Phenotypic divergence among threespine stickleback that differ in nuptial coloration

By studying systems in their earliest stages of differentiation, we can learn about the evolutionary forces acting within and among populations and how those forces could contribute to reproductive isolation. Such an understanding would help us to better discern and predict how selection leads to the maintenance of multiple morphs within a species, rather than speciation. The postglacial adaptive radiation of the threespine stickleback (Gasterosteus aculeatus) is one of the best‐studied cases of evolutionary diversification and rapid, repeated speciation. Following deglaciation, marine stickleback have continually invaded freshwater habitats across the northern hemisphere and established resident populations that diverged innumerable times from their oceanic ancestors. Independent freshwater colonization events have yielded broadly parallel patterns of morphological differences in freshwater and marine stickleback. However, there is also much phenotypic diversity within and among freshwater populations. We studied a lesser‐known freshwater “species pair” found in southwest Washington, where male stickleback in numerous locations have lost the ancestral red sexual signal and instead develop black nuptial coloration. We measured phenotypic variation in a suite of traits across sites where red and black stickleback do not overlap in distribution and at one site where they historically co‐occurred. We found substantial phenotypic divergence between red and black morphs in noncolor traits including shape and lateral plating, and additionally find evidence that supports the hypothesis of sensory drive as the mechanism responsible for the evolutionary switch in color from red to black. A newly described third “mixed” morph in Connor Creek, Washington, differs in head shape and size from the red and black morphs, and we suggest that their characteristics are most consistent with hybridization between anadromous and freshwater stickleback. These results lay the foundation for future investigation of the underlying genetic basis of this phenotypic divergence as well as the evolutionary processes that may drive, maintain, or limit divergence among morphs.     

Lateral plate number in low‐plated threespine stickleback: a study of plasticity and heritability

In the threespine stickleback Gasterosteus aculeatus model system, phenotypes are often classified into three morphs according to lateral plate number. Morph identity has been shown to be largely genetically determined, but substantial within‐morph variation in plate number exists. In this study, we test whether plate number has a plastic component in response to salinity in the low‐plated morph using a split‐clutch experiment where families were split in two, one half raised in water at 0 and the other at 30 ppt salt. We find a small salinity‐induced plastic effect on plate number in an unexpected direction, opposite to what we predicted: Fish raised in freshwater on average have slightly more plates than fish raised in saltwater. Our results confirm that heritability of plate number is high. Additionally, we find that variance in plate number at the family level can be predicted from other family level traits, which might indicate that epistatic interactions play a role in creating the observed pattern of lateral plate number variation.     

Genomic signatures of the plateless phenotype in the threespine stickleback

Understanding the genetic basis of traits involved in adaptive divergence and speciation is one of the most fundamental objectives in evolutionary biology. Toward that end, we look for signatures of extreme plate loss in the genome of freshwater threespine sticklebacks (Gasterosteus aculeatus). Plateless stickleback have been found in only a few lakes and streams across the world; they represent the far extreme of a phenotypic continuum (plate number) that has been studied for years, although plateless individuals have not yet been the subject of much investigation. We use a dense single nucleotide polymorphism dataset made using RADseq to study fish from three freshwater populations containing plateless and low plated individuals, as well as fish from full plated marine populations. Analyses were performed using FastStructure, sliding windows F_ST, Bayescan and latent factor mixed models to search for genomic differences between the low plated and plateless phenotypes both within and among the three lakes. At least 18 genomic regions which may contribute to within‐morph plate number variation were detected in our low plated stickleback populations. We see no evidence of a selective sweep between low and plateless fish; rather reduction of plate number within the low plated morph seems to be polygenic.     

Among‐lake reciprocal transplants induce convergent expression of immune genes in threespine stickleback

Geographic variation in parasite communities can drive evolutionary divergence in host immune genes. However, biotic and abiotic environmental variation can also induce plastic differences in immune function among populations. At present, there is little information concerning the relative magnitudes of heritable vs. induced immune divergence in natural populations. We examined immune gene expression profiles of threespine stickleback (Gasterosteus aculeatus) from six lakes on Vancouver Island, British Columbia. Parasite community composition differs between lake types (large or small, containing limnetic‐ or benthic‐like stickleback) and between watersheds. We observed corresponding differences in immune gene expression profiles among wild‐caught stickleback, using a set of seven immune genes representing distinct branches of the immune system. To evaluate the role of environmental effects on this differentiation, we experimentally transplanted wild‐caught fish into cages in their native lake, or into a nearby foreign lake. Transplanted individuals' immune gene expression converged on patterns typical of their destination lake, deviating from their native expression profile. Transplant individuals' source population had a much smaller effect, suggesting relatively weak genetic underpinning of population differences in immunity, as viewed through gene expression. This strong environmental regulation of immune gene expression provides a counterpoint to the large emerging literature documenting microevolution and genetic diversification of immune function. Our findings illustrate the value of studying immunity in natural environmental settings where the immune system has evolved and actively functions.     

Individuals' diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch)

Vertebrates' diets profoundly influence the composition of symbiotic gut microbial communities. Studies documenting diet‐microbiota associations typically focus on univariate or categorical diet variables. However, in nature individuals often consume diverse combinations of foods. If diet components act independently, each providing distinct microbial colonists or nutrients, we expect a positive relationship between diet diversity and microbial diversity. We tested this prediction within each of two fish species (stickleback and perch), in which individuals vary in their propensity to eat littoral or pelagic invertebrates or mixtures of both prey. Unexpectedly, in most cases individuals with more generalised diets had less diverse microbiota than dietary specialists, in both natural and laboratory populations. This negative association between diet diversity and microbial diversity was small but significant, and most apparent after accounting for complex interactions between sex, size and diet. Our results suggest that multiple diet components can interact non‐additively to influence gut microbial diversity.     

Admixture mapping of male nuptial colour and body shape in a recently formed hybrid population of threespine stickleback

Despite recent progress, we still know relatively little about the genetic architecture that underlies adaptation to divergent environments. Determining whether the genetic architecture of phenotypic adaptation follows any predictable patterns requires data from a wide variety of species. However, in many organisms, genetic studies are hindered by the inability to perform genetic crosses in the laboratory or by long generation times. Admixture mapping is an approach that circumvents these issues by taking advantage of hybridization that occurs between populations or species in the wild. Here, we demonstrate the utility of admixture mapping in a naturally occurring hybrid population of threespine sticklebacks (Gasterosteus aculeatus) from Enos Lake, British Columbia. Until recently, this lake contained two species of sticklebacks adapted to divergent habitats within the lake. This benthic–limnetic species pair diverged in a number of phenotypes, including male nuptial coloration and body shape, which were previously shown to contribute to reproductive isolation between them. However, recent ecological disturbance has contributed to extensive hybridization between the species, and there is now a single, admixed population within Enos Lake. We collected over 500 males from Enos Lake and found that most had intermediate nuptial colour and body shape. By genotyping males with nuptial colour at the two extremes of the phenotypic distribution, we identified seven genomic regions on three chromosomes associated with divergence in male nuptial colour. These genomic regions are also associated with variation in body shape, suggesting that tight linkage and/or pleiotropy facilitated adaptation to divergent environments in benthic–limnetic species pairs.     

An experimental test of the effect of predation upon behaviour and trait correlations in the threespine stickleback

Benthic and limnetic threespine stickleback (Gasterosteus aculeatus) are a classic example of ecological speciation. Behavioural and armour divergence between these species has been predicted to be the result of divergent selection driven in part by differential predation from cutthroat trout (Oncorhynchus clarki). To experimentally test this prediction, we reared split families of benthic–limnetic hybrids in the presence or absence of trout predation. Our results show that the presence of trout had little effect upon stickleback behaviour. We then compared performance in behavioural assays among stickleback that varied in armour to test if armour morphology correlates with behaviour. Our measurements revealed trait correlations between several behaviours and components of armour morphology. Trout predation did not result in an increased correlation between traits, therefore differential trout predation between benthics and limnetics is unlikely to be the cause of these correlations. The presence of trait correlations in advanced generation hybrids suggests that pleiotropy or linkage between genes underlying behaviour and armour morphology may be greater than previously appreciated.     

Nonlinear effects of temperature on body form and developmental canalization in the threespine stickleback

Theoretical models predict that nonlinear environmental effects on the phenotype also affect developmental canalization, which in turn can influence the tempo and course of organismal evolution. Here, we used an oceanic population of threespine stickleback (Gasterosteus aculeatus) to investigate temperature‐induced phenotypic plasticity of body size and shape using a paternal half‐sibling, split‐clutch experimental design and rearing offspring under three different temperature regimes (13, 17 and 21 °C). Body size and shape of 466 stickleback individuals were assessed by a set of 53 landmarks and analysed using geometric morphometric methods. At approximately 100 days, individuals differed significantly in both size and shape across the temperature groups. However, the temperature‐induced differences between 13 and 17 °C (mainly comprising relative head and eye size) deviated considerably from those between 17 and 21 °C (involving the relative size of the ectocoracoid, the operculum and the ventral process of the pelvic girdle). Body size was largest at 17 °C. For both size and shape, phenotypic variance was significantly smaller at 17 °C than at 13 and 21 °C, indicating that development is most stable at the intermediate temperature matching the conditions encountered in the wild. Higher additive genetic variance at 13 and 21 °C indicates that the plastic response to temperature had a heritable basis. Understanding nonlinear effects of temperature on development and the underlying genetics are important for modelling evolution and for predicting outcomes of global warming, which can lead not only to shifts in average morphology but also to destabilization of development.     

Adaptation and constraint in a stickleback radiation

The evolution of threespine sticklebacks in freshwater lakes constitutes a well‐studied example of a phenotypic radiation that has produced numerous instances of parallel evolution, but the exact selective agents that drive these changes are not yet fully understood. We present a comparative study across 74 freshwater populations of threespine stickleback in Norway to test whether evolutionary changes in stickleback morphology are consistent with adaptations to physical parameters such as lake depth, lake area, lake perimeter and shoreline complexity, variables thought to reflect different habitats and feeding niches. Only weak indications of adaptation were found. Instead, populations seem to have diversified in phenotypic directions consistent with allometric scaling relationships. This indicates that evolutionary constraints may have played a role in structuring phenotypic variation across freshwater populations of stickleback. We also tested whether the number of lateral plates evolved in response to lake calcium levels, but found no evidence for this hypothesis.     

Geographic and host‐mediated population genetic structure in a cestode parasite of the three‐spined stickleback

Comparative studies of genetic diversity and population structure can shed light on the ecological and evolutionary factors that influence host–parasite interactions. Here we examined whether geography, time and genetic variation in Alaskan three‐spined stickleback (Gasterosteus aculeatus Linneaus) hosts shape the population genetic structure of the diphyllobothridean cestode parasite Schistocephalus solidus (Müller, 1776). Host lineages and haplotypes were identified by sequencing the mitochondrial cytochrome b gene, and host population structure was assessed by Bayesian clustering analysis of allelic variation at 11 microsatellite loci. Parasite population structure was characterized according to allelic variation at eight microsatellite loci. Mantel tests and canonical redundancy analysis were conducted to evaluate the proportion of parasite genetic variation attributable to time and geography vs. host lineage, haplotype, and genotypic cluster. Host and parasite population structure were largely discordant across the study area, probably reflecting differences in gene flow, environmental influences external to the host, and genomic admixture among host lineages. We found that geography explained the greatest proportion of parasite genetic variation, but that variation also reflects time, host lineage, and host haplotype. Associations with host haplotypes suggest that one parasite genotypic cluster exhibits a narrower host range, predominantly infecting the most common host haplotypes, whereas the other parasite cluster infects all haplotypes equally, including rare haplotypes. Although experimental infection trials might prove otherwise, distributional differences in hosts preferentially infected by S. solidus could underlie the observed pattern of population structure.     

Structure and stability of genetic variance–covariance matrices: A Bayesian sparse factor analysis of transcriptional variation in the three‐spined stickleback

The genetic variance–covariance matrix ( G ) is a quantity of central importance in evolutionary biology due to its influence on the rate and direction of multivariate evolution. However, the predictive power of empirically estimated G ‐matrices is limited for two reasons. First, phenotypes are high‐dimensional, whereas traditional statistical methods are tuned to estimate and analyse low‐dimensional matrices. Second, the stability of G to environmental effects and over time remains poorly understood. Using Bayesian sparse factor analysis (BSFG) designed to estimate high‐dimensional G ‐matrices, we analysed levels variation and covariation in 10,527 expressed genes in a large (n = 563) half‐sib breeding design of three‐spined sticklebacks subject to two temperature treatments. We found significant differences in the structure of G between the treatments: heritabilities and evolvabilities were higher in the warm than in the low‐temperature treatment, suggesting more and faster opportunity to evolve in warm (stressful) conditions. Furthermore, comparison of G and its phenotypic equivalent P revealed the latter is a poor substitute of the former. Most strikingly, the results suggest that the expected impact of G on evolvability—as well as the similarity among G ‐matrices—may depend strongly on the number of traits included into analyses. In our results, the inclusion of only few traits in the analyses leads to underestimation in the differences between the G ‐matrices and their predicted impacts on evolution. While the results highlight the challenges involved in estimating G , they also illustrate that by enabling the estimation of large G ‐matrices, the BSFG method can improve predicted evolutionary responses to selection.     

Spatial heterogeneity in landscape structure influences dispersal and genetic structure: empirical evidence from a grasshopper in an agricultural landscape

Dispersal may be strongly influenced by landscape and habitat characteristics that could either enhance or restrict movements of organisms. Therefore, spatial heterogeneity in landscape structure could influence gene flow and the spatial structure of populations. In the past decades, agricultural intensification has led to the reduction in grassland surfaces, their fragmentation and intensification. As these changes are not homogeneously distributed in landscapes, they have resulted in spatial heterogeneity with generally less intensified hedged farmland areas remaining alongside streams and rivers. In this study, we assessed spatial pattern of abundance and population genetic structure of a flightless grasshopper species, Pezotettix giornae, based on the surveys of 363 grasslands in a 430‐km² agricultural landscape of western France. Data were analysed using geostatistics and landscape genetics based on microsatellites markers and computer simulations. Results suggested that small‐scale intense dispersal allows this species to survive in intensive agricultural landscapes. A complex spatial genetic structure related to landscape and habitat characteristics was also detected. Two P. giornae genetic clusters bisected by a linear hedged farmland were inferred from clustering analyses. This linear hedged farmland was characterized by high hedgerow and grassland density as well as higher grassland temporal stability that were suspected to slow down dispersal. Computer simulations demonstrated that a linear‐shaped landscape feature limiting dispersal could be detected as a barrier to gene flow and generate the observed genetic pattern. This study illustrates the relevance of using computer simulations to test hypotheses in landscape genetics studies.     

Ecosystem size matters: the dimensionality of intralacustrine diversification in Icelandic stickleback is predicted by lake size

Cases of evolutionary diversification can be characterized along a continuum from weak to strong genetic and phenotypic differentiation. Several factors may facilitate or constrain the differentiation process. Comparative analyses of replicates of the same taxon at different stages of differentiation can be useful to identify these factors. We estimated the number of distinct phenotypic groups in three‐spine stickleback populations from nine lakes in Iceland and in one marine population. Using the inferred number of phenotypic groups in each lake, genetic divergence from the marine population, and physical lake and landscape variables, we tested whether ecosystem size, approximated by lake size and depth, or isolation from the ancestral marine gene pool predicts the occurrence and the extent of phenotypic and genetic diversification within lakes. We find intralacustrine phenotypic diversification to be the rule rather than the exception, occurring in all but the youngest lake population and being manifest in ecologically important phenotypic traits. Neutral genetic data further indicate nonrandom mating in four of nine studied lakes, and restricted gene flow between sympatric phenotypic groups in two. Although neither the phenotypic variation nor the number of intralacustrine phenotypic groups was associated with any of our environmental variables, the number of phenotypic traits that were differentiated was significantly positively related to lake size, and evidence for restricted gene flow between sympatric phenotypic groups was only found in the largest lakes where trait specific phenotypic differentiation was highest.     

Shoal choice and ultraviolet reflections in stickleback populations from different photic habitats

Grouping is a widespread phenomenon in the animal kingdom and the decision to join a group is a function of individual and environmental conditions, meaning that any advantages and disadvantages have to be pondered constantly. Shoaling decisions in fishes are communicated via a variety of factors, such as colour signals, amongst other ultraviolet (UV) signals. The sensitivity for ultraviolet signals is assumed to be costly and a function of the predominant ecological conditions. The island of North Uist, Scotland, comprises bodies of water that possess great variation in their spectral distribution, especially in the UV spectral range. We examined different populations of three‐spined stickleback (Gasterosteus aculeatus L.), which is known to use UV for visual tasks, consisting of three populations from tea‐stained lakes and four from clear‐water lakes, concerning their preferences to join a shoal viewed under UV‐present and UV‐absent conditions. Nonreproductively active sticklebacks from tea‐stained lakes significantly preferred the shoal under UV‐absent conditions, whereas sticklebacks from clear‐water lakes did not show a significant preference. Reflection measurements showed that the UV chroma (intensity) of sticklebacks from tea‐stained lakes was higher than that of sticklebacks from clear‐water, most likely contrasting maximally against the UV‐poor background or compensating for a stronger attenuation of the signal.     

Local adaptation to salinity in the three‐spined stickleback?

Different lines of evidence suggest that the occurrence and extent of local adaptation in high gene flow marine environments – even in mobile and long‐lived vertebrates with complex life cycles – may be more widespread than earlier thought. We conducted a common garden experiment to test for local adaptation to salinity in Baltic Sea sticklebacks (Gasterosteus aculeatus). Fish from three different native salinity regimes (high, mid and low) were subjected to three salinity treatments (high, mid and low) in a full‐factorial experimental design. Irrespective of their origin, fish subjected to low (and mid) salinity treatments exhibited higher juvenile survival, grew to largest sizes and were in better condition than fish subjected to the high salinity treatment. However, a significant interaction between native and treatment salinities – resulting mainly from the poor performance of fish native to low salinity in the high salinity treatment – provided clear cut evidence for adaptation to local variation in salinity. Additional support for this inference was provided by the fact that the results concur with an earlier demonstration of significant differentiation in a number of genes with osmoregulatory functions across the same populations and that the population‐specific responses to salinity treatments exceeded that to be expected by random genetic drift.     

Widespread positive but weak assortative mating by diet within stickleback populations

Assortative mating – correlation between male and female traits – is common within populations and has the potential to promote genetic diversity and in some cases speciation. Despite its importance, few studies have sought to explain variation in the extent of assortativeness across populations. Here, we measure assortative mating based on an ecologically important trait, diet as inferred from stable isotopes, in 16 unmanipulated lake populations of three‐spine stickleback. As predicted, we find a tendency toward positive assortment on the littoral–pelagic axis, although the magnitude is consistently weak. These populations vary relatively little in the strength of assortativeness, and what variation occurs is not explained by hypothesized drivers including habitat cosegregation, the potential for disruptive selection, costs to choosiness, and the strength of the relationship between diet and body size. Our results support recent findings that most assortative mating is positive, while suggesting that new approaches may be required to identify the environmental variables that drive the evolution of nonrandom mating within populations.     

Glacial refuges for three‐spined stickleback in the Iberian Peninsula: mitochondrial DNA phylogeography

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Fitness differences between parapatric lake and stream stickleback revealed by a field transplant

Molecular comparisons of populations diverging into ecologically different environments often reveal strong differentiation in localized genomic regions, with the remainder of the genome being weakly differentiated. This pattern of heterogeneous genomic divergence, however, is rarely connected to direct measurements of fitness differences among populations. We here do so by performing a field enclosure experiment in threespine stickleback fish residing in a lake and in three replicate adjoining streams, and displaying weak yet heterogeneous genomic divergence between these habitats. Tracking survival over 29 weeks, we consistently find that lake genotypes transplanted into the streams suffer greatly reduced viability relative to local stream genotypes and that the performance of F1 hybrid genotypes is intermediate. This observed selection against migrants and hybrids combines to a total reduction in gene flow from the lake into streams of around 80%. Overall, our study identifies a strong reproductive barrier between parapatric stickleback populations, and cautions against inferring weak fitness differences between populations exhibiting weak overall genomic differentiation.     

Cryptic genetic variation and body size evolution in threespine stickleback

The role of environment as a selective agent is well-established. Environment might also influence evolution by altering the expression of genetic variation associated with phenotypes under selection. Far less is known about this phenomenon, particularly its contribution to evolution in novel environments. We investigated how environment affected the evolvability of body size in the threespine stickleback (Gasterosteus aculeatus). Gasterosteus aculeatus is well suited to addressing this question due to the rapid evolution of smaller size in the numerous freshwater populations established following the colonization of new freshwater habitats by an oceanic ancestor. The repeated, rapid evolution of size following colonization contrasts with the general observation of low phenotypic variation in oceanic stickleback. We reared an oceanic population of stickleback under high and low salinity conditions, mimicking a key component of the ancestral environment, and freshwater colonization, respectively. There was low genetic variation for body size under high salinity, but this variance increased significantly when fish were reared under low salinity. We therefore conclude that oceanic populations harbor the standing genetic variation necessary for the evolution of body size, but that this variation only becomes available to selection upon colonization of a new habitat.