Effects of population,family, and diet on craniofacial morphology of Icelandic Arctic charr (Salvelinus alpinus)

We evaluated hypotheses of intralacustrine diversification and plastic responses to two diet environments in Icelandic Arctic charr (Salvelinus alpinus). Full‐sib families of progeny of wild polymorphic charr from two lakes where morphs vary in their degree of phenotypic and ecological divergence were split, with half of the offspring reared on a benthic and half on a limnetic type of diet to estimate family norms of reaction. We focused on variation in craniofacial traits because they are probably functionally related to diet and complement a previous study of body shape in these charr. A hierarchical analysis of phenotypic variation between lakes, pairs of morphs within each lake, and two families within each morph found that phenotypic variation partitioned between families relative to morphs was reduced in the more ecologically diversified population, which is consistent with adaptive diversification. The effect size of plastic responses between lake populations was similar, suggesting little difference in the degree of canalization in contrast to a previous analysis of body form plasticity. Thus, the role that plastic morphological responses play in the adaptive diversification of morphs and different lake populations of Arctic charr may depend on the trait. © 2013 The Linnean Society of London     

Incipient speciation driven by phenotypic plasticity? Evidence from sympatric populations of Arctic charr

Recent models suggest that the existence of environmentally induced polymorphisms within a single population (especially those related to foraging) facilitates the process of evolutionary divergence within a single gene pool by generating distinct phenotypic modes that are exposed to differential selection. In order to test a prediction of the phenotypic plasticity model of divergence, we used a well-documented polymorphism to disentangle the relative effects of morph and rearing environment in generating phenotypic variance. We reared first-generation offspring of two sympatric morphs of Arctic charr Salvelinus alpinus in the laboratory and compared their head morphology with that of their wild parents. Morphological characters with a known functional role in foraging were highly plastic. Rearing environment accounted for the largest component of the variation in expressed phenotype, but this environmental effect overlaid a clear (but small) genetic effect. We conclude that phenotypic plasticity has played a significant role in the evolution of this trophic polymorphism, but that the evolutionary process has progressed to the point that the gene pool is now segregated.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 611–618.     

Trophic polymorphism amongst Arctic charr from Loch Rannoch, Scotland

This paper describes the results of a multivariate and univariate morphometric analysis of three groups of Arctic charr Salvelinus alpinus from Loch Rannoch, Perthshire, Scotland, distinguished a priori on the basis of coloration (bright v. cryptic) and site of capture (from two locations 12 km apart). The analysis produced a clear and highly significant distinction, not only between brightly and cryptically coloured charr, but also between the two cryptically coloured groups, one of which was more robust in terms of several size-independent head measurements. Stomach analysis showed that the brightly coloured charr fed entirely on zooplankton, the less robust, cryptically coloured fish, fed on benthic macroinvertebrates, whereas a significant proportion of the diet of the more robust cryptically-coloured form consisted of other fish. Differences in length at age also distinguished the three forms, with the robust, piscivorous charr, which live longer and potentially reach a larger final size, attaining smaller sizes at a given age. These data clearly confirm the previous identification of a distinct planktivorous morph of Arctic charr in Loch Rannoch and extend the morph analysis by distinguishing two additional morphs, a benthivorous morph and a piscivorous morph that are morphologically and ecologically distinct. The results are discussed in the context of other systems in which sympatric morphs of Arctic charr have been described.     

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, ?? , ??–??.     

Parallel divergence of sympatric genetic and body size forms of Arctic charr,Salvelinus alpinus,from two Scottish lakes

F _ST and R_ST estimates for Arctic charr from six microsatelite markers collected from two neighbouring Scottish lakes, Loch Maree and Loch Stack, confirm the presence of two distinct genetic groupings representing separate populations within each lake. In both lakes, there was also a clear body size dimorphism, with large and small body size forms that segregated according to genetic grouping. There was evidence of only subtle foraging ecology differences between morphs, with the small body size morph in both lakes being more generalist in its foraging in the summer (consuming mostly plankton but also some macrobenthos) than the large body size morph, which specialized on planktonic prey. Trophic morphology (head and mouth shape) did not differ significantly between morphs (although the small sample size for Maree makes this a preliminary finding). Cluster analysis of the microsatelite data and the presence of private alleles showed that morphologically similar forms in different lakes were not genetically similar, as would be expected under a multiple invasion hypothesis. Thus, the data do not support a hypothesis of a dual invasion of both lakes by two common ancestors but instead suggest an independent origin of the two forms in each lake. Thus parallel sympatric divergence as a result of common selection pressures in both lakes is the most parsimonious explanation of the evolutionary origin of these polymorphisms. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 748–757.     

The functional significance of inherited differences in feeding morphology in a sympatric polymorphic population of Arctic charr

Artificially fertilised eggs from wild-caught Arctic charr parents of two sympatric morphs (benthivorous and planktivorous) from Loch Rannoch, Scotland were reared in the laboratory under identical conditions. During the subsequent 2 years, aspects of their trophic anatomy and feeding behaviour were compared. As previously described for wild-caught fish, charr derived from the benthivorous morph had an increasingly wider mouth gape for a given body length than those derived from the planktivorous morph. The functional significance of these differences in gape was tested by comparing the maximum size of prey that could be handled by each of the two morphs. In both forms, a larger gape enabled larger food particles to be eaten, but the elevation of the regression of maximum prey size on gape was higher in the benthivorous form, indicating the existence of additional morphological and/or behavioural differences influencing the size of prey consumed. When offered a choice between a typical benthic prey item and a typical pelagic food item, charr of benthivorous origin were more likely to feed on the former, whereas those of planktivorous origin were more likely to feed on the latter. Thus inherited differences in gape place constraints on foraging ability and are associated with inherited differences in dietary preference. We conclude that the functional significance of the foraging specialisations indicate a strong selection pressure for the evolution of the divergence and propose that heterochronic growth is the mechanism resulting in the divergence of tropic anatomy.     

Ecosystem size predicts eco‐morphological variability in a postglacial diversification

Identifying the processes by which new phenotypes and species emerge has been a long‐standing effort in evolutionary biology. Young adaptive radiations provide a model to study patterns of morphological and ecological diversification in environmental context. Here, we use the recent radiation (ca. 12k years old) of the freshwater fish Arctic charr (Salvelinus alpinus) to identify abiotic and biotic environmental factors associated with adaptive morphological variation. Arctic charr are exceptionally diverse, and in postglacial lakes there is strong evidence of repeated parallel evolution of similar morphologies associated with foraging. We measured head depth (a trait reflecting general eco‐morphology and foraging ecology) of 1,091 individuals across 30 lake populations to test whether fish morphological variation was associated with lake bathymetry and/or ecological parameters. Across populations, we found a significant relationship between the variation in head depth of the charr and abiotic environmental characteristics: positively with ecosystem size (i.e., lake volume, surface area, depth) and negatively with the amount of littoral zone. In addition, extremely robust‐headed phenotypes tended to be associated with larger and deeper lakes. We identified no influence of co‐existing biotic community on Arctic charr trophic morphology. This study evidences the role of the extrinsic environment as a facilitator of rapid eco‐morphological diversification.     

Differentiation of deep-water lake charr <Emphasis Type="Italic">Salvelinus namaycush</Emphasis> in North American lakes

Deep-water morphs of lake charr, Salvelinus namaycush, are found, with one exception, in four of the largest lakes in the world: lakes Superior and Mistassini (QC) and Great Bear and Slave lakes. This paper advances a hypothesis for resource polymorphisms involving two types of deep-water morph, one of which is characteristic of the humper and the other of the siscowet charrs of Lake Superior. My hypothesis states that, first, the humper, or a humper-like morph, diverged postglacially in sympatry from the ancestral common (shallow-water) lake charr and became a feeding specialist on Mysis relicta. Second, in at least two of the four lakes the siscowet, or a siscowet-like charr, diverged as a feeding specialist on postglacially derived forms of deep-water ciscoes. In Lake Superior a successional process may have resulted in dominance of the siscowet at the expense of the humper charr. I concur with a previous inference that the one occurrence of a deep-water charr in a small lake (the above exception) represents emigration from Lake Superior. I further infer that this event involved an early humper charr, which implies that this morphotype had differentiated in Lake Superior in less than 1,900 year. I suggest that innate differences in plasticity, breeding behavior and assortive mating, and philopatry account for why Arctic charr isolate readily in small lakes whereas lake charr do not. My hypothesis assumes divergence of deep-water morphs occurred postglacially, an idea consistent with genetic and biogeographical evidence.     

Characterizing neutral and adaptive genomic differentiation in a changing climate: The most northerly freshwater fish as a model

Arctic freshwater ecosystems have been profoundly affected by climate change. Given that the Arctic charr (Salvelinus alpinus) is often the only fish species inhabiting these ecosystems, it represents a valuable model for studying the impacts of climate change on species life‐history diversity and adaptability. Using a genotyping‐by‐sequencing approach, we identified 5,976 neutral single nucleotide polymorphisms and found evidence for reduced gene flow between allopatric morphs from two high Arctic lakes, Linne'vatn (Anadromous, Normal, and Dwarf) and Ellasjøen (Littoral and Pelagic). Within each lake, the degree of genetic differentiation ranged from low (Pelagic vs. Littoral) to moderate (Anadromous and Normal vs. Dwarf). We identified 17 highly diagnostic, putatively adaptive SNPs that differentiated the allopatric morphs. Although we found no evidence for adaptive differences between morphs within Ellasjøen, we found evidence for moderate (Anadromous vs. Normal) to high genetic differentiation (Anadromous and Normal vs. Dwarf) among morphs within Linne'vatn based on two adaptive loci. As these freshwater ecosystems become more productive, the frequency of sympatric morphs in Ellasjøen will likely shift based on foraging opportunities, whereas the propensity to migrate may decrease in Linne'vatn, increasing the frequency of the Normal morph. The Dwarf charr was the most genetically distinct group. Identifying the biological basis for small body size should elucidate the potential for increased growth and subsequent interbreeding with sympatric morphs. Overall, neutral and adaptive genomic differentiation between allopatric and some sympatric morphs suggests that the response of Arctic charr to climate change will be variable across freshwater ecosystems.     

Environmental factors associated with genetic and phenotypic divergence among sympatric populations of Arctic charr (Salvelinus alpinus)

The mechanisms by which phenotypic and genetic divergence may occur among sympatric, conspecific populations have been widely discussed but are still not well understood. Possible mechanisms include assortative mating based on morphology or variation in the reproductive behaviour of phenotypes, and both have been suggested to be relevant to the differentiation of salmonid populations in post-glacial lakes. Here, we studied Arctic charr (Salvelinus alpinus) in Windermere, where putative populations are defined by spatial and temporal variation in spawning. Genetic differentiation was assessed based on nine microsatellite loci, and phenotypic variation was assessed from morphometric characters. We test hypotheses about the relative role of morphology, spawning season and spawning habitat in the evolution of genetic divergence among these populations. Distinct from other lake systems, we find that both morphological and genetic differentiation are restricted primarily to one of two interconnecting basins, that genetic and morphological differentiation are decoupled in this lake and that both phenotype and environment have changed over the last 20 years. The implication is that breeding habitat plays a primary role in isolating populations that differentiate by drift and that phenotypically plastic changes, potentially related to foraging specializations, have either become secondarily decoupled from the genetically defined populations or were never fundamental in driving the evolution of genetic diversity in the Windermere system.     

Evidence for genetic differences in the offspring of two sympatric morphs of Arctic charr

The sub-arctic Lake Fjellfrøsvatn, northern Norway, has two morphs of Arctic charr that are reproductively isolated because they spawn 5 months apart. The smaller morph (≤14 cm L_F ) is confined to the profundal zone of the lake and the larger morph is mainly littoral. Three hypotheses were tested: (i) the offspring of the profundal Arctic charr grow slower than the offspring of the littoral Arctic charr under identical conditions, thus indicating a genetic basis for the slow growth of the profundal Arctic charr in the wild; (ii) the wild phenotypes of the two morphs are morphometrically different and the differences are persistent in the offspring; (iii) the offspring of the two morphs have different behaviour traits under similar treatments. The first hypothesis was rejected; offspring of the profundal morph grew slightly better than offspring of the littoral morph at 10° C in the laboratory. The second and third hypotheses were supported by the data. Wild-caught fish of the two morphs differed in several morphometric characters and most of the differences persisted in the offspring. In the laboratory, offspring of the littoral morph were more active, more aggressive and more pelagic than offspring of the profundal morph and naive offspring of the profundal morph were more effective in eating live chironomid larvae than were offspring of the littoral morph. The data for morphometry and behaviour, but not growth, provide evidence for genetic differences between the two Arctic charr morphs of Fjellfrøsvatn.     

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.     

Morphometric analysis of two ecologically distinct forms of Arctic charr, Salvelinus alpinus (L.), in Loch Rannoch, Scotland

Gill–netted samples of Arctic charr from Loch Rannoch, Scotland were bimodal when tested by univariate and multivariate morphometric analyses. The separation into two morphs corresponded very closely (95–98%) with fish classified subjectively in the field as benthic or pelagic, based largely on colour differences and ecological observations. The benthic charr had relatively longer heads, larger eyes and more powerful jaws than the pelagic charr. Unlike sympatric morphotypes described from Scandinavia and Greenland, neither Rannoch morph is dwarfed.     

Phenotype-specific feeding behaviour of two arctic charr Salvelinus alpinus morphs

The feeding performance of two morphs of a trophically polymorphic fish, the arctic charr Salvelinus alpinus, feeding on zooplankton, was studied in the laboratory. Limnetic morphs, with a fusiform body, terminal mouth, short pectoral fins, and relatively long and dense gill rakers, fed at significantly higher rates on Daphnia and Cyclops than did benthic morphs. The benthic morphs were characterized by a chunky body form, subterminal mouth, long pectoral fins, and relatively short and spaced-out gill rakers. The limnetic morphs attacked the prey at significantly higher rates and were more successful in capture. Benthic morphs were more reluctant to start feeding on zooplankton and reaction time was longer than in limnetic morphs. In the absence as well as presence of zooplankton food, the position of the two morphs in the aquaria differed markedly. The results agree with dietary differences found in field-collected fish. The limnetic morphs consume zooplankton, whereas benthic morphs specialize on Lymnaea gastropods. The results suggest that benthic morphs are phenotypically inferior at using the pelagic food niche. This implies that the current role of competitive or predatory interactions in segregating the morphs may be minor.     

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.     

Ecological polymorphism in Arctic charr

Arctic charr, Salvelinus alpinus (L.), commonly exhibits two coexisting morphotypes, dwarf and normal charr, which are characterized by differences in adult body size and colouration. We tested whether or not the morphotypic differences were genetically determined in rearing experiments with offspring of the two morphs and of their crosses. The experiments suggest that this ecological polymorphism in Arctic charr is largely environmentally determined. When reared under similar conditions, offspring of each of the two morphs differed little in size at the same age, and they had the same early developmental rate and maturation pattern. Moreover, the presence of parr marks along the flanks of the fish, one characteristic of dwarf charr, depended on body size and not on parental morph. Genetic differences between the morphs were suggested for growth rate during the second year of life, and for jaw morphology. Comparisons between charr life histories in captivity and in the wild suggest that ecological polymorphism in Arctic charr is chiefly a result of variation in growth conditions between different habitats.     

Morphological divergence between three Arctic charr morphs – the significance of the deep‐water environment

Morphological divergence was evident among three sympatric morphs of Arctic charr (Salvelinus alpinus (L.)) that are ecologically diverged along the shallow‐, deep‐water resource axis in a subarctic postglacial lake (Norway). The two deep‐water (profundal) spawning morphs, a benthivore (PB‐morph) and a piscivore (PP‐morph), have evolved under identical abiotic conditions with constant low light and temperature levels in their deep‐water habitat, and were morphologically most similar. However, they differed in important head traits (e.g., eye and mouth size) related to their different diet specializations. The small‐sized PB‐morph had a paedomorphic appearance with a blunt head shape, large eyes, and a deep body shape adapted to their profundal lifestyle feeding on submerged benthos from soft, deep‐water sediments. The PP‐morph had a robust head, large mouth with numerous teeth, and an elongated body shape strongly related to their piscivorous behavior. The littoral spawning omnivore morph (LO‐morph) predominantly utilizes the shallow benthic–pelagic habitat and food resources. Compared to the deep‐water morphs, the LO‐morph had smaller head relative to body size. The LO‐morph exhibited traits typical for both shallow‐water benthic feeding (e.g., large body depths and small eyes) and planktivorous feeding in the pelagic habitat (e.g., streamlined body shape and small mouth). The development of morphological differences within the same deep‐water habitat for the PB‐ and PP‐morphs highlights the potential of biotic factors and ecological interactions to promote further divergence in the evolution of polymorphism in a tentative incipient speciation process. The diversity of deep‐water charr in this study represents a novelty in the Arctic charr polymorphism as a truly deep‐water piscivore morph has to our knowledge not been described elsewhere.     

Lipid‐rich zooplankton subsidise the winter diet of benthivorous Arctic charr (Salvelinus alpinus) in a subarctic lake

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How fish-helminth associations arise: an example from Arctic charr in Loch Rannoch

Three sympatric morphs of Arctic charr Salvelinus alpinus occur in Loch Rannoch, Scotland, and are identified by their differing head morphology and diet. These are small-headed benthic, large-headed benthic and pelagic morphs. Six species of endoparasitic helminth were found in the fish, but the morphs had different patterns of infection. Overall infections in pelagic charr were heavier than in large-headed benthics, which were in turn heavier than in small-headed benthics, even though benthic charr live longer than pelagics. Pelagic fish had high prevalences and intensities of pseudophyllidean tapeworms, the intermediate hosts of which are copepods. The prevalence and intensity of metacercariae of Diplostomum sp. (the intermediate hosts of which are snails) were high in the benthic morphs. The results are discussed in terms of the effects of ecological factors on transmission of helminth parasites to their hosts and the evolution of host-parasite associations.     

Allometric trajectories of body and head morphology in three sympatric Arctic charr (Salvelinus alpinus (L.)) morphs

A study of body and head development in three sympatric reproductively isolated Arctic charr (Salvelinus alpinus (L.)) morphs from a subarctic lake (Skogsfjordvatn, northern Norway) revealed allometric trajectories that resulted in morphological differences. The three morphs were ecologically assigned to a littoral omnivore, a profundal benthivore and a profundal piscivore, and this was confirmed by genetic analyses (microsatellites). Principal component analysis was used to identify the variables responsible for most of the morphological variation of the body and head shape. The littoral omnivore and the profundal piscivore morph had convergent allometric trajectories for the most important head shape variables, developing bigger mouths and relatively smaller eyes with increasing head size. The two profundal morphs shared common trajectories for the variables explaining most of the body and head shape variation, namely head size relative to body size, placement of the dorsal and pelvic fins, eye size and mouth size. In contrast, the littoral omnivore and the profundal benthivore morphs were not on common allometric trajectories for any of the examined variables. The findings suggest that different selective pressures could have been working on traits related to their trophic niche such as habitat and diet utilization of the three morphs, with the two profundal morphs experiencing almost identical environmental conditions.