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

Polyunsaturated fatty acids in fishes increase with total lipids irrespective of feeding sources and trophic position

Trophic transfer and retention of dietary compounds are vital for somatic development, reproduction, and survival of aquatic consumers. In this field study, stable carbon and nitrogen isotopes, and fatty acids (FA) contents in invertebrates and fishes of pre-alpine Lake Lunz, Austria, were used to (1) identify the resource use and trophic level of Arctic charr (Salvelinus alpinus), pike (Esox lucius), perch (Perca fluviatilis), brown trout (Salmo trutta), roach (Rutilus rutilus), and minnow (Phoxinus phoxinus) and (2) examine how polyunsaturated fatty acids (PUFA; i.e., omega-3 and -6 PUFA) are related to total lipid status, littoral-pelagic reliance, and trophic position. Stable isotope data suggest that pike, perch, and minnow derived most of their energy from littoral resources, but minnows differed from pike and perch in their trophic position and PUFA composition. The co-occurrence of cyprinids, percids, and pike segregated these fishes into more lipid-rich (roach, minnow) and lipid-poor (pike, percids) species. Although the relatively lipid-poor pike and percids occupied a higher trophic position than cyprinids, there was a concurrent, total lipid-dependent decline in omega-3 and -6 PUFA in these predatory fishes. Results of this lake food-web study demonstrated that total lipids in fish community, littoral-pelagic reliance, and trophic position explained omega-3 and -6 PUFA in dorsal muscle tissues. Omega-3 and -6 PUFA in these fishes decreased with increasing trophic position, demonstrating that these essential FAs did not biomagnify with increasing trophic level. Finally, this lake food-web study provides evidence of fish community-level relationship between total lipid status and PUFA or stable isotope ratios, whereas the strength of such relationships was less strong at the species level.Peer reviewe

Trophic ecology of piscivorous Arctic charr (Salvelinus alpinus (L.)) in subarctic lakes with contrasting food-web structures

The trophic ecology of piscivorous Arctic charr (Salvelinus alpinus (L.); charr) in the food webs of large subarctic lakes is not well understood. We assessed charr diets, parasites, growth, maturity, and stable isotope ratios in Fennoscandian subarctic lakes dominated by monomorphic or polymorphic whitefish (Coregonus lavaretus (L.)) populations. Charr density was low in all lakes, except in profundal habitats. Charr shifted to piscivory at small size (16-25 cm total length) and consumed a range of prey-fish sizes (2-25 cm). Cannibalism was observed in a few individuals from one monomorphic whitefish lake. Charr matured at 37-51 cm (5-8 years old), grew to 52-74 cm maximum observed length and 47-83 cm asymptotic length. Charr increased total area of convex hull and core stable isotopic diversity area of the fish community by 51-98% and 44-51% in monomorphic whitefish lakes, but only 8-11% and 7-10% in polymorphic whitefish lakes. The difference was due to increasing food-chain length in monomorphic whitefish lakes, whereas reliance on littoral carbon did not change. Charr were the top piscivores in monomorphic whitefish lakes, but played a less important role in polymorphic whitefish lakes, which contained a more diverse predator fauna.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

Lake eutrophication and brownification downgrade availability and transfer of essential fatty acids for human consumption

Fish are an important source of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) for birds, mammals and humans. In aquatic food webs, these highly unsaturated fatty acids (HUFA) are essential for many physiological processes and mainly synthetized by distinct phytoplankton taxa. Consumers at different trophic levels obtain essential fatty acids from their diet because they cannot produce these sufficiently de novo. Here, we evaluated how the increase in phosphorus concentration (eutrophication) or terrestrial organic matter inputs (brownification) change EPA and DHA content in the phytoplankton. Then, we evaluated whether these changes can be seen in the EPA and DHA content of piscivorous European perch (Perca fluviatilis), which is a widely distributed species and commonly consumed by humans. Data from 713 lakes showed statistically significant differences in the abundance of EPA- and DHA-synthesizing phytoplankton as well as in the concentrations and content of these essential fatty acids among oligo-mesotrophic, eutrophic and dystrophic lakes. The EPA and DHA content of phytoplankton biomass (mg HUFA g(-1)) was significantly lower in the eutrophic lakes than in the oligo-mesotrophic or dystrophic lakes. We found a strong significant correlation between the DHA content in the muscle of piscivorous perch and phytoplankton DHA content (r = 0.85) as well with the contribution of DHA-synthesizing phytoplankton taxa (r = 0.83). Among all DHA-synthesizing phytoplankton this correlation was the strongest with the dinoflagellates (r = 0.74) and chrysophytes (r = 0.70). Accordingly, the EPA + DHA content of perch muscle decreased with increasing total phosphorus (r(2) = 0.80) and dissolved organic carbon concentration (r(2) = 0.83) in the lakes. Our results suggest that although eutrophication generally increase biomass production across different trophic levels, the high proportion of low-quality primary producers reduce EPA and DHA content in the food web up to predatory fish. Ultimately, it seems that lake eutrophication and brownification decrease the nutritional quality of fish for human consumers. (C) 2016 The Authors. Published by Elsevier Ltd.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

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

From clear lakes to murky waters - tracing the functional response of high-latitude lake communities to concurrent 'greening' and 'browning'

Climate change and the intensification of land use practices are causing widespread eutrophication of subarctic lakes. The implications of this rapid change for lake ecosystem function remain poorly understood. To assess how freshwater communities respond to such profound changes in their habitat and resource availability, we conducted a space-for-time analysis of food-web structure in 30 lakes situated across a temperature-productivity gradient equivalent to the predicted future climate of subarctic Europe (temperature +3 degrees C, precipitation +30% and nutrient +45 mu g L-1 total phosphorus). Along this gradient, we observed an increase in the assimilation of pelagic-derived carbon from 25 to 75% throughout primary, secondary and tertiary consumers. This shift was overwhelmingly driven by the consumption of pelagic detritus by benthic primary consumers and was not accompanied by increased pelagic foraging by higher trophic level consumers. Our data also revealed a convergence of the carbon isotope ratios of pelagic and benthic food web endmembers in the warmest, most productive lakes indicating that the incorporation of terrestrial derived carbon into aquatic food webs increases as land use intensifies. These results, reflecting changes along a gradient characteristic of the predicted future environment throughout the subarctic, indicate that climate and land use driven eutrophication and browning are radically altering the function and fuelling of aquatic food webs in this biome.Peer reviewe