Populations Of Threespine Stickleback Research Articles

Genetic mapping of natural variation in schooling tendency in the threespine stickleback.

Although there is a heritable basis for many animal behaviors, the genetic architecture of behavioral variation in natural populations remains mostly unknown, particularly in vertebrates. We sought to identify the genetic basis for social affiliation in two populations of threespine sticklebacks (Gasterosteus aculeatus) that differ in their propensity to school. Marine sticklebacks from Japan school strongly whereas benthic sticklebacks from a lake in Canada are more solitary. Here, we expanded on our previous efforts to identify quantitative trait loci (QTL) for differences in schooling tendency. We tested fish multiple times in two assays that test different aspects of schooling tendency: 1) the model school assay, which presents fish with a school of eight model sticklebacks; and 2) the choice assay, in which fish are given a choice between the model school and a stationary artificial plant. We found low-to-moderate levels of repeatability, ranging from 0.1 to 0.5, in schooling phenotypes. To identify the genomic regions that contribute to differences in schooling tendency, we used QTL mapping in two types of crosses: benthic × marine backcrosses and an F2 intercross. We found two QTL for time spent with the school in the model school assay, and one QTL for number of approaches to the school in the choice assay. These QTL were on three different linkage groups, not previously linked to behavioral differences in sticklebacks. Our results highlight the importance of using multiple crosses and robust behavioral assays to uncover the genetic basis of behavioral variation in natural populations.

Population structure and effective/census population size ratio in threatened three-spined stickleback populations from an isolated river basin in northwest Spain.

Variability at 20 microsatellite loci was examined to assess the population genetic structure, gene flow, and effective population size (N(e)) in three populations of three-spined stickleback (Gasterosteus aculeatus) from the upper basin of the Miño River in Galicia, NW Spain, where this species is threatened. The three populations showed similar levels of genetic diversity. There is a significant genetic differentiation between the three populations, but also significant gene flow. N(e) estimates based on linkage disequilibrium yielded values of 355 for the Miño River population and 241 and 311 for the Rato and Guisande Rivers, respectively, although we expect that these are overestimates. N(e) estimates based on temporal methods, considering gene flow or not, for the tributaries yielded values of 30-56 and 47-56 for the Rato and Guisande Rivers, respectively. Estimated census size (N(c)) for the Rato River was 880 individuals. This yielded a N(e)/N(c) estimate of 3-6 % for temporal estimation of N(e), which is within the empirical range observed in freshwater fishes. We suggest that the three populations analyzed have a sufficient level of genetic diversity with some genetic structure. Additionally, the absence of physical barriers suggests that conservation efforts and monitoring should focus in the whole basin as a unit.

Temporal stability of genetic variability and differentiation in the three-spined stickleback (Gasterosteus aculeatus).

Temporal variation in allele frequencies, whether caused by deterministic or stochastic forces, can inform us about interesting demographic and evolutionary phenomena occurring in wild populations. In spite of the continued surge of interest in the genetics of three-spined stickleback (Gasterosteus aculeatus) populations, little attention has been paid towards the temporal stability of allele frequency distributions, and whether there are consistent differences in effective size (Ne) of local populations. We investigated temporal stability of genetic variability and differentiation in 15 microsatellite loci within and among eight collection sites of varying habitat type, surveyed twice over a six-year time period. In addition, Nes were estimated with the expectation that they would be lowest in isolated ponds, intermediate in larger lakes and largest in open marine sites. In spite of the marked differences in genetic variability and differentiation among the study sites, the temporal differences in allele frequencies, as well as measures of genetic diversity and differentiation, were negligible. Accordingly, the Ne estimates were temporally stable, but tended to be lower in ponds than in lake or marine habitats. Hence, we conclude that allele frequencies in putatively neutral markers in three-spined sticklebacks seem to be temporally stable – at least over periods of few generations – across a wide range of habitat types differing markedly in levels of genetic variability, effective population size and gene flow.

Conspicuous female ornamentation and tests of male mate preference in threespine sticklebacks (Gasterosteus aculeatus).

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

Population genomic evidence for adaptive differentiation in Baltic Sea three-spined sticklebacks.

BackgroundThe degree of genetic differentiation among populations experiencing high levels of gene flow is expected to be low for neutral genomic sites, but substantial divergence can occur in sites subject to directional selection. Studies of highly mobile marine fish populations provide an opportunity to investigate this kind of heterogeneous genomic differentiation, but most studies to this effect have focused on a relatively low number of genetic markers and/or few populations. Hence, the patterns and extent of genomic divergence in high-gene-flow marine fish populations remain poorly understood.ResultsWe here investigated genome-wide patterns of genetic variability and differentiation in ten marine populations of three-spined stickleback (Gasterosteus aculeatus) distributed across a steep salinity and temperature gradient in the Baltic Sea, by utilizing >30,000 single nucleotide polymorphisms obtained with a pooled RAD-seq approach. We found that genetic diversity and differentiation varied widely across the genome, and identified numerous fairly narrow genomic regions exhibiting signatures of both divergent and balancing selection. Evidence was uncovered for substantial genetic differentiation associated with both salinity and temperature gradients, and many candidate genes associated with local adaptation in the Baltic Sea were identified.ConclusionsThe patterns of genetic diversity and differentiation, as well as candidate genes associated with adaptation, in Baltic Sea sticklebacks were similar to those observed in earlier comparisons between marine and freshwater populations, suggesting that similar processes may be driving adaptation to brackish and freshwater environments. Taken together, our results provide strong evidence for heterogenic genomic divergence driven by local adaptation in the face of gene flow along an environmental gradient in the post-glacially formed Baltic Sea.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0130-8) contains supplementary material, which is available to authorized users.

Toward the genetic origins of a potentially non-native population of threespine stickleback (Gasterosteus aculeatus) in Alberta

Disentangling the origin of putatively introduced/invasive species is of increasing priority in conservation biology. The presence of a previously undocumented species may be due to an undetected recent population or range expansion associated with environmental change, or due to an introduction by humans. We used molecular tools to address the origin of a population of threespine stickleback (Gasterosteus aculeatus) first identified in central Alberta, Canada in 1980 from a single lake. We characterized this inland, high elevation Alberta population in comparison to samples from five representative geographic regions worldwide, using mtDNA and nine microsatellite loci to elucidate genetic structure and estimate divergence times. We found significantly lower levels of genetic variation in the Alberta population, which could reflect either a recent colonization or periodic bottlenecks associated with winterkills. While we did find that the Alberta samples were most closely related to the North American West Coast populations, we did not uncover a putative source population. Alberta samples formed a clade in phylogenetic analyses, with divergence time estimates between the Alberta and British Columbia samples ca. 250–750 kya. The hypothesis that the Alberta population represents a natural colonization during North America’s last glacial recession could not be rejected. Collectively, these data suggest that the genetic signature of colonizing populations following introductions may be similar to populations at their range limit, contributing to difficulties establishing population origins.

Does predation drive morphological differentiation among Adriatic populations of the three-spined stickleback?

Morphometric differentiation among freshwater fish populations is a commonplace occurrence, although the underlying causes for this divergence often remain elusive. We analysed the degree and patterns of morphological differentiation among nine freshwater three-spined stickleback (Gasterosteus aculeatus) populations inhabiting isolated karst rivers of the Adriatic Sea basin, to characterise the phenotypic diversity and differentiation in these populations. The analyses revealed marked and significant morphometric differentiation – especially in traits related to predator defence amongst most populations – even among those located within close geographic proximity in the same catchment system. Accordingly, the degree of morphometric and neutral genetic differentiation, as assessed from variability in 15 microsatellite loci from a parallel study, were uncorrelated across the populations. However, PST/FST comparisons revealed that the degree of phenotypic differentiation (PST) among populations exceeded that to be expected from genetic drift alone, suggesting a possible adaptive basis for the observed differentiation. In fact, avian predation pressure and several physiochemical environmental variables were identified as the main putative drivers of the observed differentiation, particularly in the dorsal spines, ascending process and lateral plates. Hence, the high degree of morphometric differentiation among Adriatic three-spined stickleback populations appears to reflect adaptation to local ecological conditions.

Habitat-dependent olfactory discrimination in three-spined sticklebacks (Gasterosteus aculeatus).

The ability to recognize conspecifics is indispensible for differential treatment of particular individuals in social contexts like grouping behavior. The advantages of grouping are multifarious, and there exist numerous additional benefits of joining aggregations of conspecifics. Recognition is based on different signals and transmitted via multiple channels, among others the olfactory channel. The sensory system or the combination of sensory modalities used in recognition processes is highly dependent on the availability and effectiveness of modalities, which are a function of the environmental conditions. Using F1-generations of six three-spined stickleback (Gasterosteus aculeatus) populations from two habitat types (tea-stained and clear-water lakes) from the Outer Hebrides, Scotland, we investigated whether individuals are able to recognize members of their own population solely based on olfactory cues and whether the habitat type an individual originated from had an influence on its recognition abilities. When given the choice (own vs. foreign population) sticklebacks from tea-stained lakes significantly preferred the odor of their own population, whereas fish from clear-water habitats did not show any preference. Moreover, fish from the two habitat types differed significantly in their recognition abilities, indicating that olfactory communication is better developed when visual signaling is disturbed. Thus, the observed odor preferences appear to be the consequence of different selective constraints and adaptations as a result of the differences in environmental conditions that have acted on the parental generations. These adaptations are likely genetically based as the differences are present in the F1-generation that had been reared under identical laboratory conditions.

Covarying variances: more morphologically variable populations also exhibit more diet variation.

Many ecologically generalized populations are composed of relatively specialized individuals that selectively consume a subset of their population's diet, a phenomenon known as 'individual specialization'. The Niche Variation Hypothesis posits that this individual specialization can arise during ecological release if niche expansion occurs mainly through diet divergence among individuals, leading to greater morphological variation. Most tests of this hypothesis have searched for correlations between niche width and morphological variance, but this approach rests on the untested assumption that within-population morphological diversity is highly correlated with ecological diversity. Here, we test whether intrapopulation diet variation is correlated with intrapopulation morphological variation, across 12 lacustrine populations of three-spine stickleback. First, we use behavioral observations, isotopes, and gut contents to show that, within populations, individuals differ in microhabitat use and diet. Second, we show that some populations exhibit more diet variation than others, as evidenced by differences in both isotopic and gut content variation among individuals. Finally, we confirm that populations with greater dietary variation are more morphologically variable. However, this relationship is only significant when total morphological variance is examined, not for individual morphological traits. This discordance may reflect among-population differences in the relationship between individual morphology and diet. Because morphology-diet relationships can differ among populations, morphological variance may be a poor predictor of actual diet variation when diverse populations are being compared.

Predictors of Individual Variation in Movement in a Natural Population of Threespine Stickleback (Gasterosteus aculeatus).

Species abundances and distributions are inherently tied to individuals' decisions about movement within their habitat. Therefore, integrating individual phenotypic variation within a larger ecological framework may provide better insight into how populations structure themselves. Recent evidence for consistent individual differences in behaviour prompts the hypothesis that variation in behavioural types might be related to variation in movement in natural environments. In a multiyear mark-recapture study, we found that individual sticklebacks exhibited consistent individual differences in behaviour both within a standardized testing arena designed to measure exploratory behaviour and within a river. Therefore, we asked whether individual differences in movement in a natural river were related to an individual's exploratory behavioural type. We also considered whether body condition and/or the individual's habitat or social environment use was related to movement. There was no evidence that an individual's exploratory behavioural type was related to movement within the river. Instead, an individual's habitat use and body condition interacted to influence natural movement patterns. Individuals in good condition were more likely to move further in the river, but only if they inhabited a vegetated complex part of the river; body condition had no influence on movement in those individuals inhabiting open areas of the river. Our results suggest that individual traits could help improve predictions about how populations may distribute themselves within patchy and complex environments.

Intrasexual competition and throat color evolution in female three-spined sticklebacks

Interest in the evolution of female ornaments has been growing but explaining their presence remains a challenge for many animal taxa. Although female ornaments may be sexually selected via male choice, they can also function in female–female competition. Here, we studied a stream-resident population of three-spined sticklebacks (Gasterosteus aculeatus), in which females possess male-typical red throat coloration, and a nearby anadromous population that lacks such coloration and is thought to possess ancestral character states for most traits in this species complex. We asked first whether there were population-level differences in agonism that might be associated with the evolution of female ornaments. We tested if the derived population possessing some red-throated females exhibited relatively higher levels and clearer patterns of within-population aggression and dominance in dyadic trials and more frequent behavioral dominance over individuals of the population lacking red females. Second, to address the relationship between the derived coloration and female–female competition, we tested whether red-throated stream females were more aggressive and dominant toward dull-throated stream females in both dyadic and socially complex contexts. We found that clear dominance was established more often in pairs of stream females, and stream females were more often dominant in stream-anadromous dyads. However, we found no clear evidence that the red throat coloration was directly linked to a female competitive advantage within the stream population, suggesting alternative untested signaling or perhaps nonadaptive functions. Our study represents the first evaluation of the potential relationship between a male-typical nuptial trait and intrasexual competition in female three-spined sticklebacks.

Human-induced eutrophication maintains high parasite prevalence in breeding threespine stickleback populations.

Anthropogenic activities are having profound impacts on species interactions, with further consequences for populations and communities. We investigated the influence that anthropogenic eutrophication has on the prevalence of the parasitic tapeworm Schistocephalus solidus in threespine stickleback Gasterosteus aculeatus populations. We caught stickleback from four areas along the coast of Finland, and within each area from one undisturbed and one eutrophied habitat. We found the prevalence of the parasite to be lower in the eutrophied habitats at the start of the breeding season, probably because of fewer piscivorous birds that transmit the parasite. However, while the prevalence of the parasite declined across the season in the undisturbed habitat, it did less so in eutrophied habitats. We discuss different processes that could be behind the differences, such as lower predation rate on infected fish, higher food availability and less dispersal in eutrophied habitats. We found no effect of eutrophication on the proportion of infected stickleback that entered reproductive condition. Together with earlier findings, this suggests that eutrophication increases the proportion of infected stickleback that reproduce. This could promote the evolution of less parasite resistant populations, with potential consequences for the viability of the interacting parties of the host-parasite system.

A low-density SNP array for analyzing differential selection in freshwater and marine populations of threespine stickleback (Gasterosteus aculeatus).

BackgroundThe threespine stickleback (Gasterosteus aculeatus) has become an important model species for studying both contemporary and parallel evolution. In particular, differential adaptation to freshwater and marine environments has led to high differentiation between freshwater and marine stickleback populations at the phenotypic trait of lateral plate morphology and the underlying candidate gene Ectodysplacin (EDA). Many studies have focused on this trait and candidate gene, although other genes involved in marine-freshwater adaptation may be equally important. In order to develop a resource for rapid and cost efficient analysis of genetic divergence between freshwater and marine sticklebacks, we generated a low-density SNP (Single Nucleotide Polymorphism) array encompassing markers of chromosome regions under putative directional selection, along with neutral markers for background.ResultsRAD (Restriction site Associated DNA) sequencing of sixty individuals representing two freshwater and one marine population led to the identification of 33,993 SNP markers. Ninety-six of these were chosen for the low-density SNP array, among which 70 represented SNPs under putatively directional selection in freshwater vs. marine environments, whereas 26 SNPs were assumed to be neutral. Annotation of these regions revealed several genes that are candidates for affecting stickleback phenotypic variation, some of which have been observed in previous studies whereas others are new.ConclusionsWe have developed a cost-efficient low-density SNP array that allows for rapid screening of polymorphisms in threespine stickleback. The array provides a valuable tool for analyzing adaptive divergence between freshwater and marine stickleback populations beyond the well-established candidate gene Ectodysplacin (EDA).Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-867) contains supplementary material, which is available to authorized users.

The role of calcium and predation on plate morph evolution in the three-spined stickleback (Gasterosteus aculeatus).

While the genetic basis to plate morph evolution of the three-spined stickleback (Gasterosteus aculeatus) is well described, the environmental variables that select for different plate and spine morphs are incompletely understood. Using replicate populations of three-spined sticklebacks on North Uist, Scotland, we previously investigated the role of predation pressure and calcium limitation on the adaptive evolution of stickleback morphology and behavior. While dissolved calcium proved a significant predictor of plate and spine morph, predator abundance did not. Ecol. Evol., xxx, 2014 and xxx performed a comparable analysis to our own to address the same question. They failed to detect a significant effect of dissolved calcium on morphological evolution, but did establish a significant effect of predation; albeit in the opposite direction to their prediction.

Tinkering with the axial skeleton: vertebral number variation in ecologically divergent threespine stickleback populations

Understanding how the vertebral column is impacted as populations adapt to different habitats favouring distinct body forms can provide insight into the origin of evolutionary diversity in the axial skeleton. We examined variation of vertebral number and body shape in morphologically and ecologically divergent anadromous, benthic, and limnetic threespine stickleback populations from Alaska. Variation in vertebral number was substantial and was associated with body shape variation. Both vertebral homeosis and region-specific changes in vertebral number were present. Sexual dimorphism in vertebral number was significant and resulted from vertebral homeosis; females had more abdominal vertebrae and males more caudal vertebrae, although total vertebrae did not differ. Body elongation was associated with an increase in vertebral number, especially in the caudal region, although this varied among populations. Benthics tended to have less caudal vertebrae than limnetics and anadromous stickleback generally had more abdominal vertebrae than either, although this also varied among populations. Variation among individuals indicated that external similarity in body form masks significant vertebral variation in stickleback. Although more research on the underlying mechanisms and functional significance is needed, our findings highlight the potential of the threespine stickleback as a model for studying the evolution of the vertebrate axial skeleton.

Reversed brain size sexual dimorphism accompanies loss of parental care in white sticklebacks.

Uncovering factors that shape variation in brain morphology remains a major challenge in evolutionary biology. Recently, it has been shown that brain size is positively associated with level of parental care behavior in various taxa. One explanation for this pattern is that the cognitive demands of performing complex parental care may require increased brain size. This idea is known as the parental brain hypothesis (PBH). We set out to test the predictions of this hypothesis in wild populations of threespine stickleback (Gasterosteus aculeatus). These fish are commonly known to exhibit (1) uniparental male care and (2) sexual dimorphism in brain size (males>females). To test the PBH, we took advantage of the existence of closely related populations of stickleback that display variation in parental care behavior: common marine threespine sticklebacks (uniparental male care) and white threespine sticklebacks (no care). To begin, we quantified genetic differentiation among two common populations and three white populations from Nova Scotia. We found overall low differentiation among populations, although FST was increased in between-type comparisons. We then measured the brain weights of males and females from all five populations along with two additional common populations from British Columbia. We found that sexual dimorphism in brain size is reversed in white stickleback populations: males have smaller brains than females. Thus, while several alternatives need to be ruled out, the PBH appears to be a reasonable explanation for sexual dimorphism in brain size in threespine sticklebacks.

Gene expression plasticity evolves in response to colonization of freshwater lakes in threespine stickleback.

Phenotypic plasticity is predicted to facilitate individual survival and/or evolve in response to novel environments. Plasticity that facilitates survival should both permit colonization and act as a buffer against further evolution, with contemporary and derived forms predicted to be similarly plastic for a suite of traits. On the other hand, given the importance of plasticity in maintaining internal homeostasis, derived populations that encounter greater environmental heterogeneity should evolve greater plasticity. We tested the evolutionary significance of phenotypic plasticity in coastal British Columbian postglacial populations of threespine stickleback (Gasterosteus aculeatus) that evolved under greater seasonal extremes in temperature after invading freshwater lakes from the sea. Two ancestral (contemporary marine) and two derived (contemporary freshwater) populations of stickleback were raised near their thermal tolerance extremes, 7 and 22 °C. Gene expression plasticity was estimated for more than 14,000 genes. Over five thousand genes were similarly plastic in marine and freshwater stickleback, but freshwater populations exhibited significantly more genes with plastic expression than marine populations. Furthermore, several of the loci shown to exhibit gene expression plasticity have been previously implicated in the adaptive evolution of freshwater populations, including a gene involved in mitochondrial regulation (PPARAa). Collectively, these data provide molecular evidence that highlights the importance of plasticity in colonization and adaptation to new environments.

Fecundity compensation and fecundity reduction among populations of the three-spined stickleback infected by Schistocephalus solidus in Alaska.

We surveyed nine populations of the three-spined stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus from south-central Alaska for two apparent forms of tolerance to infection in females capable of producing egg clutches notwithstanding large parasite burdens. Seven populations exhibited fecundity reduction, whereas two populations showed fecundity compensation. Our data suggest that fecundity reduction, a side effect resulting from nutrient theft, occurs in two phases of host response influenced by the parasite : host body mass (BM) ratio. The first is significantly reduced ovum mass without significant reduction in clutch size, and the second one involves significant reductions in both ovum mass and clutch size. Thus, ovum mass of host females who are functionally being starved through nutrient theft seems to be more readily influenced by parasitism and, therefore, decreased before clutch size is reduced. This inference is consistent with expectations based on the biology of and effect of feeding ration on reproduction in stickleback females. Fecundity compensation appears to be uncommon among populations of three-spined stickleback in Alaska and rare among populations throughout the northern hemisphere. Fecundity reduction seems to be common, at least among stickleback populations in Alaska.

Contrasting patterns of phenotype-dependent parasitism within and among populations of threespine stickleback.

Variation in infection rate arises from variation in host exposure and resistance to parasites both within and among populations. All things being equal, phenotypes that increase exposure risk should covary positively with infection among individuals. It might therefore be expected that populations with mean phenotypes that increase exposure might also have higher rates of infection. However, such positive covariance between exposure and infection at the population level might be undermined by other factors such as geographic variation in parasite abundance or host resistance, negating or reversing in between-population comparisons. We studied rates of infection of two parasites among 18 populations of threespine stickleback (Gasterosteus aculeatus). As predicted, within populations, trophic morphology covaries with infection of two trophically transmitted parasites: individuals with benthic (or limnetic) phenotypes were more likely to be infected with a benthic (or limnetic) parasite. However, across populations, the relationship between morphology and infection rate was absent (limnetic parasite) or reversed (benthic parasite). Our results confirm the importance of phenotype-dependent exposure, but stress different factors or processes, such as the evolution of reduced susceptibility, might shape variation in infection at larger spatial scales.

The genomic signature of parallel adaptation from shared genetic variation

Parallel adaptation is common and may often occur from shared genetic variation, but the genomic consequences of this process remain poorly understood. We first use individual-based simulations to demonstrate that comparisons between populations adapted in parallel to similar environments from shared variation reveal a characteristic genomic signature around a selected locus: a low-divergence valley centred at the locus and flanked by twin peaks of high divergence. This signature is initiated by the hitchhiking of haplotype tracts differing between derived populations in the broader neighbourhood of the selected locus (driving the high-divergence twin peaks) and shared haplotype tracts in the tight neighbourhood of the locus (driving the low-divergence valley). This initial hitchhiking signature is reinforced over time because the selected locus acts as a barrier to gene flow from the source to the derived populations, thus promoting divergence by drift in its close neighbourhood. We next empirically confirm the peak-valley-peak signature by combining targeted and RAD sequence data at three candidate adaptation genes in multiple marine (source) and freshwater (derived) populations of threespine stickleback. Finally, we use a genome-wide screen for the peak-valley-peak signature to discover additional genome regions involved in parallel marine-freshwater divergence. Our findings offer a new explanation for heterogeneous genomic divergence and thus challenge the standard view that peaks in population divergence harbour divergently selected loci and that low-divergence regions result from balancing selection or localized introgression. We anticipate that genome scans for peak-valley-peak divergence signatures will promote the discovery of adaptation genes in other organisms.