Allopatric origin of sympatric whitefish morphs with insights on the genetic basis of their reproductive isolation

The European whitefish (Coregonus lavaretus) species complex is a classic example of recent adaptive radiation. Here, we examine a whitefish population introduced to northern Finnish Lake Tsahkal in the late 1960s, where three divergent morphs (viz. littoral, pelagic, and profundal feeders) were found 10 generations after. Using demographic modeling based on genomic data, we show that whitefish morphs evolved during a phase of strict isolation, refuting a rapid sympatric divergence scenario. The lake is now an artificial hybrid zone between morphs originated in allopatry. Despite their current syntopy, clear genetic differentiation remains between two of the three morphs. Using admixture mapping, we identify five SNPs associated with gonad weight variation, a proxy for sexual maturity and spawning time. We suggest that ecological adaptations in spawning time evolved in allopatry are currently maintaining partial reproductive isolation in the absence of other barriers to gene flow.Peer reviewe

Ecological speciation in a generalist consumer expands the trophic niche of a dominant predator

Ecological speciation - whereby an ancestral founder species diversifies to fill vacant niches - is a phenomenon characteristic of newly formed ecosystems. Despite such ubiquity, ecosystem-level effects of such divergence remain poorly understood. Here, we compared the trophic niche of European whitefish (Coregonus lavaretus) and their predators in a series of contrasting subarctic lakes where this species had either diversified into four ecomorphologically distinct morphs or instead formed monomorphic populations. We found that the trophic niche of whitefish was almost three times larger in the polymorphic than in the monomorphic lakes, due to an increase in intraspecific specialisation. This trophic niche expansion was mirrored in brown trout (Salmo trutta), a major predator of whitefish. This represents amongst the first evidence for ecological speciation directly altering the trophic niche of a predator. We suggest such mechanisms may be a common and important - though presently overlooked - factor regulating trophic interactions in diverse ecosystems globally.Peer reviewe

A brain and a head for a different habitat : Size variation in four morphs of Arctic charr (Salvelinus alpinus(L.)) in a deep oligotrophic lake

Adaptive radiation is the diversification of species to different ecological niches and has repeatedly occurred in different salmonid fish of postglacial lakes. In Lake Tinnsjoen, one of the largest and deepest lakes in Norway, the salmonid fish, Arctic charr (Salvelinus alpinus(L.)), has likely radiated within 9,700 years after deglaciation into ecologically and genetically segregated Piscivore, Planktivore, Dwarf, and Abyssal morphs in the pelagial, littoral, shallow-moderate profundal, and deep-profundal habitats. We compared trait variation in the size of the head, the eye and olfactory organs, as well as the volumes of five brain regions of these four Arctic charr morphs. We hypothesised that specific habitat characteristics have promoted divergent body, head, and brain sizes related to utilized depth differing in environmental constraints (e.g., light, oxygen, pressure, temperature, and food quality). The most important ecomorphological variables differentiating morphs were eye area, habitat, and number of lamellae. The Abyssal morph living in the deepest areas of the lake had the smallest brain region volumes, head, and eye size. Comparing the olfactory bulb with the optic tectum in size, it was larger in the Abyssal morph than in the Piscivore morph. The Piscivore and Planktivore morphs that use more illuminated habitats have the largest optic tectum volume, followed by the Dwarf. The observed differences in body size and sensory capacities in terms of vision and olfaction in shallow and deepwater morphs likely relates to foraging and mating habitats in Lake Tinnsjoen. Further seasonal and experimental studies of brain volume in polymorphic species are needed to test the role of plasticity and adaptive evolution behind the observed differences.Peer reviewe

Total mercury concentrations in liver and muscle of European whitefish (Coregonus lavaretus (L.)) in a subarctic lake - Assessing the factors driving year-round variation

Subarctic lakes are characterised by extreme seasonal variation in light and temperature which influences growth, maturation, condition and resource use of fishes. However, our understanding of how seasonal changes affect mercury concentrations of fishes is limited. We conducted a year-round study (3 ice-covered months, 3 open-water months) with open-water inter-annual aspect (3 years: samples from August/September), focusing on total mercury (THg) concentrations and ecological characteristics of a common freshwater fish, European whitefish (Coregonus lavaretus (L.)) from a subarctic lake. We measured THg concentrations from tissues with fast (liver, n = 164) and moderate (muscle, n = 225) turnover rates, providing information on THg dynamics over different temporal scales. In both tissues, lipid-corrected THg concentrations were highest in winter (liver: 1.70 +/- 0.88 mu g/g, muscle: 0.24 +/- 0.05 mu g/g) and lowest in summer (liver: 0.87 +/- 0.72 mu g/g, muscle: 0.19 +/- 0.04 mu g/g). THg concentrations increased in winter following the summer-autumn dietary shift to pelagic zooplankton and starvation after spawning. Whitefish THg concentrations decreased towards summer, and were associated with consumption of benthic macroinvertebrates and subsequent growth dilution. Mercury bio-accumulated in both tissues with age, both showing the strongest regression slopes in winter and lowest in summer. THg concentrations in liver and muscle tissue were correlated throughout the year, however the correlation was lowest in summer, indicating high metabolism during somatic growing season in summer and growth dilution. Multiple linear regression models explained 50% and 55% of the THg variation in liver and muscle both models dominated by seasonally-variable factors i.e. sexual maturity, delta C-13, and condition factor. Seasonally varying bioaccumulation slopes and the higher level of intra-annual variation (21%) in whitefish THg concentration in muscle than the inter-annual accumulation (8%) highlight the importance of including seasonal factors in future THg studies. (C) 2017 Elsevier Ltd. All rights reserved.Peer reviewe

Using mathematical modelling to investigate the adaptive divergence of whitefish in Fennoscandia

Modern speciation theory has greatly benefited from a variety of simple mathematical models focusing on the conditions and patterns of speciation and diversification in the presence of gene flow. Unfortunately the application of general theoretical concepts and tools to specific ecological systems remains a challenge. Here we apply modeling tools to better understand adaptive divergence of whitefish during the postglacial period in lakes of northern Fennoscandia. These lakes harbor up to three different morphs associated with the three major lake habitats: littoral, pelagic, and profundal. Using large-scale individual-based simulations, we aim to identify factors required for in situ emergence of the pelagic and profundal morphs in lakes initially colonized by the littoral morph. The importance of some of the factors we identify and study - sufficiently large levels of initial genetic variation, size- and habitat-specific mating, sufficiently large carrying capacity of the new niche - is already well recognized. In addition, our model also points to two other factors that have been largely disregarded in theoretical studies: fitness-dependent dispersal and strong predation in the ancestral niche coupled with the lack of it in the new niche(s). We use our theoretical results to speculate about the process of diversification of whitefish in Fennoscandia and to identify potentially profitable directions for future empirical research.Peer reviewe

Resource use of crucian carp along a lake productivity gradient is related to body size, predation risk, and resource competition

Generalist fish species can feed on a wide resource spectrum and across trophic levels depending on resource availability and trophic interactions. Crucian carp (Carassius carassius) represents a good candidate species to investigate variation in the trophic ecology of generalist fish as it can be found in highly variable fish communities and its resource use is well documented. In this study, we explored the trophic ecology of crucian carp at the individual and population levels using stable isotope and gut content analysis. We tested if trophic resource use varied according to lake productivity, predation risk, intra- and interspecific competition, or individual fish size. We found that crucian carp resource preference was highly variable among and within lakes. In predator-free lakes, small crucian carp occurred in high densities, showed increased interindividual specialisation, and relied mainly on pelagic zooplankton. In presence of predators, large crucian carp occurred in low densities and included greater proportions of benthic macroinvertebrates in their diet. This shift in resource use was further favoured in productive, shallow lakes where littoral prey were probably abundant. Resource partitioning was an important factor determining crucian carp niche use, as fish had higher trophic position in absence of other cyprinids. Crucian carp showed highly dynamic resource use and food preferences in response to variable environmental conditions. Overlooking complex diet preferences of generalist fish may lead to an oversimplification of freshwater community dynamics.Peer reviewe

Genetic Variability and Structuring of Arctic Charr (Salvelinus alpinus) Populations in Northern Fennoscandia

Variation in presumably neutral genetic markers can inform us about evolvability, historical effective population sizes and phylogeographic history of contemporary populations. We studied genetic variability in 15 microsatellite loci in six native landlocked Arctic charr (Salvelinus alpinus) populations in northern Fennoscandia, where this species is considered near threatened. We discovered that all populations were genetically highly (mean F-ST approximate to 0.26) differentiated and isolated from each other. Evidence was found for historical, but not for recent population size bottlenecks. Estimates of contemporary effective population size (N-e) ranged from seven to 228 and were significantly correlated with those of historical N-e but not with lake size. A census size (N-C) was estimated to be approximately 300 individuals in a pond (0.14 ha), which exhibited the smallest N-e (i.e. N-e/N-C = 0.02). Genetic variability in this pond and a connected lake is severely reduced, and both genetic and empirical estimates of migration rates indicate a lack of gene flow between them. Hence, albeit currently thriving, some northern Fennoscandian populations appear to be vulnerable to further loss of genetic variability and are likely to have limited capacity to adapt if selection pressures change.Peer reviewe

Ecomorphological divergence drives differential mercury bioaccumulation in polymorphic European whitefish (Coregonus lavaretus) populations of subarctic lakes

Resource polymorphism, whereby ancestral trophic generalists undergo divergence into multiple specialist morphs, is common in salmonid fish populations inhabiting subarctic lakes. However, the extent to which such resource specialization into the three principal lake habitats (littoral, profundal, and pelagic) affects patterns of contaminant bioaccumulation remains largely unexplored. We assessed total mercury concentrations (THg) of European whitefish (Coregonus lavaretus (L)) and their invertebrate prey in relation to potential explanatory variables across 6 subarctic lakes, of which three are inhabited by polymorphic (comprised of four morphs) and three by monomorphic populations. Among invertebrate prey, the highest THg concentrations were observed in profundal benthic macroinvertebrates, followed by pelagic zooplankton, with concentrations lowest in littoral benthic macroinvertebrates in both lake types. Broadly similar patterns were apparent in whitefish in polymorphic systems, where average age-corrected THg concentrations and bioaccumulation rates were the highest in pelagic morphs, intermediate in the profundal morph, and the lowest in the littoral morph. In monomorphic systems, age-corrected THg concentrations were generally lower, and showed pronounced lake-specific variation. In the polymorphic systems, we found significant relationships between whitefish muscle tissue THg concentration and gill raker count, resource use, lipid content and maximum length, whilst no such relationships were apparent in the monomorphic systems. Across all polymorphic lakes, the major variables explaining THg in whitefish were gill raker count and age, whereas in monomorphic systems, the factors were lake-specific. Whitefish resource polymorphism across the three main lake habitats therefore appears to have profound impacts on THg concentration and bioaccumulation rate. This highlights the importance of recognizing such intraspecific diversity in both future scientific studies and mercury monitoring programs. (C) 2017 Elsevier B.V. All rights reserved.Peer reviewe

High Mercury Concentrations of European Perch (Perca fluviatilis) in Boreal Headwater Lakes with Variable History of Acidification and Recovery

High dissolved organic carbon and low pH are often associated with elevated mercury content of fish in boreal lakes, but less is known about the fish mercury dynamics in lakes recovering from acidification stress. We measured total mercury concentration (THg) in muscle of European perch (Perca fluviatilis) and evaluated the overall correlation with environmental and growth variables in 24 boreal headwater lakes in the 2010s. We found negative correlations of length-corrected perch THg with lake pH and perch growth, but no correlation with dissolved organic carbon. The main emphasis in the present study was focused to a subset of ten lakes in southern Finland with known perch THg during severe acidification in the 1980-1990s. The comparison of perch THg concentrations in the 2010s with values determined in the 1980-1990s showed a sharp increase in most acidic lakes where the perch populations suffered from severe acid stress in the 1980s. This increase was attributed to growth condensation caused by sharp decrease in perch growth during recovery of reproduction capacity and the consequent increases in population densities of perch. Our results highlight the importance of perch growth rate and population density for understanding the variability of fish Hg in boreal headwater lakes, where recovery from acidification can lead to higher mercury concentration of fish in certain cases.Peer reviewe

Terrestrial carbohydrates support freshwater zooplankton during phytoplankton deficiency

Freshwater food webs can be partly supported by terrestrial primary production, often deriving from plant litter of surrounding catchment vegetation. Although consisting mainly of poorly bioavailable lignin, with low protein and lipid content, the carbohydrates from fallen tree leaves and shoreline vegetation may be utilized by aquatic consumers. Here we show that during phytoplankton deficiency, zooplankton (Daphnia magna) can benefit from terrestrial particulate organic matter by using terrestrial-origin carbohydrates for energy and sparing essential fatty acids and amino acids for somatic growth and reproduction. Assimilated terrestrial-origin fatty acids from shoreline reed particles exceeded available diet, indicating that Daphnia may convert a part of their dietary carbohydrates to saturated fatty acids. This conversion was not observed with birch leaf diets, which had lower carbohydrate content. Subsequent analysis of 21 boreal and subarctic lakes showed that diet of herbivorous zooplankton is mainly based on high-quality phytoplankton rich in essential polyunsaturated fatty acids. The proportion of low-quality diets (bacteria and terrestrial particulate organic matter) was <28% of the assimilated carbon. Taken collectively, the incorporation of terrestrial carbon into zooplankton was not directly related to the concentration of terrestrial organic matter in experiments or lakes, but rather to the low availability of phytoplankton.Peer reviewe