Parasite burdens differ between sympatric three-spined stickleback species

The ecological theory of adaptive radiation states that differences in ecological circumstances among local populations are the cause of divergence that leads to speciation. The role of parasites in contributing to divergence has seldom been considered, despite their ubiquity and known selective effects. The potential for parasites to contribute to divergence between closely related taxa was examined by quantifying the variation in parasite burdens between sympatric three-spined stickleback species ( Gasterosteus aculeatus complex) in two lakes in coastal British Columbia, Canada. In doing so the relative importance of geographical differences between lakes and trophic or microhabitat differences between species within lakes were evaluated. The entire metazoan parasite burdens of a total of 255 limnetic and benthic sticklebacks in Paxton and Priest lakes were assayed over five time points between spring and autumn. Despite their sympatric distributions, there were large differences in parasite burdens between benthic and limnetic sticklebacks within lakes and these were consistent across both lakes. In particular, limnetics suffered greater burdens of the parasites Schistocephalus solidus and Diplostomum scudderi and benthics had much higher burdens of parasitic glochidia (mollusc larvae). Parasite burdens also differed quantitatively between lakes, but in general such differences were less pronounced than those between the stickleback species. The documented differences in parasite burdens between stickleback species have potential to contribute to divergent selection on life history, immunological and secondary sexual characters that could contribute to reproductive isolation between the species.     

Evolutionary history of an adaptive radiation in species pairs of threespine sticklebacks (Gasterosteus): insights from mitochondrial DNA

Species pairs of threespine stickleback, Gasterosteus aculeatus, co-exist in several lakes in the Strait of Georgia, southwestern British Columbia. One species, ‘benthics’ is robust-bodied and is morphologically and behaviourally specialized for benthivory. The other species, ‘limnetics’ is specialized for planktivory in open-water habitats of the lakes. We examined mitochondrial DNA restriction site variation in benthic and limnetic sticklebacks as well as in solitary freshwater, anadromous (sea-run), and marine populations to test: (i) if benthic and limnetic pairs have evolved only once or multiple times (parallel evolution) and (ii) if the species have evolved sympatrically, or allopatrically from ‘double invasions’ of lakes by ancestral anadromous/marine sticklebacks. Stickleback mtDNA comprised a single clade with a low (mean = 0.40%) degree of sequence divergence among the 77 haplotypes resolved. Most nucleotide diversity (97%) was found within (rather than among) populations of anadromous/marine sticklebacks whereas most diversity (77%) was found among populations in freshwater sticklebacks. Significant differences in haplotype frequencies were found between benthics and limnetics in three of the four species pair lakes examined, but in all cases the pairs within lakes were characterized by unique assemblages of closely related haplotypes. Hierarchical clustering of divergence estimates suggested that comparable species from different lakes have originated independently in all lakes because in no case did comparable species from different lakes cluster together. Divergent species within lakes tended to be more closely related to one another than to species in other lakes and there were two cases were benthics and limnetics within a particular lake were monophyletic. In two of the four two-species lakes, limnetics were less divergent from putative ancestral anadromous/marine stickleback as predicted by the double invasion hypothesis, but in the two other lakes benthics were less divergent. Our data argue strongly that the species pairs have evolved independently in each lake were they now co-exist. Further, in two lakes our data are consistent with the species having evolved by sympatric divergence, but allopatric divergence followed by introgression of mtDNA that has obscured ancestral relationships cannot be discounted completely. Finally, despite remaining uncertainty about the geography of speciation, the species appear to have evolved in the face of gene flow arguing that natural selection acting on trophic ecology has been a major component of ecological speciation in sticklebacks.     

Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes

Speciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of ecological speciation has been accepted, its mechanisms and genetic bases are still under investigation. Here, we present a mechanism for speciation that is orchestrated and strengthened by parasite communities acting on polymorphic genes of the immune system. In vertebrates, these genes have a pleiotropic role with regard to parasite resistance and mate choice. In contrasting niches, parasite communities differ and thus the pools of alleles of the adapted major histocompatibility complex (MHC) also differ between niches. Mate choice for the best-adapted MHC genotype will favour local adaptations and will accelerate separation of both populations: thus immune genes act as pleiotropic speciation genes –'magic traits'. This mechanism should operate not only in sympatric populations but also under allopatry or parapatry. Each individual has a small subset of the many MHC alleles present in the population. If all individuals could have all MHC alleles from the pool, MHC-based adaptation is neither necessary nor possible. However, the typically small optimal individual number of MHC loci thus enables MHC-based speciation. Furthermore, we propose a new mechanism selecting against species hybrids. Hybrids are expected to have super-optimal individual MHC diversity and should therefore suffer more from parasites in all habitats.     

Impacts of trout predation on fitness of sympatric sticklebacks and their hybrids

Predation may be a significant factor in the divergence of sympatric species although its role has been largely overlooked. This study examines the consequences of predation on the fitness of a pair of lacustrine stickleback species (Gasterosteus aculeatus complex) and their F(1) hybrids. Benthic sticklebacks are found in the littoral zone of lakes associated with vegetation and bare sediments, whereas limnetic sticklebacks spend most of their lives in the pelagic zone. The cutthroat trout (Oncorhynchus clarki) is a major predator of sticklebacks and the only other fish species native to lakes containing both benthic and limnetic species. In pond experiments we found that the addition of these predators primarily impacted the survival of limnetics. By contrast, benthic survival was unaffected by trout addition. The result was that relative survival of benthics and limnetics was reversed in the presence of trout. The presence of trout had no effect on the rank order of parent species growth rates, with benthics always growing faster than limnetics. F(1) hybrids survived poorly relative to benthics and limnetics and their growth rates were intermediate regardless of treatment. The results implicate predation by trout in the divergence of the species but not through increased vulnerability of F(1) hybrids.     

Natural selection on MHC IIβ in parapatric lake and stream stickleback: Balancing,divergent, both or neither?

Major histocompatibility complex (MHC) genes encode proteins that play a central role in vertebrates' adaptive immunity to parasites. MHC loci are among the most polymorphic in vertebrates' genomes, inspiring many studies to identify evolutionary processes driving MHC polymorphism within populations and divergence between populations. Leading hypotheses include balancing selection favouring rare alleles within populations, and spatially divergent selection. These hypotheses do not always produce diagnosably distinct predictions, causing many studies of MHC to yield inconsistent or ambiguous results. We suggest a novel strategy to distinguish balancing vs. divergent selection on MHC, taking advantage of natural admixture between parapatric populations. With divergent selection, individuals with immigrant alleles will be more infected and less fit because they are susceptible to novel parasites in their new habitat. With balancing selection, individuals with locally rare immigrant alleles will be more fit (less infected). We tested these contrasting predictions using three‐spine stickleback from three replicate pairs of parapatric lake and stream habitats. We found numerous positive and negative associations between particular MHC IIβ alleles and particular parasite taxa. A few allele–parasite comparisons supported balancing selection, and others supported divergent selection between habitats. But, there was no overall tendency for fish with immigrant MHC alleles to be more or less heavily infected. Instead, locally rare MHC alleles (not necessarily immigrants) were associated with heavier infections. Our results illustrate the complex relationship between MHC IIβ allelic variation and spatially varying multispecies parasite communities: different hypotheses may be concurrently true for different allele–parasite combinations.     

ECOLOGICAL SPECIATION IN STICKLEBACKS: ENVIRONMENT-DEPENDENT HYBRID FITNESS

“Ecological” speciation occurs when reproductive isolation evolves as a consequence of divergent selection between populations exploiting different resources or environments. We tested this hypothesis of speciation in a young stickleback species pair by measuring the direct contribution of ecological selection pressures to hybrid fitness. The two species (limnetic and benthic) are strongly differentiated morphologically and ecologically, whereas hybrids are intermediate. Fitness of hybrids is high in the laboratory, especially F₁ and F₂ hybrids (backcrosses may show some breakdown). We transplanted F₁ hybrids to enclosures in the two main habitats in the wild to test whether the distribution of resources available in the environment generates a hybrid disadvantage not detectable in the laboratory. Hybrids grew more slowly than limnetics in the open water habitat and more slowly than benthics in the littoral zone. Growth of F₁ hybrids was inferior to the average of the parent species across both habitats, albeit not significantly. The contrast between laboratory and field results supports the hypothesis that mechanisms of F₁ hybrid fitness in the wild are primarily ecological and do not result from intrinsic genetic incompatibilities. Direct selection on hybrids contributes to the maintenance of sympatric stickleback species and may have played an important role in their origin.     

BODY SIZE,NATURAL SELECTION,AND SPECIATION IN STICKLEBACKS

There is little evidence from nature that divergent natural selection is crucial to speciation. However, divergent selection is implicated if traits conferring adaptation to alternative environments also form the basis of reproductive isolation. We tested the importance of body size differences to premating isolation between two sympatric sticklebacks. The species differ greatly in size, and several lines of evidence indicate that this difference is an adaptation to alternative foraging habitats. Strong assortative mating was evident in laboratory trials, but a few hybridization events occurred. Probability of interspecific mating was strongly correlated with body size: interspecific spawning occurred only between the largest individuals of the smaller species and the smallest individuals of the larger species. Probability of spawning between similar-sized individuals from different species was comparable to spawning rates within species. Disruption of mating between individuals from different species can be traced to increased levels of male aggression and decreased levels of male courtship as size differences increased between paired individuals. Interspecific mate preferences in sympatric sticklebacks appears to be dominated by body size, implicating natural selection in the origin of species.     

Shared evolutionary origin of major histocompatibility complex polymorphism in sympatric lemurs

Genes of the major histocompatibility complex (MHC) play a central role in adaptive immune responses of vertebrates. They exhibit remarkable polymorphism, often crossing species boundaries with similar alleles or allelic motifs shared across species. This pattern may reflect parallel parasite‐mediated selective pressures, either favouring the long maintenance of ancestral MHC allelic lineages across successive speciation events by balancing selection (“trans‐species polymorphism”), or alternatively favouring the independent emergence of functionally similar alleles post‐speciation via convergent evolution. Here, we investigate the origins of MHC similarity across several species of dwarf and mouse lemurs (Cheirogaleidae). We examined MHC class II variation in two highly polymorphic loci (DRB, DQB) and evaluated the overlap of gut–parasite communities in four sympatric lemurs. We tested for parasite‐MHC associations across species to determine whether similar parasite pressures may select for similar MHC alleles in different species. Next, we integrated our MHC data with those previously obtained from other Cheirogaleidae to investigate the relative contribution of convergent evolution and co‐ancestry to shared MHC polymorphism by contrasting patterns of codon usage at functional vs. neutral sites. Our results indicate that parasites shared across species may select for functionally similar MHC alleles, implying that the dynamics of MHC‐parasite co‐evolution should be envisaged at the community level. We further show that balancing selection maintaining trans‐species polymorphism, rather than convergent evolution, is the primary mechanism explaining shared MHC sequence motifs between species that diverged up to 30 million years ago.     

EVALUATING PATTERNS OF CONVERGENT EVOLUTION AND TRANS‐SPECIES POLYMORPHISM AT MHC IMMUNOGENES IN TWO SYMPATRIC STICKLEBACK SPECIES

The immunologically important major histocompatibility complex (MHC) harbors some of the most polymorphic genes in vertebrates. These genes presumably evolve under parasite‐mediated selection and frequently show inconsistent allelic genealogies, where some alleles are more similar between species than within species. This phenomenon is thought to arise either from convergent evolution under parallel selection or from the preservation of ancient allelic lineages beyond speciation events (trans‐species polymorphism, TSP). Here, we examine natural populations of two sympatric stickleback species (Gasterosteus aculeatus and Pungitius pungitius) to investigate the contribution of these two mechanisms to the evolution of inconsistent allelic genealogies at the MHC. Overlapping parasite taxa between the two host species in three different habitats suggest contemporary parallel selection on the MHC genes. Accordingly, we detected a lack of species‐specific phylogenetic clustering in the immunologically relevant antigen‐binding residues of the MHC IIB genes which contrasted with the rest of the coding and noncoding sequence. However, clustering was not habitat‐specific and a codon‐usage analysis revealed patterns of similarity by descent. In this light, common descent via TSP, in combination with intraspecies gene conversion, rather than convergent evolution is the more strongly supported scenario for the inconsistent genealogy at the MHC.     

REINFORCEMENT OF STICKLEBACK MATE PREFERENCES: SYMPATRY BREEDS CONTEMPT

Detailed studies of reproductive isolation and how it varies among populations can provide valuable insight into the mechanisms of speciation. Here we investigate how the strength of premating isolation varies between sympatric and allopatric populations of threespine sticklebacks to test a prediction of the hypothesis of reinforcement: that interspecific mate discrimination should be stronger in sympatry than in allopatry. In conducting such tests, it is important to control for ecological character displacement between sympatric species because ecological character divergence may strengthen prezygotic isolation as a by-product. We control for ecological character displacement by comparing mate preferences of females from a sympatric population (benthics) with mate preferences of females from two allopatric populations that most closely resemble the sympatric benthic females in ecology and morphology. No-choice mating trials indicate that sympatric benthic females mate less readily with heterospecific (limnetic) than conspecific (benthic) males, whereas two different populations of allopatric females resembling benthics show no such discrimination. These differences demonstrate reproductive character displacement of benthic female mate choice. Previous studies have established that hybridization between sympatric species occurred in the past in the wild and that hybrid offspring have lower fitness than either parental species, thus providing conditions under which natural selection would favor individuals that do not hybridize. Results are therefore consistent with the hypothesis that female mate preferences have evolved as a response to reduced hybrid fitness (reinforcement), although direct effects of sympatry or a biased extinction process could also produce the pattern. Males of the other sympatric species (limnetics) showed a preference for smaller females, in contrast to the inferred ancestral preference for larger females, suggesting reproductive character displacement of limnetic male mate preferences as well.     

Character shifts in the defensive armor of sympatric sticklebacks

Natural enemies may contribute to the morphological divergence of sympatric species, yet their role has received little attention to date. We tested for character shifts in defensive armor of sympatric threespine sticklebacks (Gasterosteus aculeatus complex) previously shown to exhibit ecological character displacement in traits related to resource use. We scored five defensive armor traits in sympatric benthic and limnetic stickleback species from southwestern British Columbia and compared them with the same traits in nearby allopatric populations in the presence of the same predatory fish (Oncorhynchus sp.). This approach is analogous to tests of ecological character displacement that compare trophic traits of sympatric and allopatric species in the presence of the same community of resource types. Three patterns consistent with character displacement in defensive armor were found. First, limnetics in different lakes had consistently more armor than sympatric benthics. Second, the average amount of armor, averaged over both species, was reduced in sympatry compared to allopatric populations. This reduction was almost entirely the result of shifts by benthic species, whereas armor in limnetics was more similar to that in allopatric populations. Third, differences between sympatric benthics and limnetics in total armor were greater than expected from comparisons with allopatric populations. We interpret these patterns as the result of differences in habitat-specific predation regimes accompanying ecological character displacement and indirect interactions between sympatric stickleback species mediated by their top predators. These results suggest that predation may facilitate, rather than hinder, the process of divergence in sympatry.     

Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks

During sexual imprinting, offspring learn parental phenotypes and then select mates who are similar to their parents. Imprinting has been thought to contribute to the process of speciation in only a few rare cases; this is despite imprinting's potential to generate assortative mating and solve the problem of recombination in ecological speciation. If offspring imprint on parental traits under divergent selection, these traits will then be involved in both adaptation and mate preference. Such 'magic traits' easily generate sexual isolation and facilitate speciation. In this study, we show that imprinting occurs in two ecologically divergent stickleback species (benthics and limnetics: Gasterosteus spp.). Cross-fostered females preferred mates of their foster father's species. Furthermore, imprinting is essential for sexual isolation between species; isolation was reduced when females were raised without fathers. Daughters imprinted on father odour and colour during a critical period early in development. These traits have diverged between the species owing to differences in ecology. Therefore, we provide the first evidence that imprinting links ecological adaptation to sexual isolation between species. Our results suggest that imprinting may facilitate the evolution of sexual isolation during ecological speciation, may be especially important in cases of rapid diversification, and thus play an integral role in the generation of biodiversity.     

MHC-based mate choice combines good genes and maintenance of MHC polymorphism

Polymorphic genes of the major histocompatibility complex (MHC) are regarded as essential genes for individual fitness under conditions of natural and sexual selection. To test this hypothesis, we investigated the ultimate individual fitness trait — that of reproductive success. We used three-spined sticklebacks ( Gasterosteus aculeatus ) in seminatural enclosures, located in natural breeding areas where the experimental fish had been caught. During their reproductive period, fish were exposed continuously to their natural sympatric parasites. By genotyping almost 4000 eggs with nine microsatellites, we determined parenthood and inferred female mating decision. We found that with reference to their own MHC profile, female sticklebacks preferred to mate with males sharing an intermediate MHC diversity. In addition, males with a specific MHC haplotype were bigger and better at fighting a common parasite ( Gyrodactylus sp.). This translated directly into Darwinian fitness since fish harbouring this specific MHC haplotype were more likely to be chosen and had a higher reproductive output. We conclude that females also based their mating decision on a specific MHC haplotype conferring resistance against a common parasite. This identifies and supports 'good genes'. We argue that such an interaction between host and parasite driving assortative mating is not only a prerequisite for negative frequency-dependent selection — a potential mechanism to explain the maintenance of MHC polymorphism, but also potentially speciation.     

Parasite diversity,patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes

Ecological speciation has been the subject of intense research in evolutionary biology but the genetic basis of the actual mechanism driving reproductive isolation has rarely been identified. The extreme polymorphism of the major histocompatibility complex (MHC), probably maintained by parasite-mediated selection, has been proposed as a potential driver of population divergence. We performed an integrative field and experimental study using three-spined stickleback river and lake ecotypes. We characterized their parasite load and variation at MHC class II loci. Fish from lakes and rivers harbor contrasting parasite communities and populations possess different MHC allele pools that could be the result of a combined action of genetic drift and parasite-mediated selection. We show that individual MHC class II diversity varies among populations and is lower in river ecotypes. Our results suggest the action of homogenizing selection within habitat type and diverging selection between habitat types. Finally, reproductive isolation was suggested by experimental evidence: in a flow channel design females preferred assortatively the odor of their sympatric male. This demonstrates the role of olfactory cues in maintaining reproductive isolation between diverging fish ecotypes.     

Genomic insights into the vulnerability of sympatric whitefish species flocks

The erosion of habitat heterogeneity can reduce species diversity directly but can also lead to the loss of distinctiveness of sympatric species through speciation reversal. We know little about changes in genomic differentiation during the early stages of these processes, which can be mediated by anthropogenic perturbation. Here, we analyse three sympatric whitefish species (Coregonus spp) sampled across two neighbouring and connected Swiss pre‐alpine lakes, which have been differentially affected by anthropogenic eutrophication. Our data set comprises 16,173 loci genotyped across 138 whitefish using restriction‐site associated DNA sequencing (RADseq). Our analysis suggests that in each of the two lakes, the population of a different, but ecologically similar, whitefish species declined following a recent period of eutrophication. Genomic signatures consistent with hybridization are more pronounced in the more severely impacted lake. Comparisons between sympatric pairs of whitefish species with contrasting ecology, where one is shallow benthic and the other one more profundal pelagic, reveal genomic differentiation that is largely correlated along the genome, while differentiation is uncorrelated between pairs of allopatric provenance with similar ecology. We identify four genomic loci that provide evidence of parallel divergent adaptation between the shallow benthic species and the two different more profundal species. Functional annotations available for two of those loci are consistent with divergent ecological adaptation. Our genomic analysis indicates the action of divergent natural selection between sympatric whitefish species in pre‐alpine lakes and reveals the vulnerability of these species to anthropogenic alterations of the environment and associated adaptive landscape.     

Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations

The unprecedented polymorphism in the major histocompatibility complex (MHC) genes is thought to be maintained by balancing selection from parasites. However, do parasites also drive divergence at MHC loci between host populations, or do the effects of balancing selection maintain similarities among populations? We examined MHC variation in populations of the livebearing fish Poecilia mexicana and characterized their parasite communities. Poecilia mexicana populations in the Cueva del Azufre system are locally adapted to darkness and the presence of toxic hydrogen sulphide, representing highly divergent ecotypes or incipient species. Parasite communities differed significantly across populations, and populations with higher parasite loads had higher levels of diversity at class II MHC genes. However, despite different parasite communities, marked divergence in adaptive traits and in neutral genetic markers, we found MHC alleles to be remarkably similar among host populations. Our findings indicate that balancing selection from parasites maintains immunogenetic diversity of hosts, but this process does not promote MHC divergence in this system. On the contrary, we suggest that balancing selection on immunogenetic loci may outweigh divergent selection causing divergence, thereby hindering host divergence and speciation. Our findings support the hypothesis that balancing selection maintains MHC similarities among lineages during and after speciation (trans‐species evolution).     

STRONG ASSORTATIVE MATING BY DIET,COLOR, SIZE,AND MORPHOLOGY BUT LIMITED PROGRESS TOWARD SYMPATRIC SPECIATION IN A CLASSIC EXAMPLE: CAMEROON CRATER LAKE CICHLIDS

Models predict that sympatric speciation depends on restrictive parameter ranges, such as sufficiently strong disruptive selection and assortative mating, but compelling examples in nature have rarely been used to test these predictions. I measured the strength of assortative mating within a species complex of Tilapia in Lake Ejagham, Cameroon, a celebrated example of incipient sympatric adaptive radiation. This species complex is in the earliest stages of speciation: morphological and ecological divergence are incomplete, species differ primarily in breeding coloration, and introgression is common. I captured 27 mated pairs in situ and measured the diet, color, size, and morphology of each individual. I found strong assortative mating by color, size, head depth, and dietary source of benthic or pelagic prey along two independent dimensions of assortment. Thus, Ejagham Tilapia showed strong assortative mating most conducive to sympatric speciation. Nonetheless, in contrast to a morphologically bimodal Sarotherodon cichlid species pair in the lake, Ejagham Tilapia show more limited progress toward speciation, likely due to insufficient strength of disruptive selection on morphology estimated in a previous study (γ = 0.16). This supports the predicted dependence of sympatric speciation on strong assortment and strong disruptive selection by examining a potentially stalled example in nature.     

Weak link between dispersal and parasite community differentiation or immunogenetic divergence in two sympatric cichlid fishes

Geographical isolation, habitat variation and trophic specialization have contributed to a large extent to the astonishing diversity of cichlid fishes in the Great East African lakes. Because parasite communities often vary across space and environments, parasites can accompany and potentially enhance cichlid species diversification. However, host dispersal may reduce opportunities for parasite‐driven evolution by homogenizing parasite communities and allele frequencies of immunity genes. To test for the relationships between parasite community variation, host dispersal and parasite‐induced host evolution, we studied two sympatric cichlid species with contrasting dispersal capacities along the shores of southern Lake Tanganyika. Whereas the philopatric Tropheus moorii evolved into several genetically differentiated colour morphs, Simochromis diagramma is phenotypically rather uniform across its distribution range and shows only weak population structure. Populations of both species were infected with divergent parasite communities and harbour differentiated variant pools of an important set of immune genes, the major histocompatibility complex (MHC). The overall extent of geographical variation of parasites and MHC genes was similar between host species. This indicates that immunogenetic divergence among populations of Lake Tanganyika cichlids can occur even in species that are strongly dispersing. However, because this also includes species that are phenotypically uniform, parasite‐induced evolution may not represent a key factor underlying species diversification in this system.     

Discrete foraging niches promote ecological, phenotypic, and genetic divergence in sympatric whitefish (Coregonus lavaretus)

Natural populations often vary in their degree of ecological, morphological and genetic divergence. This variation can be arranged along an ecological speciation continuum of increasingly discrete variation, with high inter-individual variation at one end and well defined species in the other. In postglacial fishes, evolutionary divergence has commonly resulted in the co-occurrence of a pelagic and a benthic specialist. We studied three replicate lakes supporting sympatric pelagic and benthic European whitefish (Coregonus lavaretus (L.)) morphs in search for early signs of possible further divergence into more specialized niches. Using stomach content data (recent diet) and stable isotope analyses (time-integrated measure of trophic niche use), we observed a split in the trophic niche within the benthic whitefish morph, with individuals specializing on either littoral or profundal resources. This divergence in resource use was accompanied by small but significant differences in an adaptive morphological trait (gill raker number) and significant genetic differences between fish exploiting littoral and profundal habitats and foraging resources. The same pattern of parallel divergence was found in all three lakes, suggesting similar natural selection pressures driving and/or maintaining the divergence. The two levels of divergence (a clear and robust benthic – pelagic and a more subtle littoral – profundal divergence) observed in this study apparently represent different stages in the process of ecological speciation.     

Temporal stability of niche use exposes sympatric Arctic charr to alternative selection pressures

There is now strong evidence that foraging niche specialisation plays a critical role in the very early stages of resource driven speciation. Here we test critical elements of models defining this process using a known polymorphic population of Arctic charr from subarctic Norway. We test the long-term stability of niche specialisation amongst foraging predators and discuss the possibility that contrasting foraging specialists are exposed to differing selection regimes. Inter-individual foraging niche stability was measured by combining two time-integrated ecological tracers of the foraging niche (each individual’s δ¹³C and δ¹⁵N stable isotope (SI) signatures and their food borne parasite fauna) with a short-term measure of foraging niche use (stomach contents composition). Three dietary subgroups of predators were identified, including zooplankton, gammarid and benthivore specialists foragers. Zooplanktivorous specialists had muscle low in δ ¹³C, a high abundance of parasites transmitted from pelagic copepods, a smaller head, longer snout and a more slender body-form than gammaridivorous specialist individuals which had muscle more enriched in δ ¹³C and high abundance of parasites transmitted from benthic Gammarus. Benthivorous individuals were intermediate between the other two foraging groups according to muscle SI-signals (δ¹³C) and loadings of parasites transmitted from both copepods and Gammarus. The close relationship between subgroups identified by stomach contents, time-integrated tracers of niche use (SI and parasites) and functional trophic morphology (niche adaptations) demonstrate a long-term temporally stable niche use of each individual predator. Differential habitat use and contrasting parasite communities and loadings, show differential exposure to different suites of selection pressures for different foraging specialists. Results also show that individual specialisation in trophic behaviour and thus exposure to different suites of selection pressures are stable over time, and thus provide a platform for disruptive selection to operate within this sympatric system.