunity for selection (I), and selection on four morphological traits in males. We found sexual selection on two male traits, with the strongest selection being 20% of I. As predicted from OSR theory, increasing female scarcity caused males to become more competitive, concomitant with an increase in I and selection on morphological traits. Model simulations of I based on random mating (Imin) and maximum mate monopolization (Imax) demonstrated that the potential for sexual selection was close to its theoretical maximum across the range of OSRs. However, male density and its interaction with the OSR did not affect sexual selection. We argue that a multifaceted approach, combining mating behavior and selection analyses, can help us to understand how ecological factors affect sexual selection.

Within‐season variation in sexual selection in a fish with dynamic sex roles

The strength of sexual selection may vary between species, among populations and within populations over time. While there is growing evidence that sexual selection may vary between years, less is known about variation in sexual selection within a season. Here, we investigate within‐season variation in sexual selection in male two‐spotted gobies (Gobiusculus flavescens). This marine fish experiences a seasonal change in the operational sex ratio from male‐ to female‐biased, resulting in a dramatic decrease in male mating competition over the breeding season. We therefore expected stronger sexual selection on males early in the season. We sampled nests and nest‐holding males early and late in the breeding season and used microsatellite markers to determine male mating and reproductive success. We first analysed sexual selection associated with the acquisition of nests by comparing nest‐holding males to population samples. Among nest‐holders, we calculated the potential strength of sexual selection and selection on phenotypic traits. We found remarkable within‐season variation in sexual selection. Selection on male body size related to nest acquisition changed from positive to negative over the season. The opportunity for sexual selection among nest‐holders was significantly greater early in the season rather than late in the season, partly due to more unmated males. Overall, our study documents a within‐season change in sexual selection that corresponds with a predictable change in the operational sex ratio. We suggest that many species may experience within‐season changes in sexual selection and that such dynamics are important for understanding how sexual selection operates in the wild.

Large males fight and court more across a range of social environments: an experiment on the two spotted goby Gobiusculus flavescens

The present study explored how male size relates to mating competition across a natural range of male and female densities in the two-spotted goby Gobiusculus flavescens. Across this range of social environments, large males were more than twice as likely as small ones to chase other males, to become nest-holders, and to court females, but large males were not significantly more likely to engage in agonistic fin displays. Overall, the study showed that large males court and fight more than small ones across a wide, yet natural, span of social environments. Having a large body size appears to confer competitive advantage for males in any social environment of the study species. Further studies are needed to disentangle whether the benefit of large size is mainly in competition over resources, over matings as such, or both.

Context Consistency and Seasonal Variation in Boldness of Male Two-Spotted Gobies

In order to attribute the behaviour of an animal to its personality it is important to study whether certain behavioural traits show up consistently across a variety of contexts. The aim of this study was to investigate whether breeding state males of the two-spotted goby, Gobiusculus flavescens, showed consistent degree of boldness when tested in four different behaviour assays. We also wanted to investigate whether boldness varied over the breeding season in accordance with changes in male-male competition for matings. We used two standard assays (the emergence test and the open field test), and two simple assays related to threat response. Repeated runs of each of the tests were highly correlated, and we found significant correlations between all four assays. Thus, we have documented both a within and a between-context consistency in risk-taking behaviour. Furthermore, we found that goby males studied during the middle of the breeding season were bolder than males studied at the end of the season. Since male two-spotted gobies face strongly decreasing male-male competition as the season progresses, the benefit of being bold for the mating success of the males may differ over the time of the breeding season. The difference in behaviour found over the season thus corresponds well with the sexual dynamics of this model species.

Mate competition and resource competition are inter-related in sexual selection

Sexual selection can be affected by the competition for limited breeding resources and/or the competition for limited mates. Although there is ample evidence for each type of competition by itself, little is known about their relative importance and interaction. To address these questions, we established 48 experimental breeding populations of the two‐spotted goby (Gobiusculus flavescens), a substrate‐breeding fish with paternal care. In three experimental treatments, males were limited in the access to either nest sites or mates or were provided with both nests and mates in excess. We quantified male competition behaviour (agonistic and courtship), the opportunity for selection and selection on male body size. Limited access to nests and mates produced similar opportunities for selection, but only limited access to mates increased male competitive behaviours and caused positive selection on male body size. Selection on body size in the mate‐limited treatment was due both to larger males being more likely to take up nests and to larger males being more likely to mate once they had a nest. These findings demonstrate that resource and mate limitation can differ in their effects on sexual selection. The results also reveal that resource and mating competition can be highly inter‐related and not always separated in time, implying that methods to disentangle the two processes must be chosen with care. Future research should consider experimental and analytical approaches similar to those of the present study in attempts to elucidate the interaction of resource and mating competition in animals.

Nest distribution affects behaviour and mating success in a marine fish

The distribution of breeding resources, such as nest sites, can have a pronounced impact on a population by affecting the proportion of individuals that succeed to breed and hence, the variation in reproductive success. Aggregation of important resources can lead to resource monopolisation by a limited number of individuals and thus affect the intensity of sexual selection. In this study, we tested, by contrasting two experimental treatments (dispersed vs. aggregated), how nest distribution affects: (1) mating behaviour, (2) male nest occupation and mating success, and (3) reproductive success and the opportunity for selection. We used the two-spotted goby (Gobiusculus flavescens), a small marine fish with a resource-based mating system, as our model species. When nests were aggregated, a larger proportion of the males behaved aggressively, fewer males succeeded in occupying a nest, fewer males became mated, and those males that mated received fewer eggs from spawning females. These effects resulted in a higher variance in reproductive success and hence, a higher opportunity for selection (Irs), in the aggregated treatment. We suggest that the results are a direct consequence of males defending a territory around their nest, preventing competitively inferior males from breeding. However, we found no significant selection differentials for body length or condition of males in either treatment. Our results support the hypothesis that aggregation of essential resources like nests promotes resource monopolisation. In species facing highly clumped nesting resources in the wild, monopolisation may negatively impact population productivity but could lead to strong selection on traits that promote male competitive ability.

Did natural selection make the Dutch taller? A cautionary note on the importance of quantification in understanding evolution.

One of the main achievements of the modern synthesis is a rigorous mathematical theory for evolution by natural selection. Combining this theory with statistical models makes it possible to estimate the relevant parameters so as to quantify selection and evolution in nature. Although quantification is a sign of a mature science, statistical models are unfortunately often interpreted independently of the motivating mathematical theory. Without a link to theory, numerical results do not represent proper quantifications, because they lack the connections that designate their biological meaning. Here, we want to raise awareness and exemplify this problem by examining a recent study on natural selection in a contemporary human population. Stulp et al. (2015) concluded that natural selection may partly explain the increasing stature of the Dutch population. This conclusion was based on a qualitative assessment of the presence of selection on height. Here, we provide a quantitative interpretation of these results using standard evolutionary theory to show that natural selection has had a minuscule effect.

Social structure affects mating competition in a damselfish

The strength of mating competition and sexual selection varies over space and time in many animals. Such variation is typically driven by ecological and demographic factors, including adult sex ratio and consequent availability of mates. The spatial scale at which demographic factors affect mating competition and sexual selection may vary but is not often investigated. Here, we analyse variation in size and sex ratio of social groups, and how group structure affects mating competition, in the site-attached damselfish Chrysiptera cyanea. Site-attached reef fishes are known to show extensive intraspecific variation in social structure. Previous work has focused on species for which the size and dynamics of social groups are constrained by habitat, whereas species with group structure unconstrained by habitat have received little attention. Chrysiptera cyanea is such a species, with individuals occurring in spatial clusters that varied widely in size and sex ratio. Typically, only one male defended a nest in multi-male groups. Nest-holding males were frequently visited by mate-searching females, with more visits in groups with more females, suggesting that courtship and mating mostly occur within groups and that male mating success depends on the number of females in the group. Male–male aggression was frequent in multi-male groups but absent in single-male groups. These findings demonstrate that groups are distinct social units. In consequence, the dynamics of mating and reproduction are mainly a result of group structure, largely unaffected short term by overall population demography which would be important in open social systems. Future studies of the C. cyanea model system should analyse longer-term dynamics, including how groups are formed, how they vary in relation to density and time of season and how social structure affects sexual selection.