Water temperature,not fish morph,determines parasite infections of sympatric Icelandic threespine sticklebacks (Gasterosteus aculeatus)

Parasite communities of fishes are known to respond directly to the abiotic environment of the host, for example, to water quality and water temperature. Biotic factors are also important as they affect the exposure profile through heterogeneities in parasite distribution in the environment. Parasites in a particular environment may pose a strong selection on fish. For example, ecological differences in selection by parasites have been hypothesized to facilitate evolutionary differentiation of freshwater fish morphs specializing on different food types. However, as parasites may also respond directly to abiotic environment the parasite risk does not depend only on biotic features of the host environment. It is possible that different morphs experience specific selection gradients by parasites but it is not clear how consistent the selection is when abiotic factors change. We examined parasite pressure in sympatric morphs of threespine stickleback (Gasterosteus aculeatus) across a temperature gradient in two large Icelandic lakes, Myvatn and Thingvallavatn. Habitat‐specific temperature gradients in these lakes are opposite. Myvatn lava rock morph lives in a warm environment, while the mud morph lives in the cold. In Thingvallavatn, the lava rock morph lives in a cold environment and the mud morph in a warm habitat. We found more parasites in fish living in higher temperature in both lakes, independent of the fish morph, and this pattern was similar for the two dominating parasite taxa, trematodes and cestodes. However, at the same time, we also found higher parasite abundance in a third morph living in deep cold–water habitat in Thingvallavatn compared to the cold‐water lava morph, indicating strong effect of habitat‐specific biotic factors. Our results suggest complex interactions between water temperature and biotic factors in determining the parasite community structure, a pattern that may have implications for differentiation of stickleback morphs.     

Divergence in social foraging among morphs of the three‐spined stickleback,Gasterosteus aculeatus

Foraging in social groups has a number of benefits but can also increase the risk of exploitation. High tendency to shoal may be correlated with groups foraging, although facultatively social fish adjust both shoaling decisions and food resource defence based on intrinsic and extrinsic factors. The main aim of this study was to examine the relationships between shoaling, solitary foraging and aggression, forager tolerance of conspecifics joining at a discovered food patch and forager exploitation of resources discovered by others. We used two intra‐lacustrine three‐spined stickleback morph pairs, lava and mud, and monomorphic morphs from each of lava and mud habitats. The lava morph formed less cohesive shoals, was bolder during solitary foraging, approached and entered an occupied food patch less frequently than the mud morph, suggesting a link between shoaling and the propensity for social foraging. However, shoaling tendency and joiner tolerance were not correlated at a population level. Intralacustrine lava and mud morphs differed more markedly in joiner tolerance than morphs from single habitat lakes, whereas the opposite was true for shoaling tendency. We conclude that, in addition to differentiation in shoaling tendency, the lava and mud morphs differ in social foraging and these variations may act to promote population divergence. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 194–203.     

Sympatric and Allopatric Divergence of MHC Genes in Threespine Stickleback

Parasites can strongly affect the evolution of their hosts, but their effects on host diversification are less clear. In theory, contrasting parasite communities in different foraging habitats could generate divergent selection on hosts and promote ecological speciation. Immune systems are costly to maintain, adaptable, and an important component of individual fitness. As a result, immune system genes, such as those of the Major Histocompatability Complex (MHC), can change rapidly in response to parasite-mediated selection. In threespine stickleback (Gasterosteus aculeatus), as well as in other vertebrates, MHC genes have been linked with female mating preference, suggesting that divergent selection acting on MHC genes might influence speciation. Here, we examined genetic variation at MHC Class II loci of sticklebacks from two lakes with a limnetic and benthic species pair, and two lakes with a single species. In both lakes with species pairs, limnetics and benthics differed in their composition of MHC alleles, and limnetics had fewer MHC alleles per individual than benthics. Similar to the limnetics, the allopatric population with a pelagic phenotype had few MHC alleles per individual, suggesting a correlation between MHC genotype and foraging habitat. Using a simulation model we show that the diversity and composition of MHC alleles in a sympatric species pair depends on the amount of assortative mating and on the strength of parasite-mediated selection in adjacent foraging habitats. Our results indicate parallel divergence in the number of MHC alleles between sympatric stickleback species, possibly resulting from the contrasting parasite communities in littoral and pelagic habitats of lakes.     

Inter- and intra-morph patterns in helminth communities of sympatric whitefish morphs

Infection patterns of trophically transmitted helminth parasites were compared with feeding ecology in two sympatric whitefish Coregonus lavaretus morphs from two lake systems in northern Norway. In both lakes, the pelagic morph was an obligate zooplanktivore, while the benthic morph utilized both the benthivore and zooplanktivore trophic niches. The differences in niche utilization between the two morphs were associated with differences in trophic morphology (gill raker numbers), suggesting that they were genetically dissimilar and reproductively isolated. The benthic morph had the highest number of helminth species, probably because they exhibited a broader niche width compared to the pelagic morph. In both lakes, the species composition and intensities of helminths reflected the trophic diversification of the whitefish ecotypes with respect to different habitat choice (benthic v . pelagic) and dietary specialization (benthivore v . zooplanktivore feeding strategies within the benthic whitefish morph). Zooplanktivorous fish from both morphs acquired parasites mainly from pelagic copepods and in almost equal quantities. The benthivore feeders within the benthic morph had the highest proportion of parasites with transmission stages from benthic organisms. Host feeding behaviour seemed to be a major determinant of the helminth community structure, and helminths appeared to be useful indicators of long-term trophic specialization of whitefish ecotypes.     

Genetically isolated sympatric forms of threespine stickleback,Gasterosteus aculeatus,in Lake Azabachije (Kamchatka-peninsula,USSR)

Synopsis Two sympatric morphs of threespine stickleback Gasterosteus aculeatus are found in Lake Azabachije (Kamchatka, USSR); resident low-plated leiurus and completely plated trachurus, migrating from the Bering sea into the Lake to spawn. The absence of the intermediate morph semiarmatus and significant differences in a number of characters are indicative of reproductive isolation. The results show that the leiurus morph is common in the regions other than those with mild climate and small seasonal fluctuations of temperature.     

Disentangling the role of MHC‐dependent ‘good genes' and ‘compatible genes' in mate‐choice decisions of three‐spined sticklebacks Gasterosteus aculeatus under semi‐natural conditions

To investigate and disentangle the role of major histocompatibility complex (MHC)‐based ‘good genes' and ‘compatible genes' in mate choice, three‐spined sticklebacks Gasterosteus aculeatus with specific MHC IIB genotypes were allowed to reproduce in an outdoor enclosure system. Here, fish were protected from predators but encountered their natural parasites. Mate choice for an intermediate genetic distance between parental MHC genotypes was observed, which would result in intermediate diversity in the offspring, but no mate choice based on good genes was found under the current semi‐natural conditions. Investigation of immunological variables revealed that the less‐specific innate immune system was more active in individuals with a genetically more divergent MHC allele repertoire. This suggests the need to compensate for an MHC‐diminished T‐cell repertoire and potentially explains the observed mate choice for intermediate MHC genetic distance. The present findings support a general pattern of mate choice for intermediate MHC diversity (i.e. compatible genes). In addition, the potentially dynamic role of MHC good genes in mate choice under different parasite pressures is discussed in the light of present and previous results.     

Schistocephalus solidus parasite prevalence and biomass intensity in threespine stickleback vary by habitat and diet in boreal lakes

Trophically-transmitted parasites can affect intermediate host behaviors, resulting in spatial differences in parasite prevalence and distribution that shape the dynamics of hosts and their ecosystems. This variability may arise through differences in physical habitats or biological interactions between parasites and their hosts, and may occur on very fine spatial scales. Using a pseudophyllidean cestode (Schistocephalus solidus) and the threespine stickleback (Gasterosteus aculeatus) as a model parasite–host complex, we investigated the association of infection with host diet composition and stomach fullness in different habitats of two large lakes in southwest Alaska. To become infected, the fish must consume pelagic copepods infected with the parasite’s procercoid stage, so we predicted higher infection rates of fish in offshore habitats (where zooplankton are the primary prey) compared to fish from the littoral zone. Sticklebacks collected from the littoral and limnetic zones were assayed for parasites and their stomach contents were classified, counted, and weighed. Contrary to our prediction, permutational multivariate analysis of variance and principal components analysis revealed that threespine sticklebacks in the littoral zone, which consumed a generalist diet (pelagic zooplankton and benthic invertebrates), had higher parasite prevalence and biomass intensity than conspecifics in the limnetic zone, which consumed zooplankton. These results, consistent in two different lakes, suggest that differences in parasite prevalence between habitats may have been determined by a shift in host habitat due to infection, differential host mortality across habitats, differential procercoid prevalence in copepods across habitats, or a combination of the three factors. This paradoxical result highlights the potential for fine spatial variability in parasite abundance in natural systems.     

Variation of telencephalon morphology of the threespine stickleback (Gasterosteus aculeatus) in relation to inferred ecology

We tested the hypothesis that increased telencephalon size has evolved in threespine stickleback fish (Gasterosteus aculeatus) from structurally complex habitats using field‐caught samples from one sea‐run (ancestral) and 18 ecologically diverse freshwater (descendant) populations. Freshwater habitats ranged from shallow, structurally complex lakes with benthic‐foraging stickleback (benthics), to deeper, structurally simple lakes in which stickleback depend more heavily on plankton for prey (generalists). Contrary to our expectations, benthics had smaller telencephala than generalists, but the shape of the telencephalon of the sea‐run and benthic populations were more convex laterally. Convex telencephalon shape may indicate enlargement of the dorsolateral region, which is homologous with the tetrapod hippocampus. Telencephalon morphology is also sexually dimorphic, with larger, less convex telencephala in males. Freshwater stickleback from structurally complex habitats have retained the ancestral telencephalon morphology, but populations that feed more in open habitats on plankton have evolved larger, laterally concave telencephala.     

Parallel Evolution,not Always so Parallel: Comparison of Small Benthic Charr, <Emphasis Type="Italic">Salvelinus alpinus</Emphasis>, from Grímsnes and Thingvallavatn,Iceland

Synopsis Iceland is unique in terms of geologically young freshwater systems and rapid adaptations of fresh water fishes to diverse habitats, e.g. lava with ground water flow. Iceland has six species of freshwater fishes, including Arctic charr, Salvelinus alpinus. Previous research has shown great diversity within this species. Four different morphs of Arctic charr are found in one lake, Thingvallavatn, including a small benthivorous charr. Similar populations of small benthic charr are known from several other Icelandic freshwater locations, including Nautavakir in Grímsnes. Our comparison of the small benthic charr morphs in Thingvallavatn and in Grímsnes showed that they are similar in morphology but distinguishable in several characteristics. Small benthic charr in Grímsnes and Thingvallavatn demonstrate similar adaptations and are an example of parallel evolution. However, subtle morphological differences between them indicate further specialized adaptations at each location.     

Extensive genetic differentiation between recently evolved sympatric Arctic charr morphs

The availability of diverse ecological niches can promote adaptation of trophic specializations and related traits, as has been repeatedly observed in evolutionary radiations of freshwater fish. The role of genetics, environment, and history in ecologically driven divergence and adaptation, can be studied on adaptive radiations or populations showing ecological polymorphism. Salmonids, especially the Salvelinus genus, are renowned for both phenotypic diversity and polymorphism. Arctic charr (Salvelinus alpinus) invaded Icelandic streams during the glacial retreat (about 10,000 years ago) and exhibits many instances of sympatric polymorphism. Particularly, well studied are the four morphs in Lake Þingvallavatn in Iceland. The small benthic (SB), large benthic (LB), planktivorous (PL), and piscivorous (PI) charr differ in many regards, including size, form, and life history traits. To investigate relatedness and genomic differentiation between morphs, we identified variable sites from RNA‐sequencing data from three of those morphs and verified 22 variants in population samples. The data reveal genetic differences between the morphs, with the two benthic morphs being more similar and the PL‐charr more genetically different. The markers with high differentiation map to all linkage groups, suggesting ancient and pervasive genetic separation of these three morphs. Furthermore, GO analyses suggest differences in collagen metabolism, odontogenesis, and sensory systems between PL‐charr and the benthic morphs. Genotyping in population samples from all four morphs confirms the genetic separation and indicates that the PI‐charr are less genetically distinct than the other three morphs. The genetic separation of the other three morphs indicates certain degree of reproductive isolation. The extent of gene flow between the morphs and the nature of reproductive barriers between them remain to be elucidated.     

The Round Goby, Neogobius melanostomus, a Fish Invader on both sides of the Atlantic Ocean

During the past decade, a bottom-dwelling, aggressive, multiple-spawning fish, the round goby (Gobiidae: Neogobius melanostomus), has spread from its native region in the Ponto-Caspian throughout Europe and to the Laurentian Great Lakes in North America. An international workshop, held at the Hel Marine Station, Poland, was organized to summarize population features of the round goby. Common fish predators of round gobies in the Great Lakes and in native regions are obligate and facultative benthic fishes and occasionally, pelagic fishes. In contrast, the main predator of the round goby in the Gulf of Gdansk is the Great Cormorant (Phalacrocorax carbo). In the Great Lakes, round gobies have lead to the decline of mottled sculpin (Cottus bairdi) and logperch (Percina caprodes) and reduced the hatching success of native fishes by feeding on their eggs. In the Gulf of Gdansk, round gobies have increased in abundance, while three-spined sticklebacks (Gasterosteus aculeatus) have declined. Round gobies have a broad diet throughout their range; larger specimens are molluscivores. There are fewer species of parasites and lower infection rates of round gobies in recently colonized areas than in native areas. Overall, newly colonized round gobies in brackish waters and lakes are smaller, mature earlier, have a male biased operational sex ratio and are more short-lived compared with round gobies from marine (native) habitats.     

Non‐parallel divergence across freshwater and marine three‐spined stickleback Gasterosteus aculeatus populations

This work investigated whether multiple freshwater populations of three‐spined stickleback Gasterosteus aculeatus in different freshwater catchments in the Jutland Peninsula, Denmark, derived from the same marine populations show repeated adaptive responses. A total of 327 G. aculeatus collected at 13 sampling locations were screened for genetic variation using a combination of 70 genes putatively under selection and 26 neutral genes along with a marker linked to the ectodysplasin gene (eda), which is strongly correlated with plate armour morphs in the species. A highly significant genetic differentiation was found that was higher among different freshwater samples than between marine–freshwater samples. Tests for selection between marine and freshwater populations showed a very low degree of parallelism and no single nucleotide polymorphism was detected as outlier in all freshwater–marine pairwise comparisons, including the eda. This suggests that G. aculeatus is not necessarily the prime example of parallel local adaptation suggested in much of the literature and that important exceptions exist (i.e. the Jutland Peninsula). While marine populations in the results described here showed a high phenotype–genotype correlation at eda, a low association was found for most of the freshwater populations. The most extreme case was found in the freshwater Lake Hald where all low‐plated phenotypes were either homozygotes for the allele supposed to be associated with completely plated morphs or heterozygotes, but none were homozygotes for the putative low‐plated allele. Re‐examination of data from seven G. aculeatus studies agrees in showing a high but partial association between phenotype–genotype at eda in G. aculeatus freshwater populations and that mismatches occur everywhere in the European regions studied (higher in some areas, i.e. Denmark). This is independent of the eda marker used.     

Patterns of morphological changes and hybridization between sympatric whitefish morphs (Coregonus spp.) in a Swiss lake: a role for eutrophication?

Whitefish, genus Coregonus, show exceptional levels of phenotypic diversity with sympatric morphs occurring in numerous postglacial lakes in the northern hemisphere. Here, we studied the effects of human‐induced eutrophication on sympatric whitefish morphs in the Swiss lake, Lake Thun. In particular, we addressed the questions whether eutrophication (i) induced hybridization between two ecologically divergent summer‐spawning morphs through a loss of environmental heterogeneity, and (ii) induced rapid adaptive morphological changes through changes in the food web structure. Genetic analysis based on 11 microsatellite loci of 282 spawners revealed that the pelagic and the benthic morph represent highly distinct gene pools occurring at different relative proportions on all seven known spawning sites. Gill raker counts, a highly heritable trait, showed nearly discrete distributions for the two morphs. Multilocus genotypes characteristic of the pelagic morph had more gill rakers than genotypes characteristic of benthic morph. Using Bayesian methods, we found indications of recent but limited introgressive hybridization. Comparisons with historical gill raker data yielded median evolutionary rates of 0.24 haldanes and median selection intensities of 0.27 for this trait in both morphs for 1948–2004 suggesting rapid evolution through directional selection at this trait. However, phenotypic plasticity as an alternative explanation for this phenotypic change cannot be discarded. We hypothesize that both the temporal shifts in mean gill raker counts and the recent hybridization reflect responses to changes in the trophic state of the lake induced by pollution in the 1960s, which created novel selection pressures with respect to feeding niches and spawning site preferences.     

Implications of a fossil stickleback assemblage for Darwinian gradualism

Darwin postulated that a complete fossil record would contain numerous gradual transitions between ancestral and descendant species, but 150 years after publication of The Origin of Species, few such transitions have materialized. The fossil stickleback Gasterosteus doryssus and the deposit in which it occurs provide excellent conditions to detect such transitions. Abundant, well‐preserved fossils occur in a stratigraphic setting with fine temporal resolution. The paleoecology of G. doryssus resembles the ecology of modern lakes that harbour the phenotypically similar three‐spined stickleback Gasterosteus aculeatus. Gasterosteus aculeatus are primitively highly armoured, but G. doryssus comprised two contemporaneous biological species with relatively weak armour, including a near‐shore, benthic feeder (benthic) and an offshore planktivore (limnetic). The benthic species expanded its range into the limnetic zone of the lake, where it apparently switched to planktivory and evolved reduced armour within c. 5000 years in response to directional selection. Although gradual evolution of mean phenotypes occurred, a single major gene caused much of evolutionary change of the pelvic skeleton. Thus, Darwin's expectation that transitions between species in the fossil record would be gradual was met at a fine time scale, but for pelvic structure, a well‐studied trait, his expectation that gradual change would depend entirely on numerous, small, heritable differences among individuals was incorrect.     

Variability in the functional role of Arctic charr Salvelinus alpinus as it relates to lake ecosystem characteristics

This study investigated how dietary habits vary with lake characteristics in a fish species that exhibits extensive morphological and ecological variability, the Arctic charr Salvelinus alpinus. Iceland is a hotspot of geological activity, so its freshwater ecosystems vary greatly in physical and chemical attributes. Associations of dietary items within guts of charr were used to form prey categories that reflect habitat-specific feeding behavior. Six prey categories were defined and dominated by snails (Radix peregra), fish (Gasterosteus aculeatus), tadpole shrimp (Lepidurus arcticus), chironomid pupae, pea clam (Pisidium spp.), and the cladoceran Bosmina sp.. These reflected different combinations of feeding in littoral stone, offshore benthic, and limnetic habitats. Certain habitat-specific feeding strategies consistently occurred alongside each other within lakes. For example, zooplanktivory occurred in the same lakes as consumption from offshore habitats; piscivory occurred in the same lakes as consumption from littoral benthic habitats. Redundancy analyses (RDA) were used to investigate how lake environment was related to consumption of different prey categories. The RDA indicated that piscivory exhibited by Arctic charr was reduced where brown trout were abundant and lakes were shallow, greater zooplanktivory occurred at lower latitudes and under decreased nutrient but higher silicon dioxide concentrations, and benthic resource consumption was associated with shallower lakes and higher altitudes. This study showed that trends previously observed across fish species were supported at the intraspecific level, indicating that a single species with flexible dietary habits can fill functional roles expected of multiple species in more diverse food webs.     

Convergent evolutionary processes driven by foraging opportunity in two sympatric morph pairs of Arctic charr with contrasting post‐glacial origins

The expression of two or more discrete phenotypes amongst individuals within a species (morphs) provides multiple modes upon which selection can act semi‐independently, and thus may be an important stage in speciation. In the present study, we compared two sympatric morph systems aiming to address hypotheses related to their evolutionary origin. Arctic charr in sympatry in Loch Tay, Scotland, exhibit one of two discrete, alternative body size phenotypes at maturity (large or small body size). Arctic charr in Loch Awe segregate into two temporally segregated spawning groups (breeding in either spring or autumn). Mitochondrial DNA restriction fragment length polymorphism analysis showed that the morph pairs in both lakes comprise separate gene pools, although segregation of the Loch Awe morphs is more subtle than that of Loch Tay. We conclude that the Loch Awe morphs diverged in situ (within the lake), whereas Loch Tay morphs most likely arose through multiple invasions by different ancestral groups that segregated before post‐glacial invasion (i.e. in allopatry). Both morph pairs showed clear trophic segregation between planktonic and benthic resources (measured by stable isotope analysis) but this was significantly less distinct in Loch Tay than in Loch Awe. By contrast, both inter‐morph morphological and life‐history differences were more subtle in Loch Awe than in Loch Tay. The strong ecological but relatively weak morphological and life‐history divergence of the in situ derived morphs compared to morphs with allopatric origins indicates a strong link between early ecological and subsequent genetic divergence of sympatric origin emerging species pairs. The emergence of parallel specialisms despite distinct genetic origins of these morph pairs suggests that the effect of available foraging opportunities may be at least as important as genetic origin in structuring sympatric divergence in post‐glacial fishes with high levels of phenotypic plasticity. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Short-and long term niche segregation and individual specialization of brown trout (Salmo trutta) in species poor Faroese lakes

Trophic niche divergence is considered to be a major process by which species coexistence is facilitated. When studying niche segregation in lake ecosystems, we tend to view the niche on a one-dimensional pelagic-littoral axis. In reality, however, the niche use may be more complex and individual fidelity to a niche may be variable both between and within populations. In order to study this complexity, relative simple systems with few species are needed. In this paper, we study how competitor presence affects the resource use of brown trout (Salmo trutta) in 11 species-poor Faroese lakes by comparing relative abundance, stable isotope ratios and diet in multiple habitats. In the presence of three-spined sticklebacks (Gasterosteus aculeatus), a higher proportion of the trout population was found in the pelagic habitat, and trout in general relied on a more pelagic diet base as compared to trout living in allopatry or in sympatry with Arctic charr (Salvelinus alpinus). Diet analyses revealed, however, that niche-segregation may be more complex than described on a one-dimensional pelagic-littoral axis. Trout from both littoral and offshore benthic habitats had in the presence of sticklebacks a less benthic diet as compared to trout living in allopatry or in sympatry with charr. Furthermore, we found individual habitat specialization between littoral/benthic and pelagic trout in deep lakes. Hence, our findings indicate that for trout populations interspecific competition can drive shifts in both habitat and niche use, but at the same time they illustrate the complexity of the ecological niche in freshwater ecosystems.     

Geographical variations in freshwater populations of the three-spined stickleback,Gasterosteus aculeatus,in Japan

This paper describes an investigation of morphological variation among six freshwater populations (dominantly low-plated morph) of the three-spined stickleback,Gasterosteus aculeatus, in Japan. Such populations are mainly distributed in restricted water areas within a band from Ise to Wakasa Bays, the most constricted part of Honshu Island. According to some differences in morphological variation, i.e. plate morph, number of lateral plates, body size, body shape and body colour, they were classified into two types corresponding to occurrence in the Ibi River and Lake Biwa water systems. The former type was monomorphic dominated by lowplated morphs in spring-fed water, whereas the latter was a dimorphic population consisting of low- and partially-plated morphs. My results suggest that the plate morph type is not correlated with climate nor predation but is related to geological isolation patterns during the course of the landlocking process. Conversely, variations in meristic (number of dorsal and anal fin rays and gill rakers) and morphometric (body shape and body colour) characteristics may have been related to different environmental conditions. This study also provides supporting evidence that the freshwater three-spined stickleback is a distinct species from the anadromous stickleback,G. aculeatus.     

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.