Conspicuous Female Ornamentation and Tests of Male Mate Preference in Threespine Sticklebacks (Gasterosteus aculeatus)

Sexual selection drives the evolution of exaggerated male ornaments in many animal species. Female ornamentation is now acknowledged also to be common but is generally less well understood. One example is the recently documented red female throat coloration in some threespine stickleback (Gasterosteus aculeatus) populations. Although female sticklebacks often exhibit a preference for red male throat coloration, the possibility of sexual selection on female coloration has been little studied. Using sequential and simultaneous mate choice trials, we examined male mate preferences for female throat color, as well as pelvic spine color and standard length, using wild-captured threespine sticklebacks from the Little Campbell River, British Columbia. In a multivariate analysis, we found no evidence for a population-level mate preference in males, suggesting the absence of directional sexual selection on these traits arising from male mate choice. Significant variation was detected among males in their preference functions, but this appeared to arise from differences in their mean responsiveness across mating trials and not from variation in the strength (i.e., slope) of their preference, suggesting the absence of individual-level preferences as well. When presented with conspecific intruder males, male response decreased as intruder red throat coloration increased, suggesting that males can discriminate color and other aspects of phenotype in our experiment and that males may use these traits in intrasexual interactions. The results presented here are the first to explicitly address male preference for female throat color in threespine sticklebacks.     

Learning Influences Courtship Preferences of Male Threespine Sticklebacks (Gasterosteus aculeatus)

Male threespine sticklebacks (Gasterosteus aculeatus) prefer to court the more gravid of a pair of dummy females (Rowland 1982, 1989). In this study, males were trained to modify their courtship preferences. Males were given two pre-punishment preference trials during which two dummy females—one approximating a normally gravid female and the other, a supergravid female, possessing an abnormally large abdomen — were simultaneously presented to males. After pre-punishment trials, males were subjected to one of two punishment procedures: punishment with weak electric shock (Experiment I) or punishment by the removal of females to simulate female retreat (Experiment II). During punishment trials, males were punished each time they courted the supergravid dummy. Control males were subjected to identical trials, but were not punished for courting the supergravid dummy. Post-punishment preference trials were given to all males (Experiments I and II). The results of Experiments I and II were similar. Punished and control males did not differ in their courtship preferences in pre-punishment trials; they preferred to court the supergravid dummy. Punished males, however, spent a significantly lower proportion of time visiting and directed a smaller proportion of zigzags (a courtship display) toward the supergravid dummy than did control males during punishment training (Experiment I) and post-punishment preference trials (Experiments I and II). These results suggest that courtship preferences of male threespine sticklebacks can be modified through learning. Such a mechanism could be important for adaptive mate choice under natural conditions.     

Development of a Gill Assay Library for Ecological Proteomics of Threespine Sticklebacks (Gasterosteus aculeatus)

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Highlights

• •Construction of threespine stickleback gill assay library using DDA proteomics
• •Population-specific gill proteome signatures of four ecotypes identified by DIA
• •HSP47 and extracellular matrix proteins highly elevated in warm-adapted sticklebacks
• •Inflammasome and proteolytic proteins highly elevated in freshwater sticklebacks

     

Parasites may contribute to 'magic trait' evolution in the adaptive radiation of three-spined sticklebacks, Gasterosteus aculeatus (Gasterosteiformes: Gasterosteidae)

In the past decade, there has been a new effort to understand the ecology that drives population divergence and speciation. It is well established in theory that speciation is most likely to occur when a trait that is under divergent natural selection in different populations is also used in mate choice. Such traits have been dubbed 'magic traits' ( Gavrilets, 2004 ) and, although there appears to be good evidence that they exist, the ecological mechanisms that underlie their divergence are not well understood. Size at maturity in three-spined sticklebacks is an archetypal example of a magic trait. The present study documents for the first time that differences in body size at maturity in sympatric species pairs of lacustrine three-spined sticklebacks in British Columbia, Canada, are caused by differences in age at maturity. It is also shown that there are differences between the sympatric species in the patterns of infection with a virulent cestode, Schistocephalus solidus . Although the evidence is circumstantial, these differences in infection are consistent with the hypothesis that they have contributed to the observed divergence in age and size at maturity in these populations.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 425–433.     

A benthic predatory fish does not cause selection on armour traits in three‐spined stickleback Gasterosteus aculeatus (Gasterosteiformes: Gasterosteidae)

Predation can promote divergence between prey populations and contribute to ecological speciation. In theory, predators can also constrain prey population divergence. In coastal British Columbia, Canada, Gasterosteus aculeatus (three‐spined stickleback) species pairs only occur in lakes with a single species of predatory fish: Oncorhynchus clarkii (the cutthroat trout). Similar lakes containing additional predatory fish species (Cottus asper, prickly sculpins; Oncorhynchus mykiss, rainbow trout) contain only single species of morphologically intermediate stickleback, suggesting that these predators prevent the coexistence of stickleback species pairs. We conducted a mesocosm experiment to investigate how prickly sculpins might constrain divergence, by quantifying their impact on survival and natural selection on antipredator (armour) traits in F₂ stickleback from a cross between ecologically divergent populations. We tested three hypotheses: (1) sculpin predation on sticklebacks reduces survival in a way that could result in their exclusion from certain niches; (2) sculpins compete with stickleback; (3) sculpins respond to prey vulnerabilities in similar ways to cutthroat trout, tending to constrain rather than to enhance divergence. We found that sculpins significantly reduce stickleback survival, that their presence per se does not reduce growth in stickleback, and that predation did not result in selection on any of the armour traits measured, or on gill raker length, which is an important trophic trait. These results tend to refute hypotheses (2) and (3), while supporting hypothesis (1). © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 877–885.     

Variation in Age and Size in Fennoscandian Three-Spined Sticklebacks (Gasterosteus aculeatus)

Average age and maximum life span of breeding adult three-spined sticklebacks (Gasterosteus aculeatus) were determined in eight Fennoscandian localities with the aid of skeletochronology. The average age varied from 1.8 to 3.6 years, and maximum life span from three to six years depending on the locality. On average, fish from marine populations were significantly older than those from freshwater populations, but variation within habitat types was large. We also found significant differences in mean body size among different habitat types and populations, but only the population differences remained significant after accounting for variation due to age effects. These results show that generation length and longevity in three-spined sticklebacks can vary significantly from one locality to another, and that population differences in mean body size cannot be explained as a simple consequence of differences in population age structure. We also describe a nanistic population from northern Finland exhibiting long life span and small body size.     

Synaptonemal Complex Analysis in Oocytes and Spermatocytes of Threespine Stickleback Gasterosteus Aculeatus (Teleostei, Gasterosteidae)

A surface-spreading synaptonemal complex (SC) technique was employed to analyze spermatocytes and oocytes of stickleback, Gasterosteus aculeatus, in order to visualize the process of chromosome synapsis. The mean SC length was 150±18m in three males and 143±12m in one female analyzed. A representative SC karyotype with 21bivalents was also presented. Each SC had lateral elements of equal length. No bivalent displaying the atypical synaptic behaviour which is often associated with heteromorphic sex chromosomes was observed neither in males nor in the female analyzed.     

Osmotic and Ionic Regulation in Three-Spined Sticklebacks,Gasterosteus aculeatus Linnaeus 1758 (Gasterosteidae), from the White Sea and Freshwater Lake Krivoe

Russian Journal of Marine Biology - Several three-spined sticklebacks, Gasterosteus aculeatus Linnaeus, 1758, were live captured in the White Sea and acclimated to the conditions of freshwater Lake...     

Rapid Morphological Changes in Threespine Stickleback, Gasterosteus aculeatus, in Freshwater

Synopsis Freshwater and marine threespine stickleback, Gasterosteus aculeatus, differ remarkably in armour plate number and body shape, although differences in other morphological characters are also common. Most freshwater populations have apparently evolved after isolation of marine sticklebacks in freshwater. After colonisation of freshwater habitats, they show rapid morphological changes and associated genetic isolation within as few as eight generations. I transferred fish from marine tide pools to two isolated freshwater ponds, differing in habitat characteristics, at the beginning of the breeding season, when females had ripe ovaries and males had breeding coloration. The first generation fish that I sampled from the ponds had significantly fewer armour plates than their marine ancestors and differed in shape. I also found some significant differences between fish sampled from the larger pond and those from a smaller, adjacent pond. This extremely rapid morphological divergence suggests that either the marine sticklebacks were highly phenotypically plastic or that there was very strong natural selection acting on the first generation within freshwater habitats.     

Interacting evolutionary constraints in pelvic reduction of threespine sticklebacks, Gasterosteus aculeatus (Pisces, Gasterosteidae)

The pelvic girdle of Gasterosteus aculeatus is normally a complex and robust structure that varies moderately among and within populations, but in several populations it occurs as a vestigial series. Based on 14 Recent and fossil populations from North America and Scotland, three general patterns of intrapopulation variation of vestigial pelvic structures can be recognized. In most cases of pelvic reduction, the size and complexity of the pelvic girdle are reduced mostly by progressive truncation of distal structures, but two patterns of distal truncation occur. Paedomorphosis appears to play a role in all cases of pelvic reduction, but in a fossil assemblage and one extant population it accounts for most of the structural simplification.
Pelvic reduction in populations of Gasterosteus depends on an interaction between natural selection, which appears to determine whether or not pelvic reduction occurs, and phylogenetic constraint (especially developmental constraint), which strongly influences the form of pelvic vestiges. The empirical difficulty of discriminating between phylogenetic constraint and effects of natural selection, and the potential for phylogenetic constraint to produce homoplasy are discussed. Pelvic reduction apparently has been a recurrent phenomenon in Gasterosteus since at least the early Pliocene, but it has not resulted in evolution of a separate lineage of 'pelvicless' sticklebacks because such populations are restricted to lakes, which are ephemeral over evolutionary time. Rapid phyletic pelvic reduction coupled with selective extinction of populations with vestigial pelvic structures has resulted in phylogenetic stasis.     

Asymmetrical Effects of Prior Winning and Losing on Dominance in Sticklebacks (Gasterosteus aculeatus)

Reproductive male three-spined sticklebacks, Gasterosteus aculeatus L., without fighting experience, were given either an experience of dominance or an experience of inferiority. They were then tested for their ability to dominate an inexperienced male in a dyadic combat either a) immediately following the experience treatment, b) 3 h later or c) 6 h later. The effect of prior losing proved to be stronger and more prolonged than that of prior winning. The influence of non-experimental factors, and possible causes for this asymmetrical effect are discussed.     

Landscape Genetics of Schistocephalus solidus Parasites in Threespine Stickleback (Gasterosteus aculeatus) from Alaska

The nature of gene flow in parasites with complex life cycles is poorly understood, particularly when intermediate and definitive hosts have contrasting movement potential. We examined whether the fine-scale population genetic structure of the diphyllobothriidean cestode Schistocephalus solidus reflects the habits of intermediate threespine stickleback hosts or those of its definitive hosts, semi-aquatic piscivorous birds, to better understand complex host-parasite interactions. Seventeen lakes in the Cook Inlet region of south-central Alaska were sampled, including ten in the Matanuska-Susitna Valley, five on the Kenai Peninsula, and two in the Bristol Bay drainage. We analyzed sequence variation across a 759 bp region of the mitochondrial DNA (mtDNA) cytochrome oxidase I region for 1,026 S. solidus individuals sampled from 2009-2012. We also analyzed allelic variation at 8 microsatellite loci for 1,243 individuals. Analysis of mtDNA haplotype and microsatellite genotype variation recovered evidence of significant population genetic structure within S. solidus. Host, location, and year were factors in structuring observed genetic variation. Pairwise measures revealed significant differentiation among lakes, including a pattern of isolation-by-distance. Bayesian analysis identified three distinct genotypic clusters in the study region, little admixture within hosts and lakes, and a shift in genotype frequencies over time. Evidence of fine-scale population structure in S. solidus indicates that movement of its vagile, definitive avian hosts has less influence on gene flow than expected based solely on movement potential. Observed patterns of genetic variation may reflect genetic drift, behaviors of definitive hosts that constrain dispersal, life history of intermediate hosts, and adaptive specificity of S. solidus to intermediate host genotype.     

Agonistic Interactions in Juvenile Sticklebacks (Gasterosteus aculeatus) in Relation to Local Predation Risk

Size-matched groups of three-spined stickleback (Gasterosteus aculeatus) fry were established using fish from two sites, one with abundant piscivorous predators (the high-risk site) and the other with very few heterospecific predators (the low-risk site). Over a period of two months, social interactions within groups were monitored regularly and mean lengths and coefficients of variance in length were tracked. Agonistic behaviour was observed in 45% of observation periods, but was more common in the groups of fry from the low-risk site, where it was more likely to take the form of direct attack rather than displacement without contact. In both categories of fish, the great majority of agonistic acts were directed to fish of a similar size or smaller. Mean size increased rapidly in all groups. At the same time, the coefficient of variation also increased, approaching 15% after two months in both categories of fish, reflecting differing growth rates among individuals. After three months, the two largest and the two smallest fish from each group were observed individually during an encounter with a model predatory fish. Large and small fish from both sites behaved identically in this test, suggesting that in sticklebacks (unlike guppies, for example) early experience of aggressive attacks from conspecific companions may not influence the development of anti-predator responses. As has been reported previously, sticklebacks from the high-risk site responded much more strongly than low-risk fish.     

Divergent Macroparasite Infections in Parapatric Swiss Lake-Stream Pairs of Threespine Stickleback (Gasterosteus aculeatus)

Spatial heterogeneity in diversity and intensity of parasitism is a typical feature of most host-parasite interactions, but understanding of the evolutionary implications of such variation is limited. One possible outcome of infection heterogeneities is parasite-mediated divergent selection between host populations, ecotypes or species which may facilitate the process of ecological speciation. However, very few studies have described infections in population-pairs along the speciation continuum from low to moderate or high degree of genetic differentiation that would address the possibility of parasite-mediated divergent selection in the early stages of the speciation process. Here we provide an example of divergent parasitism in freshwater fish ecotypes by examining macroparasite infections in threespine stickleback (Gasterosteus aculeatus) of four Swiss lake systems each harbouring parapatric lake-stream ecotype pairs. We demonstrate significant differences in infections within and between the pairs that are driven particularly by the parasite taxa transmitted to fish from benthic invertebrates. The magnitude of the differences tended to correlate positively with the extent of neutral genetic differentiation between the parapatric lake and stream populations of stickleback, whereas no such correlation was found among allopatric populations from similar or contrasting habitats. This suggests that genetic differentiation is unrelated to the magnitude of parasite infection contrasts when gene flow is constrained by geographical barriers while in the absence of physical barriers, genetic differentiation and the magnitude of differences in infections tend to be positively correlated.     

LHRH-immunoreactive cells in the brain of the three-spined stickleback,Gasterosteus aculeatus L. (Gasterosteidae)

Summary Cells immunoreactive with an anti-LHRH serum were visualized in the brain of the three-spined stickleback, Gasterosteus aculeatus, by means of the PAP technique. Positive cells were found in a periventricular position in the nucleus praeopticus pars magnocellularis, the nucleus dorsomedialis thalami, the nucleus ventromedialis thalami, the nucleus periventricularis posterior, and in the periventricular dorsomedian tegmentum. These cells were frequently observed to contact the CSF.     

Age,Experience and the Development of Adaptive Variation in Anti-predator Responses in Three-spined Sticklebacks (Gasterosteus aculeatus)

Stickleback fry (approx. 10 mm in length) were collected from two sites in Scotland, one with abundant predatory fish and birds and the other free of predation. The fry were reared in the laboratory until they reached a length of about 30 mm, at which time fry of the same length were caught from the two study sites. 10 fish from each size and rearing category (10 mm fry, 30 mm labreared fry and 30 mm wild-caught fry) and from each population were exposed singly to a silhouette of an avian predator moved above the surface of the tank. On average 50% of the fish jumped away on sighting the model, and there were no differences between the groups in the proportion of fish giving this response. Other aspects of the anti-predator repertoire of sticklebacks (in particular, remaining motionless after an encounter) were absent in 10 mm fry from both sites. Protective responses appeared (in fish from the predated but not the unpredated site) by the time they reached a length of 30 mm, regardless of whether they were laboratory-reared or wild-caught. Thus adaptive behavioural differences between these two populations arise as sticklebacks from the heavily predated site develop responses that fail to appear in those from the unpredated site and that are independent of direct experience of predatory attack.     

Gravidity‐Associated Shoaling Decisions in Three‐Spined Sticklebacks (Gasterosteus aculeatus)

Group living has evolved in many animal species as an antipredator behavior, an evolutionary effect that might be augmented by grouping with similarly looking individuals. Consequently, groups are often composed according to species, size, or coloration. During egg ripening or embryo growth, the outer appearance of females often changes drastically within days, which makes them more prone to predation. Thus, a female's group preference should change according to her reproductive state, an issue that has seldom been investigated. To test this, we gave gravid and non‐gravid three‐spined sticklebacks (Gasterosteus aculeatus) the choice to shoal either with a gravid or a non‐gravid conspecific. The results showed that shoaling preferences of gravid and non‐gravid individuals differed significantly. Non‐gravid females preferred gravid fish as shoaling partners, which might rely on the fact that gravid sticklebacks show reduced escape performance, which in turn might increase a non‐gravid female's chance of survival. However, in contrast to our predictions, gravid fish did not show any significant preference. A reason for this pattern might be competition between gravid females for mating partners, which might overrule benefits of shoaling with similar looking individuals. Hence, gravidity influences social preferences in a shoaling fish, which might pose a largely overlooked form of the cost of reproduction.