Populations Of Threespine Stickleback Research Articles

Predicting population-level impacts of projected climate heating on a temperate freshwater fish.

Climate heating has the potential to drive changes in ecosystems at multiple levels of biological organization. Temperature directly affects the inherent physiology of plants and animals, resulting in changes in rates of photosynthesis and respiration, and trophic interactions. Predicting temperature-dependent changes in physiological and trophic processes, however, is challenging because environmental conditions and ecosystem structure vary across biogeographical regions of the globe. To realistically predict the effects of projected climate heating on wildlife populations, mechanistic tools are required to incorporate the inherent physiological effects of temperature changes, as well as the associated effects on food availability within and across comparable ecosystems. Here we applied an agent-based bioenergetics model to explore the combined effects of projected temperature increases for 2100 (1.4, 2.7, and 4.4°C), and associated changes in prey availability, on three-spined stickleback (Gasterosteus aculeatus) populations representing latitudes 50, 55, and 60°N. Our results showed a decline in population density after a simulated 1.4°C temperature increase at 50°N. In all other modeled scenarios there was an increase (inflation) in population density and biomass (per unit area) with climate heating, and this inflation increased with increasing latitude. We conclude that agent-based bioenergetics models are valuable tools in discerning the impacts of climate change on wild fish populations, which play important roles in aquatic food webs.

Destabilized host-parasite dynamics in newly founded populations.

When species disperse into previously unoccupied habitats, new populations encounter unfamiliar species interactions such as altered parasite loads. Theory predicts that newly founded populations should exhibit destabilized eco-evolutionary fluctuations in infection rates and immune traits. However, to understand founder effects biologists typically rely on retrospective studies of range expansions, missing early-generation infection dynamics. To remedy this, we experimentally founded whole-lake populations of threespine stickleback. Infection rates were temporally stable in native source lakes. In contrast, newly founded populations exhibit destabilized host-parasite dynamics: high starting infection rates led to increases in a heritable immune trait (peritoneal fibrosis), suppressing infection rates. The resulting temporal auto-correlation between infection and immunity suggest that newly founded populations can exhibit rapid host-parasite eco-evolutionary dynamics.

Fine-scale contemporary recombination variation and its fitness consequences in adaptively diverging stickleback fish

Despite deep evolutionary conservation, recombination rates vary greatly across the genome and among individuals, sexes and populations. Yet the impact of this variation on adaptively diverging populations is not well understood. Here we characterized fine-scale recombination landscapes in an adaptively divergent pair of marine and freshwater populations of threespine stickleback from River Tyne, Scotland. Through whole-genome sequencing of large nuclear families, we identified the genomic locations of almost 50,000 crossovers and built recombination maps for marine, freshwater and hybrid individuals at a resolution of 3.8 kb. We used these maps to quantify the factors driving variation in recombination rates. We found strong heterochiasmy between sexes but also differences in recombination rates among ecotypes. Hybrids showed evidence of significant recombination suppression in overall map length and in individual loci. Recombination rates were lower not only within individual marine–freshwater-adaptive loci, but also between loci on the same chromosome, suggesting selection on linked gene ‘cassettes’. Through temporal sampling along a natural hybrid zone, we found that recombinants showed traits associated with reduced fitness. Our results support predictions that divergence in cis-acting recombination modifiers, whose functions are disrupted in hybrids, may play an important role in maintaining differences among adaptively diverging populations.

Short-term heat waves have long-term consequences for parents and offspring in stickleback.

Extreme temperature events, such as heat waves, can have lasting effects on the behavior, physiology, and reproductive success of organisms. Here, we examine the impact of short-term exposure to a simulated heat wave on condition, parental care, and reproductive success in a population of threespine stickleback (Gasterosteus aculeatus), a small fish with exclusive paternal care, currently experiencing regular heat waves. Males were either exposed to a simulated heat wave (23 °C) for 5 d or held at an ideal temperature (18 °C). Following this 5-d treatment, all males were transferred to 18 °C, where they completed a full parenting cycle. Offspring were raised at 18 °C. We found that while mass and body condition were unaffected in males exposed to a heat wave, cortisol responses were dampened across the nesting cycle compared to control males. In addition, heat wave males had longer latency for eggs to hatch, lower hatching success, and showed lower levels of parental care behavior compared to control males. Offspring of heat wave males had lower body condition, affecting swimming performance. Altogether, our results highlight the long-term impact that even short-term events can have on reproductive success, parental behavior, and subsequent generations, providing insight into population responses to rapid environmental change.

Divergence in Reproductive Behaviors Is Associated with the Evolutionary Loss of Parental Care.

AbstractThe mechanisms underlying the divergence of reproductive strategies between closely related species are still poorly understood. Additionally, it is unclear which selective factors drive the evolution of reproductive behavioral variation and how these traits coevolve, particularly during early divergence. To address these questions, we quantified behavioral differences in a recently diverged pair of Nova Scotian three-spined stickleback (Gasterosteus aculeatus) populations, which vary in parental care, with one population displaying paternal care and the other lacking this. We compared both populations, and a full reciprocal F1 hybrid cross, across four major reproductive stages: territoriality, nesting, courtship, and parenting. We identified significant divergence in a suite of heritable behaviors. Importantly, F1 hybrids exhibited a mix of behavioral patterns, some of which suggest sex linkage. This system offers fresh insights into the coevolutionary dynamics of reproductive behaviors during early divergence and offers support for the hypothesis that coevolutionary feedback between sexual selection and parental care can drive rapid evolution of reproductive strategies.

The role of fish predators and their foraging traits in shaping zooplankton community structure.

Differentiation of foraging traits among predator populations may help explain observed variation in the structure of prey communities. However, few studies have investigated the phenotypic effects of predators on their prey in natural communities. Here, we use a comparative analysis of 78 Greenlandic lakes to examine how foraging trait variation among threespine stickleback populations can help explain variation in zooplankton community composition among lakes. We find that landscape-scale variation in zooplankton composition was jointly explained by lake properties, such as size and water chemistry, and the presence and absence of both stickleback and arctic char. Additional variation in zooplankton community structure can be explained by stickleback jaw protrusion, a trait with known utility for foraging on zooplankton, but only in lakes where stickleback co-occur with arctic char. Overall, our results illustrate how trait variation of predators, alongside other ecosystem properties, can influence the composition of prey communities in nature.

Experimental evidence for adaptive divergence in response to a warmed habitat reveals roles for morphology, allometry and parasite resistance

AbstractEctotherms are expected to be particularly vulnerable to climate change–driven increases in temperature. Understanding how populations adapt to novel thermal environments will be key for informing mitigation plans. We took advantage of threespine stickleback (Gasterosteus aculeatus) populations inhabiting adjacent geothermal (warm) and ambient (cold) habitats to test for adaptive evolutionary divergence using a field reciprocal transplant experiment. We found evidence for adaptive morphological divergence, as growth (length change) in non‐native habitats related to head, posterior and total body shape. Higher growth in fish transplanted to a non‐native habitat was associated with morphological shape closer to native fish. The consequences of transplantation were asymmetric with cold sourced fish transplanted to the warm habitat suffering from lower survival rates and greater parasite prevalence than warm sourced fish transplanted to the cold habitat. We also found divergent shape allometries that related to growth. Our findings suggest that wild populations can adapt quickly to thermal conditions, but immediate transitions to warmer conditions may be particularly difficult.

Characterizing contemporary evolutionary change in a recently isolated population of threespine stickleback (Gasterosteus aculeatus L.)

Characterizing contemporary evolutionary change in a recently isolated population of threespine stickleback (<i>Gasterosteus aculeatus</i> L.)

Variation in morphology among populations of threespine stickleback (Gasterosteus aculeatus) from western Newfoundland, Canada

Variation in morphology among populations of threespine stickleback (Gasterosteus aculeatus) from western Newfoundland, Canada

Repeatability of crossover rate in wild sticklebacks

AbstractCrossovers in meiosis have an important role in sexual reproduction in ensuring the segregation of chromosomes and shuffling of genetic material. Despite their profound importance, little is known about heritability and repeatability of the crossover rate in the wild. We studied crossover rate variation in outbred nine- (Pungitius pungitius) and three-spined (Gasterosteus aculeatus) stickleback populations to estimate its heritability (h2) and repeatability (R). Based on crossover rate interpreted from parent–F1-offspring linkage maps created from single nucleotide polymorphism data, the repeatability of crossover rate was moderate at best, but higher in females (R = 0.24 and R = 0.33) than in males (R = 0.017 and R = 0.11) in both species. Owing to the low degree and variance of parental relatedness and low sample sizes, heritabilities could not be estimated with confidence. However, given that R sets the upper limit to h2, the heritability of crossover rate is indicated to be low in males. A review and comparison with the previously reported repeatability and heritability estimates revealed that the repeatabilities in stickleback females were relatively high, whereas those in males were very low. Collectively, our results and review of earlier estimates suggest low evolvability of the crossover rate.

Molecular mechanisms of Eda-mediated adaptation to freshwater in threespine stickleback.

A main goal of evolutionary biology is to understand the genetic basis of adaptive evolution. Although the genes that underlie some adaptive phenotypes are now known, the molecular pathways and regulatory mechanisms mediating the phenotypic effects of those genes often remain a black box. Unveiling this black box is necessary to fully understand the genetic basis of adaptive phenotypes, and to understand why particular genes might be used during phenotypic evolution. Here, we investigated which genes and regulatory mechanisms are mediating the phenotypic effects of the Eda haplotype, a locus responsible for the loss of lateral plates and changes in the sensory lateral line of freshwater threespine stickleback (Gasterosteus aculeatus) populations. Using a combination of RNAseq and a cross design that isolated the Eda haplotype on a fixed genomic background, we found that the Eda haplotype affects both gene expression and alternative splicing of genes related to bone development, neuronal development and immunity. These include genes in conserved pathways, like the BMP, netrin and bradykinin signalling pathways, known to play a role in these biological processes. Furthermore, we found that differentially expressed and differentially spliced genes had different levels of connectivity and expression, suggesting that these factors might influence which regulatory mechanisms are used during phenotypic evolution. Taken together, these results provide a better understanding of the mechanisms mediating the effects of an important adaptive locus in stickleback and suggest that alternative splicing could be an important regulatory mechanism mediating adaptive phenotypes.

Plate reduction in southern Japanese freshwater populations of threespine stickleback (Gasterosteus aculeatus).

Adaptation to similar environments can lead to the evolution of similar phenotypes in phylogenetically independent lineages. However, the extent of parallel evolution often varies. Because such variations can be due to environmental heterogeneity among seemingly similar habitats, identification of the environmental factors that cause non-parallel patterns can provide valuable insight into the ecological factors associated with phenotypic diversification. Armor plate reduction in replicate freshwater populations of the threespine stickleback (Gasterosteus aculeatus) represents a well-known example of parallel evolution. Many freshwater populations in multiple regions of the Northern Hemisphere have reduced plate numbers, but not all freshwater populations exhibit plate reduction. In this study, we characterized plate number variation in Japanese freshwater populations and investigated the association between plate number and several abiotic environmental factors. We found that most freshwater populations have not reduced plate numbers in Japan. Plate reduction tends to occur in habitats with warmer winter temperatures at lower latitudes in Japan. In contrast, low dissolved calcium levels or water turbidity had no significant effects on plate reduction, although these were reported to be associated with plate reduction in Europe. Although our data are consistent with the hypothesis that winter temperatures are associated with plate reduction, further studies on the relationship between temperatures and fitness using sticklebacks with varying plate numbers are necessary to confirm this hypothesis and understand the factors causing variations in the extent of parallel evolution.

Armour reduction and pelvic girdle loss in a population of threespine stickleback (Gasterosteus aculeatus) from western Newfoundland, Canada

Armour reduction and pelvic girdle loss in a population of threespine stickleback (Gasterosteus aculeatus) from western Newfoundland, Canada

Evolution of chemical-cue-mediated antipredator behavior in threespine stickleback populations experiencing northern pike predation

Evolution of chemical-cue-mediated antipredator behavior in threespine stickleback populations experiencing northern pike predation

Genome-phenotype-environment associations identify signatures of selection in a panmictic population of threespine stickleback.

Adaptive genetic divergence occurs when selection imposed by the environment causes the genomic component of the phenotype to differentiate. However, genomic signatures of natural selection are usually identified without information on which trait is responding to selection by which selective agent(s). Here, we integrate whole-genome sequencing with phenomics and measures of putative selective agents to assess the extent of adaptive divergence in threespine stickleback occupying the highly heterogeneous lake Mývatn, NE Iceland. We find negligible genome wide divergence, yet multiple traits (body size, gill raker structure and defence traits) were divergent along known ecological gradients (temperature, predatory bird densities and water depth). SNP based heritability of all measured traits was high (h2 =0.42-0.65), indicating adaptive potential for all traits. Environment-association analyses further identified thousands of loci putatively involved in selection, related to genes linked to, for instance, neuron development and protein phosphorylation. Finally, we found that loci linked to water depth were concurrently associated with pelvic spine length variation - supporting the conclusion that divergence in pelvic spine length occurred in the face of gene flow. Our results suggest that whilst there is substantial genetic variation in the traits measured, phenotypic divergence of Mývatn stickleback is mostly weakly associated with environmental gradients, potentially as a result of substantial gene flow. Our study illustrates the value of integrative studies that combine genomic assays of multivariate trait variation with landscape genomics.

Geothermal stickleback populations prefer cool water despite multigenerational exposure to a warm environment.

Given the threat of climate change to biodiversity, a growing number of studies are investigating the potential for organisms to adapt to rising temperatures. Earlier work has predicted that physiological adaptation to climate change will be accompanied by a shift in temperature preferences, but empirical evidence for this is lacking. Here, we test whether exposure to different thermal environments has led to changes in preferred temperatures in the wild. Our study takes advantage of a "natural experiment" in Iceland, where freshwater populations of threespine sticklebacks (Gasterosteus aculeatus) are found in waters warmed by geothermal activity year-round (warm habitats), adjacent to populations in ambient-temperature lakes (cold habitats). We used a shuttle-box approach to measure temperature preferences of wild-caught sticklebacks from three warm-cold population pairs. Our prediction was that fish from warm habitats would prefer higher water temperatures than those from cold habitats. We found no support for this, as fish from both warm and cold habitats had an average preferred temperature of 13°C. Thus, our results challenge the assumption that there will be a shift in ectotherm temperature preferences in response to climate change. In addition, since warm-habitat fish can persist at relatively high temperatures despite a lower-temperature preference, we suggest that preferred temperature alone may be a poor indicator of a population's adaptive potential to a novel thermal environment.

Dimensionality and Modularity of Adaptive Variation: Divergence in Threespine Stickleback from Diverse Environments.

AbstractPopulations are subjected to diverse environmental conditions that affect fitness and induce evolutionary or plastic responses, resulting in phenotypic divergence. Some authors contend that such divergence is concentrated along a single major axis of trait covariance even if that axis does not lead populations directly toward a fitness optimum. Other authors argue that divergence can occur readily along many phenotype axes at the same time. We use populations of threespine stickleback (Gasterosteus aculeatus) from 14 lakes with contrasting ecological conditions to find some resolution along the continuum between these two extremes. Unlike many previous studies, we included several functional suites of traits (defensive, swimming, trophic) potentially subject to different sources of selection. We find that populations exhibit dimensionality of divergence that is high enough to preclude a history of constraint along a single axis-both for divergence in multivariate mean trait values and for the structure of trait covariances. Dimensionality varied among trait suites and were strongly influenced by the inclusion of specific traits, and integration of trait suites varied between populations. We leverage this variation into new insights about the process of divergence and suggest that similar analyses could increase understanding of other adaptive radiations.

Testing the predictability of morphological evolution in contrasting thermal environments.

Gaining the ability to predict population responses to climate change is a pressing concern. Using a "natural experiment," we show that testing for divergent evolution in wild populations from contrasting thermal environments provides a powerful approach, and likely an enhanced predictive power for responses to climate change. Specifically, we used a unique study system in Iceland, where freshwater populations of threespine sticklebacks (Gasterosteus aculeatus) are found in waters warmed by geothermal activity, adjacent to populations in ambient-temperature water. We focused on morphological traits across six pairs from warm and cold habitats. We found that fish from warm habitats tended to have a deeper mid-body, a subterminally orientated jaw, steeper craniofacial profile, and deeper caudal region relative to fish from cold habitats. Our common garden experiment showed that most of these differences were heritable. Population age did not appear to influence the magnitude or type of thermal divergence, but similar types of divergence between thermal habitats were more prevalent across allopatric than sympatric population pairs. These findings suggest that morphological divergence in response to thermal habitat, despite being relatively complex and multivariate, are predictable to a degree. Our data also suggest that the potential for migration of individuals between different thermal habitats may enhance nonparallel evolution and reduce our ability to predict responses to climate change.

Intraspecific diversity of threespine stickleback (Gasterosteus aculeatus) populations in eastern Canada

The threespine stickleback (Gasterosteus aculeatus) is a small, mesopredatory fish that is widespread in coastal regions of the northern hemisphere. Although studied extensively as a model organism in evolutionary biology, behavioral ecology, genomics, and numerous related subfields, this research relies heavily on populations from the Pacific coastal regions of North America and Asia, and those of northern Europe. However, based on the morphology of some western Atlantic populations, the different ecological context, and the evolutionary history of the species, not all of the knowledge gained from Pacific and European lineages is likely to be fully transferrable to the populations of North America’s East Coast. Nevertheless, work in eastern Canada does suggest high levels of intraspecific phenotypic diversity and local adaptation, though much of this diversity may be under threat from climate change, altered land use patterns, and introduced species. These factors warrant a research program focused on broad sampling of previously identified populations, identifying previously undocumented populations, determining whether there are unique genetic mechanisms underlying the unusual trait combinations present in the region, and exploring novel community interactions. Such a research program would facilitate future studies in ecology, conservation, and evolution by documenting phenotypic changes and establish baselines for future work. Because the work on nearshore marine threespine stickleback populations is sparse in the western Atlantic, I focus here on freshwater populations—with the exception of a brief discussion of the “white” stickleback populations of Nova Scotia—but this is not to suggest that nearshore marine populations are not phenotypically diverse.

Salinity-induced transcriptome profiles in marine and freshwater threespine stickleback after an abrupt 6-hour exposure.

Saltwater and freshwater environments have opposing physiological challenges, yet, there are fish species that are able to enter both habitats during short time spans, and as individuals they must therefore adjust quickly to osmoregulatory contrasts. In this study, we conducted an experiment to test for plastic responses to abrupt salinity changes in two populations of threespine stickleback, Gasterosteus aculeatus, representing two ecotypes (freshwater and ancestral saltwater). We exposed both ecotypes to abrupt native (control treatment) and non‐native salinities (0‰ and 30‰) and sampled gill tissue for transcriptomic analyses after 6 h of exposure. To investigate genomic responses to salinity, we analyzed four different comparisons; one for each ecotype (in their control and exposure salinity; (1) and (2), one between ecotypes in their control salinity (3), and the fourth comparison included all transcripts identified in (3) that did not show any expressional changes within ecotype in either the control or the exposed salinity (4)). Abrupt salinity transfer affected the expression of 10 and 1530 transcripts for the saltwater and freshwater ecotype, respectively, and 1314 were differentially expressed between the controls, including 502 that were not affected by salinity within ecotype (fixed expression). In total, these results indicate that factors other than genomic expressional plasticity are important for osmoregulation in stickleback, due to the need for opposite physiological pathways to survive the abrupt change in salinity.