A receiver bias in the origin of three-spined stickleback mate choice

Receiver-bias models of signal evolution predict that male sexually selected traits evolve through prior selection for other functions. Female three-spined sticklebacks (Gasterosteus aculeatus) in many populations show a mating preference for males with a red throat and jaw. It has been proposed that this preference evolved because the choice of males with red coloration confers direct and indirect benefits to females in accordance with the Fisher-Zahavi model of sexual selection. We present indirect evidence that the preference is an effect of a receiver bias in the perceptual or cognitive system of G. aculeatus for the colour red, which may have arisen in the context of foraging. In laboratory trials, male and female three-spined and nine-spined sticklebacks (Pungitius pungitius) responded most strongly to red objects outside a mating context. This result demonstrates a correlation between a sexually selected trait and an intrinsic attraction to red objects, and supports the sensory-exploitation model for the evolution of red nuptial coloration in three-spined sticklebacks.     

Female mate choice and male red coloration in a natural three-spined stickleback (Gasterosteus aculeatus) population

Under laboratory conditions, female three-spined sticklebacks(Gasterosteus aculeatus L.) show a mating preference for intenselyred-colored males. We verified this female choice in the fieldby observing a freshwater stickleback population in its naturalhabitat. During the egg collection phase, individual courtingmales were localized with the aid of a dummy of a ripe female,caught and photographed under standardized conditions, and released.After males had stopped collecting eggs, we counted the numberof eggs in the nests. The more intense a male's red breedingcoloration, the more eggs he received. Simultaneous female choiceexperiments in the laboratory suggested that ripe females ofthis population preferred redder males. Breeding activitiesof the males in the field were clustered and seem to be synchronizedwithin clusters. At one of the breeding sites, more intensered males were in better physical condition, but this was notthe case at another site. Although several synchronized breedingcycles were observed, the majority of males seem to completeonly one breeding cycle.     

Association patterns and shoal fidelity in the three-spined stickleback

We investigated pairwise association patterns and shoal fidelity in free-ranging, individual three-spine sticklebacks (Gasterosteus aculeatus) by capturing entire shoals of sticklebacks and tagging each shoal member with a unique individual mark before releasing the shoal at the point of capture. We recaptured tagged fishes in the study area on five subsequent days, noting their identity, their location and the individuals with which they were associated. Stable partner associations between fishes were observed which might provide the basis for shoal fidelity via social networks. These results suggest the potential for the kinds of inter-individual association patterns assumed by models of predator inspection and 'tit-for-tat' behaviours in free-ranging fishes.     

Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks

Genes of the major histocompatibility complex (MHC) have been studied for several decades because of their pronounced allelic polymorphism. Structural allelic polymorphism is, however, not the only source of variability subjected to natural selection. Genetic variation may also exist in gene expression patterns. Here, we show that in a natural population of three-spined sticklebacks (Gasterosteus aculeatus) the expression of MHC class IIB genes was positively correlated with parasite load, which indicates increased immune activation of the MHC when infections are frequent. To experimentally study MHC expression, we used laboratory-bred sticklebacks that were exposed to three naturally occurring species of parasite. We found strong differences in MHC class IIB expression patterns among fish families, which were consistent over two generations, thus demonstrating a genetic component. The average number of MHC class IIB sequence variants within families was negatively correlated to the MHC expression level suggesting compensatory up-regulation in fish with a low (i.e. suboptimal) MHC sequence variability. The observed differences among families and the negative correlation with individual sequence diversity imply that MHC expression is evolutionary relevant for the onset and control of the immune response in natural populations.     

MHC,mate choice and heterozygote advantage in a wild social primate

Preferences for mates carrying dissimilar genes at the major histocompatibility complex (MHC) may help animals increase offspring pathogen resistance or avoid inbreeding. Such preferences have been reported across a range of vertebrates, but have rarely been investigated in social species other than humans. We investigated mate choice and MHC dynamics in wild baboons (Papio ursinus). MHC Class II DRB genes and 16 microsatellite loci were genotyped across six groups (199 individuals). Based on the survey of a key segment of the gene‐rich MHC, we found no evidence of mate choice for MHC dissimilarity, diversity or rare MHC genotypes. First, MHC dissimilarity did not differ from random expectation either between parents of the same offspring or between immigrant males and females from the same troop. Second, female reproductive success was not influenced by MHC diversity or genotype frequency. Third, population genetic structure analysis revealed equally high genotypic differentiation among troops, and comparable excess heterozygosity within troops for juveniles, at both Mhc‐DRB and neutral loci. Nevertheless, the age structure of Mhc‐DRB heterozygosity suggested higher longevity for heterozygotes, which should favour preferences for MHC dissimilarity. We propose that high levels of within‐group outbreeding, resulting from group‐living and sex‐biased dispersal, might weaken selection for MHC‐disassortative mate choice.     

Migrations of three-spined stickleback, nine-spined stickleback, and pond smelt in the Chignik catchment, Alaska

Upstream spawning migrations of age-2 three-spined stickleback, nine-spined stickleback, and pond smelt, and subsequent downstream migrations of young-of-the-year and age-1 individuals are documented in Black River of the Chignik catchment, Alaska.     

Polymorphism and signature of selection in the MHC class I genes of the three-spined stickleback Gasterosteus aculeatus

The role and intensity of positive selection maintaining the polymorphism of major histocompatibility complex (MHC) class I genes in the three-spined stickleback Gasterosteus aculeatus was investigated. The highly polymorphic set of MHC class I genes found was organized in a single linkage group. Between 5 and 14 sequence variants per individual were identified by single-stranded conformation polymorphism (SSCP) analysis. Segregation analysis studied in 10 three-spined stickleback families followed the expected pattern of Mendelian inheritance. The gamete fusion in three-spined stickleback thus seems to be random with respect to the MHC class I genes. The DNA sequence analyses showed that the expressed MHC class I loci are under strong selection pressure, possibly mediated by parasites. Codons that were revealed to be under positive selection are potentially important in antigen binding. MHC class I sequences did not form significant supported clusters within a phylogenetic tree. Analogous to MHC class II genes, it was not possible to assign the class I sequences to a specific locus, suggesting that the class I genes may have been generated by recent gene duplication.     

Nest site choice by the three-spined stickleback, Gasterosteus aculeatus (form leiurus), in spring-fed waters

The nest site characteristics of the freshwater three-spined stickleback, Gasterosteus aculeatus (form leiurus ), were quantitatively investigated in springs and the main stream of the Yamayoke and the Tsuya River system, central Japan. Most nests (93·4%) were on a muddy or sandy substratum, at depths of 10–40 cm (84·3%), in water velocities less than 15 cm s⁻¹ (76·2%) and in the temperature range of 14 to 16° C (82·7%), Spring-fed localities provided more of these conditions than the main stream channel and hence contained more potential nesting areas. Thus, they were utilized by male sticklebacks both temporally (prolonged breeding season) and spatially (more nest sites).     

Individual MHC class I and MHC class IIB diversities are associated with male and female reproductive traits in the three-spined stickleback

Genes of the major histocompatibility complex (MHC) are indispensable for pathogen defence in vertebrates. With wild-caught three-spined sticklebacks (Gasterosteus aculeatus) we conducted the first study to relate individual reproductive parameters to both MHC class I and II diversities. An optimal MHC class IIB diversity was found for male nest quality. However, male breeding colouration was most intense at a maximal MHC class I diversity. One MHC class I allele was associated with male redness. Similarly, one MHC class IIB allele was associated with continuous rather than early female reproduction, possibly extending the reproductive period. Both alleles occurred more frequently with increasing individual allele diversity. We suggest that if an allele is currently not part of the optimum, it had not been propagated by choosy females. The parasite against which this allele provides resistance is therefore unlikely to have been predominant the previous year - a step to negative frequency-dependent selection.     

MHC-based mate choice combines good genes and maintenance of MHC polymorphism

Polymorphic genes of the major histocompatibility complex (MHC) are regarded as essential genes for individual fitness under conditions of natural and sexual selection. To test this hypothesis, we investigated the ultimate individual fitness trait — that of reproductive success. We used three-spined sticklebacks ( Gasterosteus aculeatus ) in seminatural enclosures, located in natural breeding areas where the experimental fish had been caught. During their reproductive period, fish were exposed continuously to their natural sympatric parasites. By genotyping almost 4000 eggs with nine microsatellites, we determined parenthood and inferred female mating decision. We found that with reference to their own MHC profile, female sticklebacks preferred to mate with males sharing an intermediate MHC diversity. In addition, males with a specific MHC haplotype were bigger and better at fighting a common parasite ( Gyrodactylus sp.). This translated directly into Darwinian fitness since fish harbouring this specific MHC haplotype were more likely to be chosen and had a higher reproductive output. We conclude that females also based their mating decision on a specific MHC haplotype conferring resistance against a common parasite. This identifies and supports 'good genes'. We argue that such an interaction between host and parasite driving assortative mating is not only a prerequisite for negative frequency-dependent selection — a potential mechanism to explain the maintenance of MHC polymorphism, but also potentially speciation.     

Comparative study of the olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius)

Summary The olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius) has been studied with a conventional histochemical and a novel immunological staining technique. In both species, the sensory epithelium is arranged in folds separated by non-sensory epithelial tissue. In the nine-spined stickleback, intrinsic folds consisting of non-sensory cells are found in the apical part of the sensory epithelium where they divide the surface of the sensory epithelium into small islets. These non-sensory cells are non-ciliated, flattened and piled on top of each other; they contain numerous electron-translucent vesicles. The intrinsic folds are absent from the sensory epithelium of the three-spined stickleback. In both species, axons of receptor cells form a layer of fibers in the sensory epithelium immediately above the basal cells. In the three-spined stickleback, thick branches of the olfactory nerve are frequently found in this layer. These branches are only occasionally observed in the sensory epithelium of the nine-spined stickleback. Thus, the three-spined stickleback and the nine-spined stickleback show considerable differences in the organization of the sensory regions of the olfactory epithelium.     

Evaluation of ovum fixation and storage in three-spined stickleback

Ripe eggs removed from three-spined sticklebacks stored in 50% isopropyl alcohol showed significantly Sower mean masses than those stored in 10% formalin. These results are considered in relationship to preservation techniques for stickleback.     

Annual variation in energy reserves in male three-spined stickleback, Gasterosteus aculeatm L. (Pisces, Gasterosteidae)

Wet and dry weights of tissue were measured and concentrations of glycogen, lipid and protein were estimated for the liver, gonad and carcass of male sticklebacks from an annual population collected each month over one complete year. In young-of-the-year there is one period of rapid weight gain, in all three body regions (liver, carcass and gonads) but particularly of the carcass, in the autumn and a second in spring and early summer. This is accompanied by an increase in the water content of all three body regions. The gonadosomatic index also increases sharply in spring and early summer. Young sticklebacks accumulate lipid and glycogen slowly during the autumn and winter of their first year of life and more rapidly from late winter to early summer. Thus, the period of most rapid accumulation of these reserves coincides with the time when body weight and gonad maturation are also increasing sharply. Lipid and glycogen levels fall during the reproductive season in those males that breed, so that by July they are reduced to 43% and 37% (respectively) of their peak values in May. Levels of protein increase throughout the year as the fish grow, but in breeding males by July the concentration of protein in the carcass falls to 70% of pre-breeding levels. Breeding males therefore reach the end of the reproductive season with their total energy reserves severely reduced, and consequently they suffer a very high mortality. In contrast, adult males that fail to reproduce survive beyond the breeding season. They continue to gain weight and to accumulate lipid and glycogen from August to September, but these energy reserves fall (to levels comparable to those of post-breeding fish) in December, when these fish probably die. These results demonstrate that in male sticklebacks, growth and gonad maturation can be sustained in parallel with the accumulation of energy reserves, which are subsequently extensively depleted as a result of reproductive activities.     

Parasite infection,host resistance and mate choice: battle of the genders in a simultaneous hermaphrodite

Parasites have been proposed to be fundamental in the evolution of mate choice because differential mating on the basis of heritable disease resistance is expected to lead to progeny with a better genome-environment match than random mating. However, direct empirical data in support of this hypothesis are often lacking, and the relative influences of current and potential infection status (i.e. resistance genotype), and of mate choice versus mate conflict, remain largely unknown. We demonstrate experimentally, using simultaneous hermaphroditic snails (Biomphalaria glabrata) artificially selected for resistance or susceptibility to Schistosoma mansoni infection, that mate choice is influenced by a combination of current and potential parasitic infection status. As predicted by game-theory models, we also found a picture of conflict and cooperation: resistant and susceptible genotypes copulated in either gender and reciprocated (i.e. switched gender) equally when faced with an uninfected partner, but, by contrast, resistant snails actively refused to copulate as females with an infected partner. Such recognition and discrimination has implications for the maintenance of sex and the evolution of recognition systems.     

Reproductive patterns in mantled howler monkeys: Estrus,mate choice and copulation

The present study was undertaken to evaluate non-random mating patterns in two groups of mantled howler monkeys in two tropical dry forest habitats. Sexual dimorphism, female estrus stage, male dominance rank, sexual solicitations and copulations were assessed. Males are significantly larger than females, but female weight varies more than male weight. The length of female estrus cycles is comparable in both habitats, but females in the more strongly seasonal habitat demonstrate greater estrus synchrony relative to their numbers. Males solicit potential mates more frequently than females, a pattern explained by the relatively high rate of sexual solicitation by high-ranking males. Females in “peak” estrus solicit “alpha” males, while females in other stages of estrus solicit males equally by rank. Intersexual aggression occurs rarely, and “forced copulations” are attempted but, apparently, are unsuccessful. Sexual solicitations by “alpha” males and “peak” estrus females are most likely to lead to copulation, and “alpha” males are more likely to copulate than “gamma” males. In general, latencies from first solicitation to copulation are expensive in time, especially for high-ranking males. Estimated annual reproduction success favors high-ranking males, and results indicate that male and female mating behavior is mutually coordinated and controlled.     

Predation risk and inter-population variation in antipredator behaviour in the three-spined stickleback, Gasterosteus aculeatus L.

Predation risk from fish and bird predators was assessed at seven Scottish Gasterosteus aculeatus L. sites. Samples of adult male and female sticklebacks and fry from each site were tested with either a model heron or a live pike to measure anti-predator responses. Principal Component Analyses were then used to describe the responses, the first factor to emerge from each multivariate analysis providing an index of overall level of response toward the predator. Significant sexual and inter-population differences in behaviour are described. Sticklebacks from populations at high risk from either predatory fish or birds showed higher fright response scores than fish from low risk sites. In general, adult male sticklebacks are bolder than adult females during interactions with predators.     

Ultraviolet light and visual behaviour in the three-spined stickleback, Gasterosteus aculeatus

The ability of various vertebrates to perceive visual information in the ultraviolet region of the electromagnetic spectrum (300-400 nm) is receiving increasing interest. To date, many of these studies have concentrated on the role of ultraviolet perception in mate choice, yet there are several ways in which the ability to perceive ultraviolet information may affect other behaviours. Until now, it has been widely assumed that colour in the three-spined stickleback can be quantified by methods appropriate to the human visual system. However, evidence does exist that suggests that, in some populations, sticklebacks are capable of perceiving ultraviolet wavelengths. Using a behavioural technique, we tested the ability of the stickleback to perceive ultraviolet light under full-spectrum conditions to establish whether such wavelengths are utilised within their normal behavioural repertoire. We tested this ability by assessing whether subjects could locate hidden food in a foraging task where food position was indicated by the position of landmarks. These landmarks differed only in their ultraviolet content, appearing identical when viewed across the human visible region of the spectrum. We found that sticklebacks were able to use ultraviolet perception to locate a foraging patch under full-spectrum conditions.     

RSCA genotyping of MHC for high-throughput evolutionary studies in the model organism three-spined stickleback Gasterosteus aculeatus

Background  

In all jawed vertebrates, highly polymorphic genes of the major histocompatibility complex (MHC) encode antigen presenting molecules that play a key role in the adaptive immune response. Their polymorphism is composed of multiple copies of recently duplicated genes, each possessing many alleles within populations, as well as high nucleotide divergence between alleles of the same species. Experimental evidence is accumulating that MHC polymorphism is a result of balancing selection by parasites and pathogens. In order to describe MHC diversity and analyse the underlying mechanisms that maintain it, a reliable genotyping technique is required that is suitable for such highly variable genes.     

Mating patterns,mate choice,and birth season heterosexual relationships in free-ranging rhesus macaques

Birth season adult heterosexual nonkin relationships of 50 free-ranging female rhesus macaques (Macaca mulatta) in two social groups at Cayo Santiago, Puerto Rico were examined using focal follow (289 hr) and ad lib data. Eighty-eight percent of subjects had at least one relationship characterized by particularly high frequencies of spatial proximity, grooming, or both. These were designated “friendships.” Males intervened in aggressive interactions more frequently on behalf of Friends than non-Friends. Female aggressive support of males was extremely rare. Higher-ranking males experienced more friendships than lower-ranking males. High-ranking females had higher-ranking Friends than low-ranking females. Older females had higher-ranking Friends than younger females. Females groomed high-ranking Friends more than they were groomed by them, whereas they groomed low-ranking Friends less than they were groomed by them. In one social group, high-ranking females were more likely than low-ranking females to groom their Friends more than they were groomed by them. Males were more responsible than females for spatial proximity maintenance in 9 of 14 Friend dyads for which sufficient data were available. Neither male nor female dominance rank affected responsibility for proximity maintenance in Friend dyads. Eight of 24 females had friendships with males with whom they had completed copulations during their conception peri-ovulatory period of the preceding mating season. Two of 19 females completed peri-ovulatory copulations with Friends during the following mating season. Friendship was not correlated with either of two demonstrated female mate choice indicators: (1) proximity maintenance during estrus; or (2) cooperation with male “hip-grasp” courtship attempts. Males directed “muzzle-up” courtship signals at lower rates toward Friends than toward non-Friends. These and other investigators' results indicate that (1) protection from aggression is the primary benefit to female rhesus macaques of birth season heterosexual relationships; (2) the most effective protectors are in greatest demand as Friends; and (3) friendship has no effect or an inhibitory effect on mate choice in this species. Benefits to males of friendships were not apparent from this study but may include coalitional support against lower-ranking males.