Theo C. M. Bakker

Costs Influence Sequential Mate Choice in Sticklebacks, Gasterosteus aculeatus

In nature females can usually choose among males only sequentially. Recent models of sequential choice predict that, with increasing costs of sampling, selectivity for preferred males should decline. In our tests female sticklebacks were highly selective in their sequential choice between dull and bright males when costs were low. With increasing time and energy costs of moving between males, they reduced their selectivity. In particular, when the females had to swim against a current, dull males when met became highly acceptable. The females’ response to increased costs of sampling shows that they make the kind of economic decisions predicted by models of sequential choice. The strength of sexual selection by female choice therefore depends on the spatial structure of the population.

The genetic basis of female mate preferences

We review the evidence for genetic variation in female and male mate preferences. Genetic differences between species and partially isolated races show that preferences can evolve and were genetically variable in the past. Within populations there is good evidence of genetic variation, both of discrete genetic effects (8 cases) and quantitative genetic effects (17 cases), from a diverse range of taxa. We also review evidence for the presence of genetic covariance between mate preferences and sexual traits in the other sex. The 11 studies go a long way to validating the theoretical prediction of positive genetic covariance. The few negative results are best explained by a lack of appropriate experimental design. One unresolved question is whether genetic covariance is due to linkage disequilibrium between unlinked genes or physical linkage. Some evidence points to linkage disequilibrium but this is not yet conclusive.

Sequential female choice and the previous male effect in sticklebacks

SummaryFemale choice, identified as a major force in sexual selection theory, has recently been demonstrated in a number of species. These tests concentrated on simultaneous choice situations although females have to compare males sequentially in most territorial species, which is the more demanding task. Here it is shown that female three-spined sticklebacks, Gasterosteus aculeatus L., rate sequentially presented males according to their brightness. With increasing costs of sampling the females become less choosy. Furthermore, a males attractiveness has a significant effect on the females rating of the next male; a given male is rated higher when preceded by a duller male than by a brighter one and vice versa. Female sticklebacks use a stochastic decision rule in sequential mate choice that is attuned to the attractiveness of the present and previously encountered male. This demonstration of a “previous male effect” not only indicates an efficient mechanism for finding the best of a number of males but also extends the applicability of sexual selection theory.

Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation.

The acanthocephalan parasite Pomphorhynchus laevis is transmitted by crustaceans such as Gammarus pulex to its paratenic or final hosts, fish. The conspicuous orange-yellow parasite is visible through the transparent cuticle of G. pulex. Infected gammarids are significantly less photophobic than uninfected ones. When hungry three-spined sticklebacks (Gasterosteus aculeatus), one of the hosts of this parasite, were offered equal numbers of uninfected and infected prey, G. pulex infected with P. laevis were eaten significantly more often. We tested experimentally whether parasite color and parasite-induced changes in host behavior affected the predation rate of G. pulex. Color effects were tested with uninfected G. pulex by painting an orange spot on their cuticle that simulated infection. Behavioral effects were tested with infected G. pulex by covering the place through which the orange parasite was visible with inconspicuous brown paint. We showed for the first time that both parasite color and changed intermediate host behavior promote the transmission of P. laevis to its next host. The evolution of orange parasite color, and why sticklebacks do not avoid infected prey, are discussed.

Aggressiveness in sticklebacks (Gasterosteus aculeatus L.): a behaviour-genetic study

This behaviour-genetic study concentrates on intra-specific aggressiveness in the three-spined stickleback (Gasterosteus aculeatus L., forma leiura). Aggressiveness was studied under standardized conditions in five different test situations, referred to as juvenile aggressiveness, female aggressiveness, territorial aggressiveness, courtship aggressiveness, or dominance ability. The aim of the study is two-fold: 1. To assess the extent to which variation of aggressiveness in each of the different test situations is attributable to genetic causes. 2. To assess the extent to which variation in these various manifestations of aggressiveness is influenced by common genetic factors. The paper starts with an analysis of the variation of aggressiveness in the base population, composed of individually isolated progeny of wild-caught parents (chapter 2). In each of the different test situations aggressiveness is highly variable across individuals. Repeated measurements with the same individuals as well as similarity of the levels of aggression between full sibs shows that phenotypic variation is to a considerable extent attributable to genotypic variation in each of the investigated situations. The genetic influence on variation of aggressiveness is further analysed with the aid of selection experiments (chapter 3). Bidirectional selection is exerted upon juvenile aggressiveness in juveniles of both sexes (juvenile aggression lines), upon territorial aggressiveness in males and female aggressiveness in adult females (territorial aggression lines), and lastly, upon dominance ability in males (dominance lines). Besides these six selection lines an unselected control line was maintained. Selection is highly successful in downward direction in each of the different contexts. However, enhancement of the level of aggression is less successful in most lines, with the exception of female aggressiveness. Possible causes for these asymmetries of responses are discussed in detail. It is argued that the lack of response in males to selection for territorial aggressiveness and dominance ability in upward directions is probably due to an upper selection limit for territorial aggressiveness and dominance ability, that is already present in the base population. The combined two-way responses yield heritability-estimates of at least 0.30 for aggressiveness in the different test situations. In the single selection lines the realized heritabilities range from 0 to at least 0.60. Across individuals of the base population the levels of aggression in the different test situations are correlated with each other to various degrees. In females there is a distinctly positive phenotypic correlation between juvenile and female aggressiveness, but in males correlations between juvenile, territorial and courtship aggressiveness are weaker. Dominance ability is uncorrelated with aggressiveness in the other test situations. Since fish of the various selection lines are not only scored for their aggressiveness in the particular situation in which they are selected, but also for their aggressiveness in the other test situations, these phenotypic correlations can be translated into genetic correlations (chapter 4). The genetic correlations between the levels of aggression in the different test situations are comparable to the corresponding phenotypic correlations. The genetic basis of juvenile aggressiveness is most likely identical for both juvenile males and juvenile females. In adult females variation of aggressiveness remains most likely governed by the same genetic factors. The genetic factors that contribute to variation of territorial aggressiveness are only partly identical to those that contribute to variation of juvenile aggressiveness. Changes of courtship aggressiveness parallel those of territorial aggressiveness in the various selection lines, suggesting that common genetic influences underlie variation in both manifestations of intra-specific aggressiveness in reproductive males. Lastly, variation of dominance ability is probably governed by genetic factors different from those governing variation of juvenile or territorial aggressiveness. Indirect determination of the level of androgens in reproductive males of the various selection lines, by means of kidney-size measurements, reveals that selection for territorial aggressiveness most likely acts on the level of androgens. In view of changes accompanying selection for juvenile aggressiveness (viz. a difference between high and low line fish in age at sexual maturity, in age at onset of juvenile aggression, and in incidence of ripeness) selection for juvenile aggressiveness likely acts on the level of gonadotropic hormones. Finally, selection for dominance ability acts on factors (probably androgen-independent) that influence the brightness of colouration. Throughout this paper the influence of a number of variables on aggressiveness in the various test situations, such as age, degree of ripeness, location of the nest, age of sexual maturity, experience, length, isolation and responsiveness, are analysed. Furthermore, attention is paid to threatening displays, to a peculiar behaviour called snapping at air-bubbles, to aggressiveness of juveniles in groups of fixed size, and to measures of aggressiveness other than the criterion applied during selection in a particular situation. Finally, the literature is reviewed with respect to selection studies on aggressiveness and to selective forces acting on aggressiveness in the three-spined stickleback.

Mutual mate choice in sticklebacks: attractive males choose big females, which lay big eggs

Brighter red three-spined stickleback, Gasterosteus aculeatus, males have been shown to be preferred by females in the laboratory but in the field, these males did not receive more eggs. Instead, they had heavier eggs in their brood. We investigated the hypothesis that sexual selection for red coloration in male sticklebacks acts through mate choice by preferred males, who can afford to be choosy, for high-quality females which lay heavier eggs. We assume here that heavier eggs provide a direct fitness advantage. In simultaneous choice tests males were presented with two females differing in size. The number of zigzags directed to and the time spent orienting to each female were measured. After the test the females laid eggs, which we counted and weighed. Bigger (i.e. longer and heavier) females laid significantly more and heavier eggs than smaller females. For all 23 males pooled together, the preferred female was the bigger of the two in 17 cases, laid more eggs in 18 cases, but laid heavier eggs in only 13 cases. When bright and dull males were analysed separately, we found that bright but not dull males spent more time oriented to the bigger female, and to the female that laid more eggs. Females preferred by bright males tended to lay heavier eggs than nonpreferred females, although this result was not quite significant. We conclude that in nature this preference for bigger females results in brighter males receiving on average heavier eggs. Assuming higher survival of bigger offspring, we propose that this can explain how brightness can be sexually selected in spite of brighter males not receiving more eggs. Copyright 1998 The Association for the Study of Animal Behaviour.

Condition-related mate choice in sticklebacks

Exactly how the high genetic variance of traits involved in sexual selection through female mate choice is maintained is a much debated issue. Theoretical models attempt to explain the high genetic variance of sexual traits, among others, by the evolution of condition dependence, in which expression of the trait depends on physical condition. If it is costly to be choosy, then these models should also apply to female mate preference and predict that female condition affects the choice of mate. Here we allow female laboratory-bred three-spined sticklebacks, Gasterosteus aculeatus, to choose between computer animations of courting males, and find that the choice of mate correlates well with female physical condition.

Active Inbreeding in a Cichlid Fish and Its Adaptive Significance

Levels of inbreeding are highly variable in natural populations. Inbreeding can be due to random factors (like population size), limited dispersal, or active mate choice for relatives. Because of inbreeding depression, mating with kin is often avoided, although sometimes intermediately related individuals are preferred (optimal outbreeding). However, theory predicts that the advantages of mating with close kin can override the effects of inbreeding depression, but in the animal kingdom, empirical evidence for this is scarce. Here we show that both sexes of Pelvicachromis taeniatus, an African cichlid with biparental brood care, prefer mating with unfamiliar close kin over nonkin, suggesting inclusive fitness advantages for inbreeding individuals. Biparental care requires synchronous behavior among parents. Since parental care is costly, there is a conflict between parents over care, which can reduce offspring fitness. Relatedness is expected to enhance cooperation among individuals. The comparison of the parental behavior of in- and outbreeding pairs showed that related parents were more cooperative and invested more than unrelated parents. Since we found no evidence for inbreeding depression, our results suggest that in P. taeniatus, inbreeding is an advantageous strategy.

THE STUDY OF INTERSEXUAL SELECTION USING QUANTITATIVE GENETICS

In this review, I stress the importance of incorporating Quantitative Genetics (QG) in the study of sexual selection through female mate choice. A short overview of QG principles and methods of estimating genetic variance and covariance is given. The state of knowledge is summarized as to two QG assumptions (genetic variance in female mating preferences and male sexual traits) and one QG prediction (genetic covariance between preferences and preferred traits) of models of sexual selection. A review is given of studies of repeatability of mating preferences because of recent accumulation of data. The general conclusion is that sexual traits and mating preferences show large genetic variation and are genetically correlated. The extensive genetic variation asks for an explanation that goes beyond the ususal explanations of the maintenance of genetic variation in fitness traits. Two models that explain the high genetic variance in sexual traits are treated in detail: modifier selection and condition dependence. There are many unexplored areas of QG research that could stimulate further research in sexual selection like the study of genetic covariance between mating preferences and good genes, of genetic variances and covariances of multiple male traits and multiple females preferences, of genetic variance in condition, and of condition dependence of mating preferences.

UV wavelengths affect female mate choice in three-spined sticklebacks

Recent behavioural studies on fish have emphasized the role of ultraviolet (UV) wavelengths in mate choice. We performed female mate choice experiments, focusing on the UV wavelength range, with the three-spined stickleback, Gasterosteus aculeatus, a species in which the role of visually guided behaviour in the human-visible wavelength range (400–700 nm) has been well studied. Ripe female sticklebacks were given the opportunity to watch courting males behind UV-transmitting (UVþ) and UV-blocking (UV� ) optical filters. We tested the hypothesis that a difference in viewing conditions, manipulated by the two optical filters, would affect male attractiveness, as indicated by the time that the female stayed near the males. Females significantly preferred UVþ males. They also became less selective with time. Control experiments, in which neutral-density optical filters were used, showed that the ability to perceive UV wavelengths is likely to be used for colour discrimination instead of detecting brightness differences.