Choice In Sticklebacks Research Articles

Mate choice in sticklebacks reveals that immunogenes can drive ecological speciation.

Adaptation to ecologically contrasting niches can lead to the formation of new species. Theoretically, this process of ecological speciation can be driven by pleiotropic "magic traits" that genetically link natural and sexual selection. To qualify as a true magic trait, the pleiotropic function of a gene must be reflected in biologically relevant mechanisms underlying both local adaptation and mate choice. The immune genes of the major histocompatibility complex (MHC) contribute to parasite resistance and also play a major role in sexual selection. Hence, the MHC may encode a candidate magic trait. Using diverging 3-spined stickleback populations from a connected lake-river habitat, we show with mate choice experiments in a flow channel that polymorphic MHC genes probably underlie assortative mating with respect to particular habitat-adapted ecotypes, potentially resulting in reproductive isolation. By manipulating olfactory cues in controlled experiments, we show that female sticklebacks employ MHC-dependent male olfactory signals to select mates with which they can achieve a habitat-specific MHC gene structure that optimally protects their offspring against local parasites. By using MHC-based olfactory signals, females thus select individuals of their own population as mates. Our results demonstrate how mate choice and parasite resistance may be functionally linked. These findings suggest that MHC genes are pleiotropic and encode a true magic trait of biologically significant effect.

ENVIRONMENT SPECIFIC PLEIOTROPY FACILITATES DIVERGENCE AT THEECTODYSPLASINLOCUS IN THREESPINE STICKLEBACK

Adaptive radiation occurs when divergent natural selection in different environments leads to phenotypic differentiation. The pleiotropic effects of underlying genes can either promote or constrain this diversification. Identifying the pleiotropic effects of genes responsible for divergent traits, and testing how the environment influences these effects, can therefore help to provide an understanding of how ecology drives evolutionary change between populations. Positive selection on low-armor alleles at the Ectodysplasin (Eda) locus in threespine stickleback has led to the repeated evolution of reduced armor in populations following freshwater colonization by fully armored marine sticklebacks. Here, we demonstrate that Eda has environmentally determined pleiotropic effects on armor and growth. When raised in freshwater, reduced armor sticklebacks carrying "low" alleles at Eda had increased growth rate relative to fully armored sticklebacks carrying "complete" alleles. In saltwater treatments this growth advantage was present during juvenile growth but lost during adult growth, suggesting that in this environment stickleback are able to develop full armor plates without sacrificing overall growth rate. The environment specific pleiotropic effects of Eda demonstrate that ecological factors can mediate the influence of genetic architecture in driving phenotypic evolution. Furthermore, because size is important for mate choice in stickleback, the growth rate differences influenced by Eda may have effects on reproductive isolation between marine and freshwater populations.

Color signaling in conspicuous red sticklebacks: do ultraviolet signals surpass others?

BackgroundThe use of ultraviolet (UV) signals for communication tasks is widespread in vertebrates. For instance, there is a UV component to mate choice in several species. Nevertheless, it remains unclear how the signal value of the UV wave band compares to that of other regions of the animal's visible spectrum. We investigated the relative importance of UV signals compared with signals of longer wavelengths in the threespine stickleback (Gasterosteus aculeatus), a species using UV wavelengths in female and male mate choice as well as in shoaling behavior. In a choice experiment, female sticklebacks were simultaneously presented with four male visual appearances manipulated by optical filters. Each male lacked one wavelength range of the stickleback's visible spectrum corresponding to the spectral sensitivities of the four cone types. The resulting male appearances thus had no UV (UV-), no short-wave (SW-), no medium-wave (MW-) or no long-wave (LW-) body reflectance.ResultsMales without UV wavelengths and long wavelengths ("red") were least preferred. In contrast, the removal of medium and most notably short wavelengths left male attractiveness to females rather unaffected. Using color metrics, the effects of the four optical filters on stickleback perception of three male body regions were illustrated as quantal catches calculated for the four single cones.ConclusionThe removal of UV light (UV-) considerably reduced visual attractiveness of courting males to female three-spined sticklebacks particularly in comparison to the removal of short-wave light (SW-). We thus report first experimental evidence that the UV wave band clearly outranks at least one other part of an animal's visible spectrum (SW-) in the context of communication. In addition, females were also less attracted to males presented without long wavelengths (LW-) which supports the traditionally considered strong influence of the red color component on stickleback mate choice. Overall, the removal of medium wavelengths (MW-) and especially short (SW-) left male attractiveness for females rather unaffected. Our work suggests that, in addition to long wavelengths ("red"), the UV wave band contains important information for visual mate choice in sticklebacks. Hence, the previously suggested exclusive role of the characteristic red nuptial coloration in visual interactions between reproductively active stickleback conspecifics may be overestimated with UV wavelengths playing a more important role than previously suggested.

The origin of species

The origin of species

The function of mate choice in sticklebacks: optimizing Mhc genetics

Sexual reproduction is an evolutionary 'puzzle'. A sexual female 'throws away' half of her genes (during meiosis), and 'fills up' what she lost with genes from a male. Thus, sexual reproduction can only be successful if the offspring with the new mixture of genes should be more than twice as fit as if she had just made a copy of herself. A challenging hypothesis assumes that infectious diseases select for females that reshuffle the immune genes for their offspring in each generation. The required increase in quality could be achieved by females selectively 'smelling out' suitable immune-genes (i.e. Mhc alleles) in potential partners, which, in combination with the female's genes, offer optimal resistance against quickly changing infectious diseases. It was found that most three spined sticklebacks Gasterosteus aculeatus in natural populations around Plon, Germany, had intermediate instead of maximal numbers of different Mhc class IIB alleles. Furthermore, fish with an intermediate number of different Mhc alleles were infected with the lowest number of both parasite species and parasites per species. This suggests that Mhc heterozygosity was optimized instead of maximized. Can this immunogenetic optimum be achieved through female choice? In a flow channel design that allowed the detection of olfactory signals only, it was found that female three-spined sticklebacks that were ready to spawn preferred males as mates that in combination with their Mhc alleles would allow the production of offspring with the optimal number of Mhc alleles. Thus, mate choice in three-spined sticklebacks could have the two-fold advantage over asexual reproduction that is required to maintain sexual reproduction. The interaction of olfactory with visual signals in three-spined stickleback mate choice is discussed. The three-spined stickleback is a suitable model organism for studying the evolution of sexual reproduction in relation to optimizing offspring immune genetics although other fishes may be as suitable.

Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections.

'Good genes' models of sexual selection suggest that elaborate male sexual ornaments have evolved as reliable signals of male quality because only males of high genetic viability are able to develop and maintain them. Females benefit from choosing such individuals if quality is heritable. A key prediction is that the offspring of males with elaborate mating displays will perform better than those of less elaborate males, but it has proved difficult to demonstrate such an effect independently of the effects of differences in parental investment. We tested for 'good genes' linked to male ornamentation in the three-spined stickleback Gasterosteus aculeatus using in vitro fertilization to generate maternal half-siblings, which were raised without parental care. Maternal half-siblings sired by brightly coloured males grew less quickly than half-siblings sired by dull males but were more resistant to a controlled disease challenge. Among the offspring that became infected, those with brighter fathers had higher white blood cell counts. This suggests that highly ornamented males confer disease resistance on their offspring. The association with reduced growth suggests a mechanism for the maintenance of heritable variation in both disease resistance and male sexual coloration.

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 issue1,2,3. Theoretical models attempt to explain the high genetic variance of sexual traits, among others, by the evolution of condition dependence1,4, 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 males5, and find that the choice of mate correlates well with female physical condition.

Male–male competition facilitates female choice in sticklebacks

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.

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.

Female sand gobies prefer good fathers over dominant males

Female preference for males successful in male–male competition is generally assumed to result in mating with high quality males. Here I report results from an experiment disentangling the effects of intra– and intersexual selection in the sand goby, Pomatoschistus minutus , a marine fish that exhibits paternal care. I show that large males are successful in male–male competition, but contrary to what one would expect, dominants are not preferred by females and are not better at taking care of the eggs. Female preference, however, correlated with the subsequent hatching success of the eggs. Thus, female choice selects for good parenting. Hence, direct benefits in the form of superior paternal care can explain female choice in this species, supporting a good parent process of sexual selection. However, choosing on the outcome of male–male competition does not enable females to mate with the ‘best’ males.