Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations.
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ABSTRACT:
SUBMITTER: Cresko WA
PROVIDER: S-EPMC395921 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Changing environments, whether through natural or anthropogenic causes, can lead to the loss of some selective pressures ('relaxed selection') and possibly even the reinstatement of selective agents not encountered for many generations ('reversed selection'). We examined the outcome of relaxed and reversed selection in the adaptive radiation of the threespine stickleback fish, Gasterostues aculeatus L., in which isolated populations encounter a variety of predation regimes. Oceanic stickleback, which represent the ancestral founders of the freshwater radiation, encounter many piscivorous fish. Derived, freshwater populations, on the other hand, vary with respect to the presence of predators. Some populations encounter native salmonids, whereas others have not experienced predation by large fish in thousands of generations (relax-selected populations). Some relax-selected populations have had sport fish, including rainbow trout, Oncorhynchus mykiss, introduced within the past several decades (reverse-selected). We examined the behavioural responses of stickleback from three populations of each type to simulated attacks by trout and birds to determine whether relaxed and reversed selection has led to divergence in behaviour, and whether this divergence was predator specific. Fish from trout-free populations showed weak responses to trout, as predicted, but these responses were similar to those of oceanic (ancestral) populations. Fish from populations that co-occur with trout, whether native or introduced, showed elevated antipredator responses, indicating that in freshwater, trout predation selects for enhanced antipredator responses, which can evolve extremely rapidly. Comparison of laboratory-reared and wild-caught individuals suggests a combination of learned and genetic components to this variation. Responses to a model bird flyover were weakly linked to predation environment, indicating that the loss of predation by trout may partially influence the evolution of responses to birds. Our results reject the hypothesis that the consistent presence of predatory birds has been sufficient to maintain responses to piscivorous fish under periods of relaxed selection.
| S-EPMC4528399 | biostudies-literature
Project description:Individuals can reduce sampling costs and increase foraging efficiency by using information provided by others. One simple form of social information use is delayed local enhancement or increased interest in a location because of the past presence of others. We tested for delayed local enhancement in two ecomorphs of stickleback fish, benthic and limnetic, from three different lakes with putative independent evolutionary origins. Two of these lakes have reproductively isolated ecomorphs (species-pairs), whereas in the third, a previously intact species-pair recently collapsed into a hybrid swarm. Benthic fish in both intact species-pair lakes were more likely to exhibit delayed local enhancement despite being more solitary than limnetic fish. Their behaviour and morphology suggest their current perceived risk and past evolutionary pressure from predation did not drive this difference. In the hybrid swarm lake, we found a reversal in patterns of social information use, with limnetic-looking fish showing delayed local enhancement rather than benthic-looking fish. Together, our results strongly support parallel differentiation of social learning differences in recently evolved fish species, although hybridization can apparently erode and possibly even reverse these differences.
| S-EPMC10368488 | biostudies-literature
Project description:Adaptation of threespine stickleback to freshwater involves parallel recruitment of freshwater alleles in clusters of closely linked sites, or divergence islands (DIs). However, it remains unclear to what extent the DIs and the alleles that constitute them coincide between populations that underwent adaptation to freshwater independently. We examine threespine sticklebacks from ten freshwater lakes that emerged 500-1500 years ago in the White Sea basin, with the emphasis on repeatability of genomic patterns of adaptation among the lake populations and the role of local recombination rate in the distribution and structure of DIs. The 65 detected DIs are clustered in the genome, forming 12 aggregations, and this clustering cannot be explained by the variation of the recombination rate. Only 21 of the DIs are present in all the freshwater populations, likely being indispensable for successful colonization of freshwater environment by the ancestral marine population. Within most DIs, the same set of single nucleotide polymorphisms (SNPs) distinguish marine and freshwater haplotypes in all the lake populations; however, in some DIs, freshwater alleles differ between populations, suggesting that they could have been established by recruitment of different haplotypes in different populations.
| S-EPMC6761963 | biostudies-literature
Project description:Species such as threespine stickleback (Gasterosteus aculeatus) that inhabit divergent selective environments and that have diversified on different time scales can be of value for understanding evolutionary processes. Here we synthesize high-resolution genotypic and phenotypic data to explore a largely unstudied distribution of threespine stickleback populations living in oceanic and freshwater habitats along coastal and inland regions of Oregon. Many inland aquatic habitats of Oregon remained unglaciated during the last ice age, meaning that some extant Oregon lake and river stickleback may have descended from freshwater populations established long before more well-studied, post-glacial freshwater populations. To address the degree of congruence between genetic and phenotypic divergence, we directly compared Oregon stickleback to much younger (post-glacial) Alaskan populations. We found phenotypic variation in Oregon stickleback to be primarily partitioned between oceanic and freshwater habitats, as has been documented in other stickleback systems. However, the main axis of genetic divergence was between coastal and inland regions regardless of habitat type. Furthermore, when comparing patterns between Oregon and Alaska we found similar levels of phenotypic divergence, but much greater genetic divergence among Oregon's populations. The Oregon stickleback system therefore appears well suited for future studies linking genotypic and phenotypic change, further extending the utility of this small fish to provide general insights into evolutionary processes.
| S-EPMC9957565 | biostudies-literature
Project description:How many genetic changes control the evolution of new traits in natural populations? Are the same genetic changes seen in cases of parallel evolution? Despite long-standing interest in these questions, they have been difficult to address, particularly in vertebrates. We have analyzed the genetic basis of natural variation in three different aspects of the skeletal armor of threespine sticklebacks (Gasterosteus aculeatus): the pattern, number, and size of the bony lateral plates. A few chromosomal regions can account for variation in all three aspects of the lateral plates, with one major locus contributing to most of the variation in lateral plate pattern and number. Genetic mapping and allelic complementation experiments show that the same major locus is responsible for the parallel evolution of armor plate reduction in two widely separated populations. These results suggest that a small number of genetic changes can produce major skeletal alterations in natural populations and that the same major locus is used repeatedly when similar traits evolve in different locations.
| S-EPMC385219 | biostudies-literature
Project description:Sexual dimorphism (SD) in morphological, behavioural and physiological features is common, but the genetics of SD in the wild has seldom been studied in detail. We investigated the genetic basis of SD in morphological traits of threespine stickleback (Gasterosteus aculeatus) by conducting a large breeding experiment with fish from an ancestral marine population that acts as a source of morphological variation. We also examined the patterns of SD in a set of 38 wild populations from different habitats to investigate the relationship between the genetic architecture of SD of the marine ancestral population in relation to variation within and among natural populations. The results show that genetic architecture in terms of heritabilities, additive genetic variances and covariances (as well as correlations) is very similar in the two sexes in spite of the fact that many of the traits express significant SD. Furthermore, population differences in threespine stickleback body shape and armour SD appear to have evolved despite constraints imposed by genetic architecture. This implies that constraints for the evolution of SD imposed by strong genetic correlations are not as severe and absolute as commonly thought.
| S-EPMC3183875 | biostudies-other
Project description:Adaptation is driven by natural selection; however, many adaptations are caused by weak selection acting over large timescales, complicating its study. Therefore, it is rarely possible to study selection comprehensively in natural environments. The threespine stickleback (Gasterosteus aculeatus) is a well-studied model organism with a short generation time, small genome size, and many genetic and genomic tools available. Within this originally marine species, populations have recurrently adapted to freshwater all over its range. This evolution involved extensive parallelism: pre-existing alleles that adapt sticklebacks to freshwater habitats, but are also present at low frequencies in marine populations, have been recruited repeatedly. While a number of genomic regions responsible for this adaptation have been identified, the details of selection remain poorly understood. Using whole-genome resequencing, we compare pooled genomic samples from marine and freshwater populations of the White Sea basin, and identify 19 short genomic regions that are highly divergent between them, including three known inversions. 17 of these regions overlap protein-coding genes, including a number of genes with predicted functions that are relevant for adaptation to the freshwater environment. We then analyze four additional independently derived young freshwater populations of known ages, two natural and two artificially established, and use the observed shifts of allelic frequencies to estimate the strength of positive selection. Adaptation turns out to be quite rapid, indicating strong selection acting simultaneously at multiple regions of the genome, with selection coefficients of up to 0.27. High divergence between marine and freshwater genotypes, lack of reduction in polymorphism in regions responsible for adaptation, and high frequencies of freshwater alleles observed even in young freshwater populations are all consistent with rapid assembly of G. aculeatus freshwater genotypes from pre-existing genomic regions of adaptive variation, with strong selection that favors this assembly acting simultaneously at multiple loci.
| S-EPMC4191950 | biostudies-literature
Project description:Colonization of new habitats often reduces population sizes and may result in the accumulation of deleterious mutations by genetic drift. Compared with the genomic basis for adaptation to new environments, genome-wide analysis of deleterious mutations in isolated populations remains limited. In the present study, we investigated the accumulation of deleterious mutations in five endangered freshwater populations of threespine stickleback (Gasterosteus aculeatus) in the central part of the mainland of Japan. Using whole-genome resequencing data, we first conducted phylogenomic analysis and confirmed at least two independent freshwater colonization events in the central mainland from ancestral marine ecotypes. Next, analyses of single nucleotide polymorphisms showed a substantial reduction of heterozygosity in freshwater populations compared with marine populations. Reduction in heterozygosity was more apparent at the center of each chromosome than the peripheries and on X chromosomes compared with autosomes. Third, bioinformatic analysis of deleterious mutations showed increased accumulation of putatively deleterious mutations in the landlocked freshwater populations compared with marine populations. For the majority of populations examined, the frequencies of putatively deleterious mutations were higher on X chromosomes than on autosomes. The interpopulation comparison indicated that the majority of putatively deleterious mutations may have accumulated independently. Thus, whole-genome resequencing of endangered populations can help to estimate the accumulation of deleterious mutations and inform us of which populations are the most severely endangered. Furthermore, analysis of variation among chromosomes can give insights into whether any particular chromosomes are likely to accumulate deleterious mutations.
| S-EPMC7197494 | biostudies-literature
Project description:The lateral line is a mechanoreceptive sensory system that allows fish to sense objects and motion in their local environment. Variation in lateral line morphology may allow fish in different habitats to differentially sense and respond to salient cues. Threespine sticklebacks (Gasterosteus aculeatus) occupy a diverse range of aquatic habitats; we therefore hypothesized that populations within the G. aculeatus species complex might show variation in the morphology of the lateral line sensory system. We sampled 16 threespine stickleback populations from marine, stream and lake (including benthic and limnetic) habitats and examined the distribution, type and number of neuromasts on different regions of the body. We found that the threespine stickleback has a reduced lateral line canal system, completely lacking canal neuromasts. Although the arrangement of lines of superficial neuromasts on the body was largely the same in all populations, the number of neuromasts within these lines varied across individuals, populations and habitats. In pairwise comparisons between threespine sticklebacks adapted to divergent habitats, we found significant differences in neuromast number. Stream residents had more neuromasts than marine sticklebacks living downstream in the same watershed. In two independent lakes, benthic sticklebacks had more trunk neuromasts than sympatric limnetic sticklebacks, providing evidence for parallel evolution of the lateral line system. Our data provide the first demonstration that the lateral line sensory system can vary significantly between individuals and among populations within a single species, and suggest that this sensory system may experience different selection regimes in alternative habitats.
| S-EPMC2792588 | biostudies-literature
Project description:How predictable is the genetic basis of phenotypic adaptation? Answering this question begins by estimating the repeatability of adaptation at the genetic level. Here, we provide a comprehensive estimate of the repeatability of the genetic basis of adaptive phenotypic evolution in a natural system. We used quantitative trait locus (QTL) mapping to discover genomic regions controlling a large number of morphological traits that have diverged in parallel between pairs of threespine stickleback (Gasterosteus aculeatus species complex) in Paxton and Priest lakes, British Columbia. We found that nearly half of QTL affected the same traits in the same direction in both species pairs. Another 40% influenced a parallel phenotypic trait in one lake but not the other. The remaining 10% of QTL had phenotypic effects in opposite directions in the two species pairs. Similarity in the proportional contributions of all QTL to parallel trait differences was about 0.4. Surprisingly, QTL reuse was unrelated to phenotypic effect size. Our results indicate that repeated use of the same genomic regions is a pervasive feature of parallel phenotypic adaptation, at least in sticklebacks. Identifying the causes of this pattern would aid prediction of the genetic basis of phenotypic evolution.
| S-EPMC4649644 | biostudies-literature