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.     

State-Dependent Mate-Assessment and Mate-Selection Behavior in Female Threespine Sticklebacks (Gasterosteus aculeatus, Gasterosteiformes: Gasterosteidae)

Most investigations of mate-choice have focused on the outcomes of mate-choice (i.e. which mates are chosen), and thus we generally know very little about how mates are chosen (i.e. how mates are found, assessed, and selected). Mate-choice by females has been shown to be dependent on the state of the female, with females being less selective when limited by time or energy. This result could be caused by changes in female mate-assessment or mate-selection behavior. We examined whether manipulations of time and energy affected the mate-choice behavior of female threespine stickleback ( Gasterosteus aculeatus ). We found that female mate-choice behavior, when not divided into stages, was affected by both of the manipulations. This matches previous findings. When we divided female courtship behavior into six stages, we found that the two manipulations affected different portions of the mate-choice process. The holding-time manipulation changed female behavior at the beginning and end of the mate-choice process and the swimming manipulation changed female behavior only at the end of the mate-choice process. Neither of the manipulations significantly affected female behavior in the middle portion of the mate-choice process. Thus, the mate-choice process appears to be composed of multiple state-dependent decisions. We discuss how a better mechanistic understanding of how female state affects female mate-choice behavior can produce testable predictions and provide a basis for investigating the evolution of mating systems.     

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

     

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.     

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.     

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.     

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.     

Brood Value and Life Expectancy as Determinants of Parental Investment in Male Three-spined Sticklebacks,Gasterosteus aculeatus

29 breeding male three-spined sticklebacks (Gasterosteus aculeatus) caught in the wild at different times in the breeding season were exposed simultaneously to a potential threat to their nest (a conspecific male) and to two hunting trout (potential predators of adult sticklebacks, seen through a transparent partition). By promoting a variety of protective responses, the presence of the predators reduced both the time spent confronting the intruder and the rate at which it was attacked. Subjects with a clutch of eggs in their nest maintained higher levels of territorial defence in the presence of predators than did those with an empty nest. However, those breeding later in the season took fewer risks to defend their nest. Possible proximate mechanisms responsible for these results are discussed. In addition, the adaptive significance of the behavioural changes is considered in the light of the value of the brood and the expected future reproductive output of the sticklebacks breeding at different times in the season.     

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.     

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.     

The Effects of Isolation on the Sensitization and Habituation of Aggression in the Threespine Stickleback (Gasterosteus aculeatus)

Our previous research showed that territorial threespine sticklebacks are more aggressive toward a male conspecific placed in their territory if they have been housed adjacent to a gravid female rather than a male or a nongravid female. This study replicated the condition of a territorial male with an adjacently housed male and compared the results with isolated territorial males. This permitted us to contrast explanations for the increased aggression when the neighbor was a gravid female. If the social context determines the level of aggression, then males with no neighbors (isolates) might be less aggressive because there would be no unique reproductive resource to protect nor any neighbor to protect resources from. Alternatively, if aggression is higher in the isolated group it might be because there was no male neighbor to redirect aggression toward. We found that isolated males were more aggressive toward an intruded male stimulus than males with a male neighbor. The study also provided evidence that sensitization produced by the appearance of an intruding male energizes other aggressive behavior, but not those related to feeding, nor does it cause increase in general activation as measured by increased locomotion.     

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.     

RESEARCH PAPER: Multiple Sexual Ornamentation Signals Male Quality and Predicts Female Preference in Minnows

Sexual ornamentation often consists of multiple components. Different sexual signals may indicate different aspects of mate quality or reflect quality in different time scales. On the other hand, same signals can have a dual function and are used both in male–male competition and courtship. Many fish species are capable of rapidly altering their colouration (ephemeral colour changes), but this capability is usually ignored in sexual selection studies. Here, we used experimentally manipulated social environments to study the ephemeral colour changes in multicomponent sexual signals of male minnows (Phoxinus phoxinus) during male–male competition and female choice. We found that the dominant males courted the females more actively and had redder and/or darker skin colouration than the subordinate males. Furthermore, darkness difference between subordinate and dominant males increased in the presence of female, which suggests that the male–male competition may increase the honesty of signalling and thus facilitate female choice. In support of this hypothesis, females had a strong behavioural preference towards the more colourful males, which may indicate female choice. As colourful males often had a higher social status than paler individuals, it is possible that females base their preference on male status, not only the colouration per se. In any case, our results suggest that sexual ornamentation of male minnows may signal status, courting activity and superior quality of the males and that these signals may have a dual function in both male–male competition and female choice. Females preferred different ornamental traits (dark and red colour patterns) relatively equally, indicating that mate choice is based on multiple cues.     

The Effect of Familiarity with Demonstrators on Social Learning in Three‐Spined Sticklebacks (Gasterosteus aculeatus)

Social learning is an important process in the spread of information, especially in changing environments where inherited behaviors may not remain relevant. In many species, the decision of whom to trust to have reliable information depends on the relationship between individuals. Many fish species, including three‐spined sticklebacks, preferentially associate with familiar individuals. Previous studies in three‐spined sticklebacks have provided mixed evidence about the effect of familiarity on social learning in this species. Therefore, this study further explores familiarity and social learning in sticklebacks, specifically from a demonstrator‐focused perspective. We found that in a food patch discrimination task, individuals with unfamiliar demonstrators performed significantly better than those with familiar demonstrators. In a problem‐solving task, we found that focal fish attended to the behavior of demonstrators, but we did not detect an effect of familiarity on performance, and indeed the proportion of individuals to solve the task after observing demonstrators was low. These results suggest that sticklebacks have a preference for unfamiliar demonstrators, but that the use of social information varies depending on context.     

Quantitative Differences in the Courtship of two Populations of Three-spined Sticklebacks,Gasterosteus aculeatus

Die männliche Balz einer amerikanischen Population des Dreistacheligen Stichlings wurde mit der der europäischen Variation verglichen. Die amerikanischen ♂ ♂ erreichen die Schwelle für die meisten sexuellen Verhaltensweisen viel langsamer; sie zeigen während der Balz mehr Nestaktivitäten und Stachelreizungen. Da es Anzeichen gibt, daß sie auch weit angriffslustiger sind, werden diese Handlungen (nach Wilz 1970 b) als bedeutsam für die Umstellung des ♂ auf sexuelles Verhalten aufgefaßt.     

Some aspects of adaptation in a polymorphism for breeding colours in the Threespine stickleback (Gasterosteus aculeatus))

Polymorphism in the nuptial colouration of male Threespine sticklebacks ( Garterosteus aculeatus L.) was studied. In Lake Wapato in Eastern Washington, approximately 14% of the breeding males develop typical red nuptial colouration while others develop various colours which were grouped into a non-red category. The hypothesis was tested that red males are adaptive in Lake Wapato as a result of sexual selection and differential egg predation.
In a series of mate preference tests, females demonstrated a significant preference for red males over non-red males. In a second experiment, using artiticially coloured non-red males, it was shown that the females are responding to the red colouration alone. This evidence suggests that one of the selective pressures maintaining the red morph is sexual selection.
In a stomach analysis of male and female sticklebacks collected from a breeding colony it was found that 51 % of the fish examined had stickleback eggs in their stomachs. Both male and female sticklebacks eat a large number of eggs; however, males eat significantly more eggs than females. Eggs were found to be most susceptible to predation during their first four days of development. Given that red ventral colouration has threat value, red males may also be adaptive because of a reduction in egg predation within their territories in contrast to non-red males.
One of the selective forces against red males is probably differential predation by trout ( Salmo gairdneri ). This trout predation has been shown to be extensive in Lake Wapato. The opposing selective forces discussed in this paper cannot maintain the polymorphism; they are only components of fitness of the colour morphs.     

Dynamics of Prolactin Axis Genes in the Brain of Male and Female Three-spined Stickleback Gasterosteus aculeatus (Gasterostaidae) during Short-Term Freshwater Adaptation

Journal of Ichthyology - Expression of prolactin axis genes (prolactin Prl1, prolactin-like hormone Prl2, prolactin receptor “a” PrlRa, and prolactin receptor “b” PrlRb)...     

Social Regulation of Gene Expression in Threespine Sticklebacks

Identifying genes that are differentially expressed in response to social interactions is informative for understanding the molecular basis of social behavior. To address this question, we described changes in gene expression as a result of differences in the extent of social interactions. We housed threespine stickleback (Gasterosteus aculeatus) females in either group conditions or individually for one week, then measured levels of gene expression in three brain regions using RNA-sequencing. We found that numerous genes in the hindbrain/cerebellum had altered expression in response to group or individual housing. However, relatively few genes were differentially expressed in either the diencephalon or telencephalon. The list of genes upregulated in fish from social groups included many genes related to neural development and cell adhesion as well as genes with functions in sensory signaling, stress, and social and reproductive behavior. The list of genes expressed at higher levels in individually-housed fish included several genes previously identified as regulated by social interactions in other animals. The identified genes are interesting targets for future research on the molecular mechanisms of normal social interactions.