Genetic analysis of four sympatric morphs of Arctic charr,Salvelinus alpinus,from Thingvallavatn,Iceland

Synopsis The degree of genetic differentiation among four morphs of Arctic charr (small benthivorous, large benthivorous, piscivorous, and planktivorous) from Thingvallavatn, Iceland, was determined electrophoretically. Five of 36 enzyme loci were found to be polymorphic (Est2, Gpi3, Ldh4, Mdh4, 5 and Pgm2). However, only Est2 and Mdh4,5 showed enough variability to permit statistical analysis of divergence among morphs. All four morphs are very closely related; the values of Nei's (D) range from 0.00004 to 0.00126. These morphs are conspecific and do not represent different evolutionary lineages. There is significant genetic differentiation between the small benthivorous charr and the other three morphs. The relative relatedness of morphs based on gene frequency data is only partially concordant with that based on morphology and ecological specialization. The biological significance of this result is unclear because of the limited number of polymorphic loci upon which the genetic analysis is based and the high degree of relatedness among morphs.     

Molecular genetic examination of the polymorphic Arctic charr Salvelinus alpinus of Thingvallavatn, Iceland

Thingvallavatn, Iceland contains two sympatric morphotypes (benthic and limnetic) of Arctic charr Salvelinus alpinus. Each morphotype is composed of two morphs and these differ markedly in ecology, behaviour and life history. We used molecular genetic approaches to test whether (i) genetic heterogeneity exists among morphs and (ii) if morphs arose in allopatry and came into secondary contact or arose sympatrically within the lake through genetic segregation and/or phenotypic plasticity. Direct sequencing of 275 bp of the mitochondrial DNA (mtDNA) control region, mtDNA restriction fragment length polymorphisms and single locus minisatellite analyses detected insufficient variation to test our hypotheses. Analysis of multilocus minisatellite band sharing detected no significant differences between morphs within the same morphotype. However, significant differences among morphs belonging to different morphotypes suggest some genetic heterogeneity in Thingvallavatn charr. Limnetic charr from Thingvallavatn were more similar to sympatric benthic charr than to allopatric limnetics from two other Icelandic lakes. This suggests that the Thingvallavatn morphs arose sympatrically within the lake rather than in allopatry followed by secondary contact.     

Ecological parasitology of polymorphic Arctic charr, Salvelinus alpinus (L.), in Thingvallavatn, Iceland

The helminth endoparasite fauna in four Arctic charr morphs, Salvelinus alpinus (L.), small benthivorous (SB), large benthivorous (LB), planktivorous (PL) and piscivorous (PI) charr, from Thingvallavatn, Iceland consisted of: Crepidostomum farionis (Trematoda: Allocreadiidae); Diplosttomum sp. (Trematoda: Diplostomatidae); Eubothrium salvelini; Diphyllobothrium dendriticum; D. ditremum (Cestoda: Pseudophyllidae); Proteocephalus longicollis (Cestoda: Proteocepha-lidae): and Philonema oncorhynchi (Nematoda: Filariidae). The morphs exhibited distinctive patterns in prevalences and parasite burdens (mean intensity and mean relative density of parasites). SB charr had high prevalence and parasite burden of the eye fluke Diplostomum sp. and none to very light infections of the other parasite species. LB charr had relatively high prevalence and parasite burden of the intestinal fluke C. farionis , whereas infections of the remaining parasite species were light to moderate. PL and PI charr had high prevalences and worm burdens of Diphyllobothrium spp. and P. longicollis . PL charr differed from PI charr in higher worm burden off P. longicollis and lighter burden of £. salvelini . Prevalences of P. oncorhynchi were high in PL and PI charr. Association of parasite intensities and age and length offish were investigated. The different infection patterns among the morphs agree well with their partitioning in food and habitat utilization, and confirm that there is a high degree of ecological segregation between the morphs. The results demonstrate the importance of ecological factors influencing transmission efficiency of parasites to the fish host.     

Genetic differentiation among local populations and morphotypes of Arctic charr, Salvelinus alpinus

The systematica of coexisting morphotypes of Arctic charr, Salvelinus alpinus , has been a matter of dispute ever since the days of Linnaeus. Widespread allelic variation at an esterase locus has led some investigators to propose that the morphotypes reflect a complex of at least three sibling species. We tested this hypothesis by examining 42 electrophoretically detectable loci in natural and transplanted charr populations from 15 localities in S Norway. The absolute values of Nei's genetic distance between morphotypes and populations are small (typically in the order of 0.001), and morphotype changes may occur without accompanying changes in frequencies of esterase alleles. Differentiation among localities explains far more of the total gene diversity than differences between morphotypes in the four cases of naturally occurring sympatric morphotypes examined. The data are consistent with an intraspecific population structuring based on locality, and the multiple species hypothesis is rejected.     

Mitochondrial DNA diversity among four sympatric morphs of Arctic charr, Salvelinus alpinus L., from Thingvallavatn, Iceland

Restriction fragment length polymorphisms in mitochondrial DNA (mtDNA) were examined in progeny of four sympatric morphs of Arctic charr ( Salvelinus alpinus L.) from Thingvallavatn, Iceland. The mtDNA analysis with 46 hexanucleotide restriction enzymes indicates that the Thingvallavatn morphs are very closely related. Sequence divergence was less than 0.2% between any of the five clones detected. Although not significant, the topology of the mtDNA UPGMA dendogram was similar to that from a previous allozyme survey. Icelandic Arctic charr show greater affinity to charr from the British Isles than those from North America supporting their current taxonomic distinction.     

Alternative mating tactics of arctic charr,Salvelinus alpinus,in Thingvallavatn,Iceland

Synopsis During the spawning season the operational sex ratio of the large benthivorous (LB) arctic charr morph in Thingvallavatn is skewed in favour of males which compete intensely on the spawning site. The skewness is caused by males staying longer on the spawning ground than females. LB males employ two mating tactics. Either they guard the female or they attempt sneak-matings with guarded females. The tactics seem to obey a pure conditional strategy where relative size is the important criterion. Generally, the larger males use the guarding tactic and the smaller the sneaking tactic. Assessment of size is a part of the strategy. Relative size influences male behaviour irrespective of which tactic they employ. Guarding is more successful when courting is considered, both with respect to relative frequency and duration of courting acts. Females are aggressive towards the sneakers especially when they are small. This could be interpreted as female choice in favour of large males, but also as a defence against egg predation. A small dwarflike benthivorous morph (SB) is found in the same area. It is mainly active during night and on rare occasions SB-males are seen sneaking into the nest of LB-females. In such cases they are attacked vigorously by both LB sexes.     

Exercise,agonistic behaviour and food acquisition in Arctic charr,Salvelinus alpinus

Synopsis Although swimming is energetically costly, a number of studies on salmonid species have demonstrated increased growth rates in fishes forced to swim for prolonged periods at moderate speeds (typically 1–2 body lengths per sec). This suggests that additional energetic costs of swimming are more than met by alternative compensatory gains. The mechanisms underlying such effects are not fully understood. In this paper, we describe an experiment designed to examine one possible mechanism, namely a swimming-induced inhibition of aggression, with consequent beneficial effects on growth. The study used Arctic charr,Salvelinus alpinus, a species for which a positive relationship between exercise and growth has been clearly established. Using direct behavioural observations on small groups, we demonstrate that individuals displaying high levels of aggressive behaviour are able to monopolise access to food and that enforced swimming at a moderate speed (1 body length per sec) reduces the incidence of aggression although not the degree of monopolisation of food shown by aggressive individuals. These results suggest that the enhanced growth rates accompanying enforced swimming may reflect lower energetic costs of reduced aggressive activity rather than improved access to food by subordinates.     

Contrasting life history strategies of sympatric Arctic charr morphs, Salvelinus alpinus

In polymorphic populations morphs usually diverge in morphology, ecology and life history, which is most likely driven by adaptations to different environments or resources. Sympatric morphs may develop differences in several life history traits to be able to maximize fitness in alternative niches and habitats. Here, the contrasting life history traits of three sympatric Arctic charr (Salvelinus alpinus (L.)) morphs in a deep and oligotrophic lake in sub-arctic Norway are addressed. The charr morphs differ in spawning habitat and trophic niche. One is a littoral spawning morph that feeds on benthic invertebrates and zooplankton in the littoral and pelagic zones (referred to as the LO-morph), and two other are profundal spawning morphs that either utilize profundal soft bottom benthos as food resource (the PB-morph) or are piscivorous (the PP-morph). The LO-morph typically had intermediate life-history traits relative to the two profundal morphs that had highly contrasting life history traits, especially in growth and age and size of maturity. The PB-morph matured at a young age (～3 years) and at a small body size (～8.5 cm), thereby increasing their fitness by investing in reproduction early in life, which results in a short generation time and decreased probability of being predated before first reproduction. The PP-morph on the other hand, matured at an old age (～9.2 years) and a large body size (～26 cm), thereby increasing their fitness by investing in somatic growth to enhance initial fecundity, and also to reach a large body size profitable for piscivory. The different trade-off regime between the PP- and PB-morphs seems to be caused by adaptation to alternative trophic niches, and appears to be an important factor for the co-occurrence of the two sister-morphs in the profundal zone.     

Marine trophic niche use and life history diversity among Arctic charr Salvelinus alpinus in southwestern Greenland

Life history strategies and potential marine niche use of Arctic charr Salvelinus alpinus (n = 237, 84–652 mm, total body length, L_T) were determined during the ice-free season (2012) at three different watercourses in south-western Greenland. All Arctic charr were collected from freshwater habitats. Based on stable isotopes of δ³⁴S, the Arctic charr were categorized as either marine- or freshwater-dependent feeders. The use of time-integrated trophic tracers (stable isotopes of δ¹³C, δ¹⁵N, δ³⁴S) suggested that several trophic groups of Arctic charr operate alongside within each fjord system. The groups suggested were one group that specialized in the marine habitat, in addition to two freshwater resident morphs (small-sized resident and/or large-growing cannibalistic individuals). Stomach contents consisted entirely of freshwater and terrestrial prey (i.e., insects), indicating that marine-dependent feeders also fed in freshwater habitats after return from their marine migration. Growth and maturity patterns further supported variable life history strategies within each watercourse. The life history strategy patterns and marine trophic niche use were consistent across the watercourses along several hundred kilometres of coastline. This study represents the first ecological baseline for partially anadromous populations of Greenland Arctic charr.     

Evolution of adaptive diversity and genetic connectivity in Arctic charr (Salvelinus alpinus) in Iceland

The ecological theory of adaptive radiation predicts that the evolution of phenotypic diversity within species is generated by divergent natural selection arising from different environments and competition between species. Genetic connectivity among populations is likely also to have an important role in both the origin and maintenance of adaptive genetic diversity. Our goal was to evaluate the potential roles of genetic connectivity and natural selection in the maintenance of adaptive phenotypic differences among morphs of Arctic charr, Salvelinus alpinus, in Iceland. At a large spatial scale, we tested the predictive power of geographic structure and phenotypic variation for patterns of neutral genetic variation among populations throughout Iceland. At a smaller scale, we evaluated the genetic differentiation between two morphs in Lake Thingvallavatn relative to historically explicit, coalescent-based null models of the evolutionary history of these lineages. At the large spatial scale, populations are highly differentiated, but weakly structured, both geographically and with respect to patterns of phenotypic variation. At the intralacustrine scale, we observe modest genetic differentiation between two morphs, but this level of differentiation is nonetheless consistent with strong reproductive isolation throughout the Holocene. Rather than a result of the homogenizing effect of gene flow in a system at migration-drift equilibrium, the modest level of genetic differentiation could equally be a result of slow neutral divergence by drift in large populations. We conclude that contemporary and recent patterns of restricted gene flow have been highly conducive to the evolution and maintenance of adaptive genetic variation in Icelandic Arctic charr.     

Heterochrony in skeletal development and body size in progeny of two morphs of Arctic charr from Thingvallavatn, Iceland

Planktivorus Arctic charr had larger eggs than small benthivorous charr and the progeny of the former were longer (total length) at days 125, 145 and 159 after fertilization. Size differences remained significant after the removal of egg size effect on embryo size. Size of hybrid progeny tended to be similar to their maternal pure progeny group, suggesting maternal effects not directly related to yolk volume. In general, fin ray number increased faster in small benthivorous charr progeny than in planktivorous charr progeny, hybrid progeny tending to have intermediate fin ray numbers. The results indicate that morph differences in embryonic growth and skeletal development have a genetic and maternal component. Results support the hypothesis that in the period from hatching until just after first external feeding small benthivorous charr allocate more energy towards bone development, e.g. formation of fin rays, while planktivorous charr allocate more energy to body growth. The different developmental trajectories may reflect adaptations to discrete differences in habitats between the morphs.     

Phenotypic variation in growth trajectories in the Arctic charr Salvelinus alpinus

Animals with determinate growth have shown little variation in individual growth patterns, but similar analyses for animals with indeterminate growth have been lacking. We analysed the amount of phenotypic variation in growth patterns across ages among individuals of a hatchery-based population of Arctic charr, Salvelinus alpinus, Salmonidae, using the infinite-dimensional model and including the effects of group size structure. There was little phenotypic variation in growth trajectories: individuals that were small (in relation to the mean) early in life were among the smallest 2.5 years later. If the genetic variation reflects phenotypic variation, not much evolutionary change can be expected. Our results show that there are ecological conditions that determine the strong covariation of size across ages, most likely size-related dominance behaviour, which can mask the true variation of growth patterns. Thus, social interactions can have strong evolutionary effects on traits not directly involved in the behavioural interactions.     

Population structure, ecological segregation and reproduction in non-anadromous Arctic charr, Salvelinus alpinus (L), in four unexploited lakes in the Canadian high Arctic

Land-locked populations of Arctic charr in four lakes on Northern Ellesmere Island (80° N) were found to consist of two distinct sizes: 'dwarf' and 'normal' charr. Both groups attained sexual maturity but differed in appearance and habitat. The smaller fish, occupying the more marginal habitats, retained their parr-markings; the larger group had the general characteristics of smolts, being more silvery and without parr-marks. In their juvenile stages, the charr destined to attain the larger group were indistinguishable from members of the smaller group. Although fish in the larger group were capable of cannibalism, this was rarely observed. In general, the fish in the larger group were older than the smaller ones but great variation in size at a given age resulted in certain age classes containing representatives of both groups. The population structure varied considerably between lakes; a high proportion of 'normal' charr correlated well with a high growth rate in the first few years of development. It is postulated that the two groups live in dynamic equilibrium where the advantages of progenesis (retention of juvenile characters by adults) in the smaller type are traded against the larger proportion of the energy resources available to the larger type. The concept of heterochrony in an ecological setting is introduced.     

Variation in scale shape among alternative sympatric phenotypes of Arctic charr Salvelinus alpinus from two lakes in Scotland

Landmark‐based geometric morphometric analysis was used to detect differences in scale shape between ecologically distinct phenotypes of Arctic charr Salvelinus alpinus coexisting in the same lake. Relative warp analysis and standard multivariate analyses of the partial warps, obtained after a Procrustes superimposition, showed that scale landmarks were efficient in discriminating among two closely related alternative phenotypes within each of the two lakes. In Loch Tay, S. alpinus exhibited a bimodal body size‐frequency distribution among sexually mature fish, whereas in Loch Awe, S. alpinus are unimodal in body size but segregated into two distinct spawning phenotypes. In both lakes, alternative phenotypes showed significant differences in foraging ecology, habitat use and life history. It is probable that differences in scale shape reflect differences in ecology of these forms.     

Microprobe analyses of anadromous Arctic charr, Salvelinus alpinus, otoliths to infer life history migration events

Otoliths of Arctic charr, Salvelinus alpinus, from north Labrador were examined to gather life history information pertinent to anadromous migrations. Wavelength dispersive electron microprobe measurements confirm the presence of strontium in otolith tissue. Trace element analyses of charr otoliths imply that otolith strontium/calcium concentration ratios are related to external environmental factors with salinity having a great influence. Otoliths clearly record habitat shifts consistent with migration across major salinity boundaries. Most charr first migrate to sea following at least 2 years in freshwater. Generally, when anadromy begins, it continues annually. Robust relationships in otolith chemistry, combined with macrostructure patterns in field-captured specimens, provide time-series data describing individual migrational histories. Validation studies are still required in order to couple information contained within daily increments with chemical analyses to infer additional temporal events in diadromous migrations. Received: 6 November 1996 / Accepted: 18 May 1997     

Population genetic structure of Arctic charr, Salvelinus alpinus from northwest Europe on large and small spatial scales

To examine the population genetic structure of lake-resident Arctic charr, Salvelinus alpinus from northwest Europe on multiple spatial scales, 2367 individuals from 43 lakes located in three geographical regions (Iceland, the British Isles and Scandinavia) were genotyped at six microsatellite loci. On a large scale, data provided little evidence to support clustering of populations according to geographical region. Hierarchical analysis of molecular variance indicated that, although statistically significant, only 2.17% of the variance in allelic frequencies was partitioned at the among-region level. Within regions, high levels of genetic differentiation were typically found between lakes regardless of the geographical distance separating them. These results are consistent with the hypothesis of rapid postglacial recolonization of all of northwest Europe from a single charr lineage, with subsequent restriction of gene flow. On a smaller scale, there was evidence for close genetic relationships among lakes from within common drainage basins in Scotland. Thus, interlake genetic structure reflects localized patterns of recent (or contemporary) gene flow superimposed onto a larger scale structure that is largely a result of historical processes. There was also evidence for widespread genetic structuring at the within-lake level, with sympatric populations detected in 10 lakes, and multilocus heterozygote deficits found in 23 lakes. This evidence of the Wahlund effect was found in all lakes known to contain discrete phenotypic morphs, as well as many others, suggesting that morphs may often represent separate breeding populations, and also that the phenomenon of polymorphism in this species may be more widespread than is currently realized.     

Digestive capacities,inbreeding and growth capacities in juvenile Arctic charr Salvelinus alpinus

Genetic variation in growth performance was estimated in 26 families from two commercial strains of Arctic charr Salvelinus alpinus. Physiological determinants of growth and metabolic capacities were also assessed through enzymatic assays. A relatedness coefficient was attributed to each family using parental genotypes at seven microsatellite loci. After 15 months of growth, faster growing families had significantly lower relatedness coefficients than slower growing families, suggesting their value as indicators of growth potential. Individual fish that exhibited higher trypsin activity also displayed higher growth rate, suggesting that superior protein digestion capacities can be highly advantageous at early stages. Capacities to use amino acids as expressed by glutamate dehydrogenase (GDH) activities were lower in the liver of fast‐growing fish (13–20%), whereas white muscle of fast‐growing fish showed higher activities than that of slow‐growing fish for amino acid metabolism and aerobic capacity [22–32% increase for citrate synthase (CS), aspartate aminotransferase (AAT) and GDH]. The generally higher glycolytic capacities (PK and LDH) in white muscle of fast‐growing fish indicated higher burst swimming capacities and hence better access to food.     

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.     

Seasonal changes in hypoosmoregulatory ability in landlocked and anadromous populations of Arctic charr,Salvelinus alpinus,and Atlantic salmon,Salmo salar

Synopsis Seasonal changes in hypoosmoregulatory ability were compared in landlocked and anadromous strains of Arctic charr and Atlantic salmon. Seawater adaptability was assessed using periodic 48 h seawater challenge tests with 25. seawater. The landlocked strains of Arctic charr, two from northern Sweden and one from Southern Norway, displayed similar seasonal changes in seawater adaptability as the anadromous strain. Seawater tolerance increased during spring and remained high until the end of July — early August after which it declined. The two strains of Atlantic salmon displayed different seasonal patterns in hypoosmoregulatory ability. The anadromous strain showed a pronounced seasonal pattern with maximal seawater adaptability in early June. In contrast, seawater tolerance in the landlocked strain improved steadily during spring and remained high until late autumn. During the period of enhanced seawater tolerance, hypoosmoregulatory ability increased significantly with body size in both Arctic charr and anadromous Atlantic salmon. The minimum size at which fish were able to regulate plasma sodium following seawater transfer at a level comparable to freshwater levels (<170 mmol I^–1) differed significantly between anadromous Atlantic salmon (ca. 14 cm) and Arctic charr (ca. 22 cm). The results show that seasonal changes in hypoosmoregulatory ability are present in both Atlantic salmon and Arctic charr, and that these physiological traits are retained in the corresponding landlocked strains. However, the seasonal pattern of seawater adaptability as well as the minimum size at which seawater tolerance occurs differs between the two species.