Populations Of Threespine Stickleback Research Articles

Behavioural syndromes differ predictably between 12 populations of three‐spined stickleback

Animals often differ in suites of correlated behaviours, comparable with how humans differ in personality. Constraints on the architecture of behaviour have been invoked to explain why such 'behavioural syndromes' exist. From an adaptationist viewpoint, however, behavioural syndromes should evolve only in those populations where natural selection has favoured such trait covariance, and they should therefore exist only in particular types of population. A comparative approach was used to examine this prediction of the adaptive hypothesis. We measured behavioural correlations in 12 different populations of three-spined stickleback (Gasterosteus aculeatus) and assessed whether they indeed varied consistently according to the selective environment, where population was unit of analysis. For a sample of fry from each population, we measured five different behaviours within the categories of (i) aggression (towards conspecifics); (ii) general activity; and (iii) exploration-avoidance (of novel foods, novel environments and altered environments). We show that behavioural syndromes are not always the same in different types of stickleback population: the often-documented syndrome between aggressiveness, activity and exploratory behaviour existed only in large ponds where piscivorous predators were present. In small ponds where predators were absent, these behaviours were not (or only weakly) associated. Our findings imply that population variation in behavioural syndromes does not result from stochastic evolutionary processes, but may result instead from adaptive evolution of behaviour favouring what should prove to be optimal trait combinations.

Parallel Evolution of Pitx1 Underlies Pelvic Reduction in Scottish Threespine Stickleback (Gasterosteus aculeatus)

Little is known about the genetic and molecular mechanisms that underlie adaptive phenotypic variation in natural populations or whether similar genetic and molecular mechanisms are utilized when similar adaptive phenotypes arise in independent populations. The threespine stickleback (Gasterosteus aculeatus) is a good model system to investigate these questions because these fish display a large amount of adaptive phenotypic variation, and similar adaptive phenotypes have arisen in multiple, independent stickleback populations. A particularly striking pattern of parallel evolution in sticklebacks is reduction of skeletal armor, which has occurred in numerous freshwater locations around the world. New genetic and genomic tools for the threespine stickleback have made it possible to identify genes that underlie loss of different elements of the skeletal armor. Previous work has shown that regulatory mutations at the Pitx1 locus are likely responsible for loss of the pelvic structures in independent stickleback populations from North America and Iceland. Here we show that the Pitx1 locus is also likely to underlie pelvic reduction in a Scottish population of threespine stickleback, which has apparently evolved pelvic reduction under a different selection regime than the North American populations.

QUANTIFYING THE CONSTRAINING INFLUENCE OF GENE FLOW ON ADAPTIVE DIVERGENCE IN THE LAKE-STREAM THREESPINE STICKLEBACK SYSTEM

The constraining effect of gene flow on adaptive divergence is often inferred but rarely quantified. We illustrate ways of doing so using stream populations of threespine stickleback (Gasterosteus aculeatus) that experience different levels of gene flow from a parapatric lake population. In the Misty Lake watershed (British Columbia, Canada), the inlet stream population is morphologically divergent from the lake population, and presumably experiences little gene flow from the lake. The outlet stream population, however, shows an intermediate phenotype and may experience more gene flow from the lake. We first used microsatellite data to demonstrate that gene flow from the lake is low into the inlet but high into the outlet, and that gene flow from the lake remains relatively constant with distance along the outlet. We next combined gene flow data with morphological and habitat data to quantify the effect of gene flow on morphological divergence. In one approach, we assumed that inlet stickleback manifest well-adapted phenotypic trait values not constrained by gene flow. We then calculated the deviation between the observed and expected phenotypes for a given habitat in the outlet. In a second approach, we parameterized a quantitative genetic model of adaptive divergence. Both approaches suggest a large impact of gene flow, constraining adaptation by 80-86% in the outlet (i.e., only 14-20% of the expected morphological divergence in the absence of gene flow was observed). Such approaches may be useful in other taxa to estimate how important gene flow is in constraining adaptive divergence in nature.

Sexual Dimorphism in the External Morphology of the Threespine Stickleback (Gasterosteus Aculeatus)

Information about sexual dimorphism is essential for understanding the ecology, behavior, and life history of a species, as well as for making morphological comparisons between populations. Furthermore, in order to understand the evolution of sexual dimorphism, it is important to know whether sexual dimorphism is genetically determined or the result of phenotypic plasticity. To this end, we have characterized patterns of sexual dimorphism in the threespine stickleback (Gasterosteus aculeatus). These fish are widely distributed throughout the temperate Northern Hemisphere, and their behavior, ecology, and evolution have been extensively characterized. We first examined sexual dimorphism in morphometric and meristic characters of wild-caught threespine sticklebacks from multiple populations that demonstrate different life history strategies in order to understand general patterns of sexual dimorphism in the threespine stickleback. Next, we made several crosses by in vitro fertilization and raised them in the laboratory to investigate developmental and genetic contributions to sexual dimorphism. Morphological analysis of wild-caught breeding males and females from four North American and six Asian populations revealed that adult males have larger heads and mouths than adult females in all populations. In contrast, adult females were longer in standard length and had longer pelvic girdles than adult males in many populations. Sexual dimorphism in dorsal-spine length was variable among populations. Except for body size, sexual dimorphism in most external morphological traits was similar between wild-caught and lab-reared fish. However, sexual dimorphism was only observed after the fish became reproductively mature. These results suggest that general features of secondary sexual characters are shared across different threespine stickleback populations and that sexual dimorphism in some morphological traits may have a genetic basis.

PARALLEL EVOLUTION BY CORRELATED RESPONSE: LATERAL PLATE REDUCTION IN THREESPINE STICKLEBACK

Recent work has revealed the molecular mechanisms governing one of the most dramatic examples of parallel evolution in nature: the repeated loss of lateral plate armor in freshwater populations of threespine stickleback. Yet, the ecological mechanisms responsible for armor loss remain unclear. Using a balanced experimental design, we examined Heuts' (1947) hypothesis that selection due to differences in salinity indirectly drive the reduction of lateral plate armor in fresh water while maintaining armor in the sea. We measured two fitness-related traits, hatching success and juvenile growth rate, in offspring of reduced (low and partial) and complete lateral plate morphs from two polymorphic populations when raised in either fresh water or salt water. In contrast to Heuts' results, there was little difference among morphs in hatching success. However, salinity strongly influenced juvenile growth: offspring of reduced lateral plate morphs grew substantially faster (up to 65%) than offspring of completely plated morphs in fresh water, but there was little difference in salt water. We suggest that the parallel loss of lateral plates in fresh water has arisen through a correlated response to selection for faster growth during lateral plate development, but the effect of salinity on hatching success and juvenile growth rate cannot explain the predominance of completely plated morphs in marine populations.

Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes

Freshwater populations of three-spined sticklebacks (Gasterosteus aculeatus) in northern Germany are found as distinct lake and river ecotypes. Adaptation to habitat-specific parasites might influence immune capabilities of stickleback ecotypes. Here, naive laboratory-bred sticklebacks from lake and river populations were exposed reciprocally to parasite environments in a lake and a river habitat. Sticklebacks exposed to lake conditions were infected with higher numbers of parasite species when compared with the river. River sticklebacks in the lake had higher parasite loads than lake sticklebacks in the same habitat. Respiratory burst, granulocyte counts and lymphocyte proliferation of head kidney leucocytes were increased in river sticklebacks exposed to lake when compared with river conditions. Although river sticklebacks exposed to lake conditions showed elevated activation of their immune system, parasites could not be diminished as effectively as by lake sticklebacks in their native habitat. River sticklebacks seem to have reduced their immune-competence potential due to lower parasite diversity in rivers.

Social recognition in wild fish populations

The ability of animals to gather information about their social and physical environment is essential for their ecological function. Odour cues are an important component of this information gathering across taxa. Recent laboratory studies have revealed the importance of flexible chemical cues in facilitating social recognition of fishes. These cues are known to be mediated by recent habitat experience and fishes are attracted to individuals that smell like themselves. However, to be relevant to wild populations, where animals may move and forage freely, these cues would have to be temporally flexible and allow spatial resolution. Here, we present data from a study of social recognition in wild populations of three-spined sticklebacks (Gasterosteus aculeatus). Focal fish preferentially associated with conspecifics from the same habitat as themselves. These preferences were changed and updated following translocation of the focal fish to a different site. Further investigation revealed that association preferences changed after 3 h of exposure to different habitat cues. In addition to temporal flexibility, the cues also allowed a high degree of spatial resolution: fish taken from sites 200 m apart produced cues that were sufficiently different to enable the focal fish to discriminate and associate with fish captured near their own home site. The adaptive benefits of this social recognition mechanism remain unclear, though they may allow fish to orient within their social environment and gain current local information.

Editorial and Retrospective 2007

Editorial and Retrospective 2007

Extinction of a weakly armoured threespine stickleback (Gasterosteus aculeatus) population in Prator Lake, Alaska

Abstract – Threespine stickleback (Gasterosteus aculeatus) samples from Prator Lake in southcentral Alaska consist of the relatively rare form of weakly armoured individuals with few lateral plates and no pelvic spines. Prator Lake has been sampled for threespine stickleback since 1983. Exotic northern pike (Esox lucius) were first observed in this lake in 1996. The appearance of pike corresponds with a dramatic decrease in stickleback numbers and apparent local extinction. The stickleback population may have been vulnerable to an exotic predator because Prator Lake lacks native piscivorous fishes, and this population had extreme armour reduction.

Contrasting patterns of body shape and neutral genetic divergence in marine and lake populations of threespine sticklebacks

Comparisons of neutral marker and quantitative trait divergence can provide important insights into the relative roles of natural selection and neutral genetic drift in population differentiation. We investigated phenotypic and genetic differentiation among Fennoscandian threespine stickleback (Gasterosteus aculeatus) populations, and found that the highest degree of differentiation occurred between sea and freshwater habitats. Within habitats, morphological divergence was highest among the different freshwater populations. Pairwise phenotypic and neutral genetic distances among populations were positively correlated, suggesting that genetic drift may have contributed to the morphological differentiation among habitats. On the other hand, the degree of phenotypic differentiation (PST) clearly surpassed the neutral expectation set by FST, suggesting a predominant role for natural selection over genetic drift as an explanation for the observed differentiation. However, separate PST/FST comparisons by habitats revealed that body shape divergence between lake and marine populations, and even among marine populations, can be strongly influenced by natural selection. On the other hand, genetic drift can play an important role in the differentiation among lake populations.

Parallel genetic origins of pelvic reduction in vertebrates

Despite longstanding interest in parallel evolution, little is known about the genes that control similar traits in different lineages of vertebrates. Pelvic reduction in stickleback fish (family Gasterosteidae) provides a striking example of parallel evolution in a genetically tractable system. Previous studies suggest that cis-acting regulatory changes at the Pitx1 locus control pelvic reduction in a population of threespine sticklebacks (Gasterosteus aculeatus). In this study, progeny from intergeneric crosses between pelvic-reduced threespine and ninespine (Pungitius pungitius) sticklebacks also showed severe pelvic reduction, implicating a similar genetic origin for this trait in both genera. Comparative sequencing studies in complete and pelvic-reduced Pungitius revealed no differences in the Pitx1 coding sequences, but Pitx1 expression was absent from the prospective pelvic region of larvae from pelvic-reduced parents. A much more phylogenetically distant example of pelvic reduction, loss of hindlimbs in manatees, shows a similar left-right size bias that is a morphological signature of Pitx1-mediated pelvic reduction in both sticklebacks and mice. These multiple lines of evidence suggest that changes in Pitx1 may represent a key mechanism of morphological evolution in multiple populations, species, and genera of sticklebacks, as well as in distantly related vertebrate lineages.

LOCAL HETEROZYGOSITY-FITNESS CORRELATIONS WITH GLOBAL POSITIVE EFFECTS ON FITNESS IN THREESPINE STICKLEBACK

The complex interactions between genetic diversity and evolution have important implications in many biological areas including conservation, speciation, and mate choice. A common way to study these interactions is to look at heterozygosity-fitness correlations (HFCs). Until recently, HFCs based on noncoding markers were believed to result primarily from global inbreeding effects. However, accumulating theoretical and empirical evidence shows that HFCs may often result from genes being linked to the markers used (local effect). Moreover, local effect HFCs could differ from global inbreeding effects in their direction and occurrence. Consequently, the investigation of the structure and consequences of local HFCs is emerging as a new important goal in evolutionary biology. In this study of a wild threespine stickleback (Gasterosteus aculeatus) population, we first tested the presence of significant positive or negative local effects of heterozygosity at 30 microsatellites loci on five fitness components: survival, mating success, territoriality, length, and body condition. Then, we evaluated the direction and shape of total impact of local HFCs, and estimated the magnitude of the impacts on fitness using regression coefficients and selection differentials. We found that multilocus heterozygosity was not a reliable estimator of individual inbreeding coefficient, which supported the relevance of single-locus based analyses. Highly significant and temporally stable local HFCs were observed. These were mainly positive, but negative effects of heterozygosity were also found. Strong and opposite effects of heterozygosity are probably present in many populations, but may be blurred in HFC analyses looking for global effects only. In this population, both negative and positive HFCs are apparently driving mate preference by females, which is likely to contribute to the maintenance of both additive and nonadditive genetic variance.

Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation, host adaptation, or side effect?

Parasitic infections may cause alterations in host life history, including changes in reproductive investment (absolute amount of energy allocated to reproduction) and reproductive effort (proportion of available energy allocated to reproduction). Such changes in host life history may reflect: 1) a parasite tactic: the parasite adaptively manipulates energy flow within the host so that the host is induced to make a reduction in reproductive effort and reproductive investment, making more energy available to the parasite; 2) no tactic: there is no change in host reproductive effort and reproductive investment simply decreases as a side effect of the parasite depleting host energy stores; 3) a host tactic: the host adaptively increases reproductive effort in the face of infection and loss of body condition, reproductive investment possibly being reduced despite the increased reproductive effort. Females in Alaskan lake populations of threespine sticklebacks (Gasterosteus aculeatus) are capable of clutch production when parasitized by the cestode Schistocephalus solidus despite large relative parasite masses. We analyzed the somatic energy reserves, maturation stage and ovarian mass of female sticklebacks collected from an Alaska lake during a single reproductive season. We found that parasitized females were less likely to carry fully‐matured gametes, had smaller ovarian masses, and had lower somatic energy stores than unparasitized females. The relationship between reproductive investment and energy storage did not differ between parasitized and unparasitized females. Thus, reproductive effort did not change in response to parasitic infection. We conclude there was no indication of either a parasite tactic or a host tactic. Simple nutrient theft is involved in the parasite's influence on host reproduction, consistent with an earlier hypothesis that reproductive curtailment in threespine sticklebacks is a side effect.

Mitochondrial DNA evidence of an early Holocene population expansion of threespine sticklebacks from Scotland

In this study, we analyzed the cytochrome b gene in threespine stickleback ( Gasterosteus aculeatus) populations from Scotland. We found evidence of a postglacial population expansion in Scotland and large differences in genetic diversity estimates among populations. Higher levels of genetic diversity are negatively correlated with distance from the ocean. In addition, distance from the ocean and predation risk both explain variation in plate count in Scottish populations. Overall, the mtDNA data support the racemic model of evolution in threespine stickleback.

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.

Ornaments or offspring? Female sticklebacks (Gasterosteus aculeatus L.) trade off carotenoids between spines and eggs

Hypotheses and models to explain female ornaments often assume that the elaborated traits are condition dependent; nevertheless, few empirical studies have addressed this topic. We studied a population of three-spined sticklebacks (Gasterosteus aculeatus) in which the females have conspicuous, carotenoid-based red coloration to their pelvic spines. The red coloration seems not to be condition dependent, as coloration is negatively associated with age and body length and not associated with condition. Furthermore, redder females did not have a lower density of leucocytes. We found a negative association between the females' red carotenoid-based coloration in the spines and the amount of carotenoids in the female's gonads. Males choosing red-coloured females will fertilize eggs with small amounts of carotenoids and appear not to gain any benefit from their mates' phenotypic quality that could result in offspring of improved quality. These results do not support the 'direct selection hypothesis' to explain the existence of the female ornaments.

Geographical and Temporal FA Variation in Threespine Stickleback Populations from Galicia (NW Spain)

Subtle departures from bilateral symmetry (FA) in morphological traits has been used as a measure of developmental stability in populations subjected to genetic and environmental processes as inbreeding, pollution or parasitic infection. Geographic variation of FA was assessed in 19 threespine stickleback (Gasterosteus aculeatus) populations from Mino and Limia rivers, from Galicia (NW Spain). This variation was evaluated using four FA indices on five meristic and one morphometric traits. Temporal variation of FA was also assessed using several samples through time in only one population. Significant geographical variation was detected for pectoral fin rays, lateral forks, lateral plates and spine length. Lateral plates, upper gillrakers, pectoral fin rays and spine length showed significant variation through the time. The variation of FA through the time showed a common performance for all characters during the period considered: a slight increase in the intermediate months with a decrease at the end of the period. Symmetric and asymmetric sticklebacks exhibited similar infection, with one exception: symmetric sticklebacks for lower gillrakers of Antela populations exhibited increased parasite infection relative to asymmetric ones. Sticklebacks with extreme phenotypes exhibited much higher levels of asymmetry than modal ones in all samples for all traits.

Empirical Modelling of the Population Dynamics of a Small Population of the Threespine Stickleback, Gasterosteus aculeatus

We estimated the abundance of a small population of threespine stickleback, Gasterosteus aculeatus, by mark-recapture over a 21 year period. Length-frequency analysis showed that the population in October consisted almost entirely of young-of-the-year. The per capita annual rate of increase was inversely related to abundance in October. Time series analysis suggested the presence of a cycle of abundance with a period of about 6 years. There was a significant inverse relationship between abundance in year t and in year t + 3. A simple, empirical, deterministic model based on this inverse relationship and run for 100 years predicted that population abundance showed damped oscillations leading to a stable abundance. When a stochastic component was added to the model, seven of 10 runs included a component with a period of about 6 years. These simulations suggest that the dynamics of this population are driven by an interaction between a deterministic (density-dependent) component and a stochastic component. We compare these results with time series of abundance of threespine stickleback obtained from the Thames Estuary in south-east England and Loch Lomond in Scotland.

Heterozygosity and phylogenetic relationship of Japanese threespine stickleback (Gasterosteus aculeatus) populations revealed by microsatellite analysis

Heterozygosity and phylogenetic relationships were analyzed using eight microsatellite loci for nine freshwater and one anadromous populations of threespine stickleback Gasterosteus aculeatus from northern Japan. Fis values and Hardy–Weinberg tests indicated that nine of the populations were in heterozygote deficit. Furthermore, on-going isolation of most of the populations by artificial destruction of population connection and habitat deterioration suggested that nearly all of the populations are likely to be in a threatened condition. Phylogenetic analysis revealed that there were two distinctive phylogenetic groups, each of which was composed of two and three freshwater populations. These populations included in the groups except ones recently established were located in inland waters and isolated from anadromous populations, so that they may have been able to keep unique genetic features. Therefore, it is necessary to protect as many populations as possible within the local population network including these inland populations. On the other hand, for freshwater populations located near the river mouth but recently isolated from anadromous populations by weir construction, it is important to remove or ameliorate the barrier and recover the gene flow. Microsatellite markers are important tools to monitor the population network and gene flow.

Unusual number of pectoral fin rays in an Icelandic population of threespine stickleback (Gasterosteus aculeatus) recently isolated in freshwater

Threespine stickleback most often have 10 pectoral fin rays, and it seems to be a highly canalized trait. We observed an unusually high frequency of stickleback with 11 pectoral fin rays in a population recently isolated from the marine environment in a freshwater lagoon in Iceland. These new morphologies may be beneficial for the fish in the new habitat but may disappear because of strong canalizing selection for the typical 10 pectoral fin rays.