Empirical evaluation of phenotype–environment correlation and trait utility with allopatric and sympatric whitefish, Coregonus lavaretus (L.), populations in subarctic lakes

Adaptive phenotypic divergence of sympatric morphs in a single species may have significant evolutionary consequences. In the present study, phenotypic impacts of predator on zooplankton prey populations were compared in two northern Finnish lakes; one with an allopatric whitefish, Coregonus lavaretus (L.), population and the other with three sympatric whitefish populations. First, we examined whether there were phenotypic associations with specific niches in allopatric and sympatric whitefish. Second, trait utility (i.e. number of gillrakers) of allopatric and sympatric whitefish in utilizing a pelagic resource was explored by comparing predator avoidance of prey, prey size in environment, and prey size in predator diet. The allopatric living large sparsely rakered (LSR) whitefish morph, was a generalist using both pelagic and benthic niches. In contrast, sympatric living whitefish morphs were specialized: LSR whitefish was a littoral benthivore, small sparsely rakered whitefish was a profundal benthivore and densely rakered (DR) whitefish was a pelagic planktivore. In the lake with allopatric whitefish, zooplankton prey did not migrate vertically to avoid predation whereas, in the lake with sympatric whitefish, all important prey taxa migrated significantly. Trait utility was observed as significantly smaller size of prey in environment and predator diet in the lake with DR whitefish than in the lake with only LSR whitefish.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 561–572.     

Seasonal movements and habitat use of river whitefish (Coregonus lavaretus) in the Koitajoki River (Finland), as determined by Carlin tagging and acoustic telemetry

In the Koitajoki River, Eastern Finland, there exists a self-sustaining population of river-spawning densely rakered whitefish (Coregonus lavaretus pallasi). The population has been classified as near-threatened due to overexploitation and possible hybridization with the lake-spawning sparsely rakered whitefish form. Thus, knowledge of habitat use, movements, and migrations is important for threat assessment and management decisions. We employed conventional tagging and acoustic telemetry to provide information on movements and home range of the Koitajoki River whitefish. We tagged mature individuals at their spawning areas and followed fish movements by tag recoveries and continuously recording fixed receiving stations. The maximum movement distances were 40–50?km both upstream and downstream from the releasing site. There were indications of a clear seasonal migration pattern and spawning-site fidelity; riverine habitats were mainly occupied for spawning and overwintering, while feeding and growth mainly took place in lacustrine environments within several lakes of the river system. Due to their migratory nature, whitefish is vulnerable to environmental disturbances and overfishing in a large geographic area.     

Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times

The extensive phenotypic polymorphism in the European whitefish has triggered evolutionary research in order to disentangle mechanisms underlying diversification. To illuminate the ecological distinctiveness in polymorphic whitefish, and evaluate taxonomic designations, we studied nine Norwegian lakes in three watercourses, which each harboured pairs of divergent whitefish morphs. We compared the morphology and life history of these morphs, documented the extent of genetic differentiation between them, and contrasted the niche use of sympatric morphs along both the habitat and resource axes. In all cases, sympatric morphs differed in the number of gill rakers, a highly heritable trait related to trophic utilization. Individual growth rate, age and size at maturity, diet and habitat use also differed between morphs within lakes, but were remarkably similar across lakes within the same morph. Microsatellite analyses confirmed for all but one pair that sympatric morphs were significantly genetically different, and that similar morphs from different lakes likely have a polyphyletic origin. These results are most compatible with the process of parallel evolution through recurrent postglacial divergence into pelagic and benthic niches in each of these lakes. We propose that sparsely and densely rakered whitefish sympatric pairs may be a likely case of ecological speciation, mediated in oligotrophic lakes with few trophic competitors.     

Morphological differentiation and resource polymorphism in three sympatric whitefish Coregonus lavaretus(L.) forms in a subarctic lake

Three field‐identified whitefish Coregonus lavaretus forms in Lake Muddusjärvi, Finland, were compared in morphology, diet and prey size. First, these forms were studied with univariate and multivariate analysis to assess morphological divergence at a higher resolution level than in the field. Second, stomach contents were analysed to estimate diet‐overlap among forms. Finally, the relationship between prey size and morphology was examined. The whitefish were assigned to the initial field‐classification with 99·2% and 98·8% accuracy for morphologic and meristic traits, respectively. The small sparsely‐rakered form (SSR) had the shortest rakers and largest gillraker space, followed by the large sparsely‐rakered form (LSR) with intermediate gillraker length and gillraker space, while densely‐rakered whitefish (DR) had the longest rakers and smallest gillraker space. The two sparsely‐rakered whitefish forms (LSR and SSR), consumed mainly benthic macroinvertebrates, while densely‐rakered whitefish (DR), utilized pelagic food items. Average diet‐overlaps between whitefish forms were low in June‐September (Schoener's α = 0·02 − 0·23). Gillraker number and length were negatively correlated to prey length in the diet ( r  = −0·73, and r  = −0·60), while gillraker space was positively correlated with prey length ( r  = 0·81). The fact that these whitefish forms were morphologically and ecologically segregated, and that gillraker traits probably have a functional value in food selection, further suggests that natural selection has been important in structuring life‐history trajectories into divergent niche use.     

Piscivory and prey selection of four predator species in a whitefish dominated subarctic lake

According to logistic regressions derived for pike Esox lucius and burbot Lota lota , the probability of ingesting fishes in Lake Muddusjärvi, northern Finland, was 50% at 19·3 and 22·1 cm L _T, whereas Arctic charr Salvelinus alpinus and brown trout Salmo trutta shifted to piscivory at the lengths of 25·7 and 26·4 cm L _T. The specialist piscivores, pike and burbot, consumed more prey species and took a wider range of prey sizes than Arctic charr and brown trout. The prey length for all predators increased in relationship to predator length. Whitefish Coregonus lavaretus was the dominant prey species in the lake and in the diet of all the piscivorous species. The whitefish population was divided into three forms, of which the slow-growing, and the most numerous densely rakered whitefish form (DR), was selected by all predator species. This form also had the smallest average size and widest habitat range, utilizing both pelagic and epibenthic habitats. Two sparsely rakered whitefish forms (LSR and SSR) occupied only epibenthic habitats and had lower relative densities than DR. These forms, LSR and SSR, had a minor importance in the diet of predator species.     

Histopathological characteristics of Coregonus fishes under the impact of metal industry

This article provides results from monitoring studies of the state of common whitefish (Coregonus lavaretus L.) inhabiting the border Pasvik River and a number of lakes of Northern Fennoskandia. The water catchment area is subject to a significant contamination by coper, nickel, and sulfur dioxide due to the airborne transport of emissions from the Pechenganikel smelter. The ecological situation near the smelter is evaluated as very unfavorable and requires constant control, including the monitoring of aquatic systems. We used histopathologies of gills, liver, and kidneys as biomarkers to diagnose the state of sparsely rakered whitefish. Changes in their cellular structure were diagnosed and classified. The presence of the revealed abnormalities is associated with long-term aerotechnogenic stress on the investigated water bodies. The possibility of using the obtained data for assessing water quality has been considered.     

Ongoing Speciation in the Tibetan Plateau Gymnocypris Species Complex

Local adaptation towards divergent ecological conditions often results in genetic differentiation and adaptive phenotypic divergence. To illuminate the ecological distinctiveness of the schizothoracine fish, we studied a Gymnocypris species complex consisting of three morphs distributed across four bodies of water (the Yellow River, Lake Qinghai, the Ganzi River and Lake Keluke) in the Northeast Tibetan Plateau. We used a combination of mitochondrial (16S rRNA and Cyt b) and nuclear (RAG-2) genetic sequences to investigate the phylogeography of these morphs based on a sample of 277 specimens. Analysis of gill rakers allowed for mapping of phenotypic trajectories along the phylogeny. The phylogenetic and morphological analyses showed that the three sparsely rakered morphs were present at two extremes of the phylogenetic tree: the Yellow River morphs were located at the basal phylogenetic split, and the Lake Keluke and Ganzi River morphs at the peak, with the densely rakered Lake Qinghai morphs located between these two extremes. Age estimation further indicated that the sparsely rakered morphs constituted the oldest and youngest lineages, whereas the densely rakered morph was assigned to an intermediate-age lineage. These results are most compatible with the process of evolutionary convergence or reversal. Disruptive natural selection due to divergent habitats and dietary preferences is likely the driving force behind the formation of new morphs, and the similarities between their phenotypes may be attributable to the similarities between their forms of niche tracking associated with food acquisition. This study provides the first genetic evidence for the occurrence of convergence or reversal in the schizothoracine fish of the Tibetan Plateau at small temporal scales.     

Acute effects on perch (Perca fluviatilis) and long-term effects on whitefish (Coregonus lavaretus pallasi) of liming of an acidified lake

The acute effects on perch and long‐term effects on whitefish were studied after liming one side of a lake [initial pH: 4.6–5.5; aluminium (Al): 29–54 μg L^?1; Ca²⁺: 0.02–0.07 mmol L^?1] that was divided into two parts with a plastic curtain. Some Al precipitation was observed on the gill surface of perch 1 day after liming; the concentration of plasma sodium of perch females in the limed side was also higher than in the acidic side. Nearly 6 months after liming, at the spawning time of whitefish, the plasma chloride concentration of whitefish in the limed side was higher and blood glucose concentration lower than in the acidic side. Four of five whitefish males from the limed side, but only one of five males and none of the five females from the acidic side, were ready to spawn. The growth of whitefish in the limed side was also more rapid. These changes illustrate that liming had no acute harmful effects on perch, and allowed whitefish to recover from acidity‐related physiological stress.     

Biology of round whitefish <Emphasis Type="Italic">Prosopium cylindraceum</Emphasis> (Coregonidae) of the Anadyr River

The recent state of the population of round whitefish Prosopium cylindraceum from the Anadyr River is described. Age composition of the catches of round whitefish remained almost without changes over the 35-year observation period. During this period, the proportion of large fishes (>380 mm in body length) slightly decreased, and the average body length of sexually mature individuals had become smaller. Possible reasons of interannual changes of the size-age composition of the catches and growth rate of the fish are discussed. A main factor determining growth variation of the fish is the abundance of chum salmon Oncorhynchus keta that migrated. The abundance of the round whitefish of the Anadyr River remains at a stable level (except the area of Markovo village) over a long time, and this population is hardly exploited.     

Diet, growth and competitive abilities of sympatric whitefish forms in a dense introduced population: results of a stocking experiment

The food of five whitefish stocks Coregonus lavaretus planted in Lake Vuokalanjärvi consisted mainly of zooplankton and insects taken from the water surface. The amount of benthic food in the diet of the two sparsely gill-rakered (23 and 28 rakers) stocks increased from the age of 2 years onwards. The growth of whitefish was slow in all stocks. The densely gill-rakered stock (50–51 rakers) originating from the same lake system as Lake Vuokalanjärvi grew faster than the other stocks, and the food consumption of 4- and 5-year-old fish belonging to this stock was nearly double compared with the other stocks. The habitat choice of the whitefish differed between the stocks even in the densely-rakered stocks classified as the same form. A stock with flexible habitat use and feeding habits is most likely to succeed. Introducing whitefish stocks from distant areas is not advisable.     

Ecological speciation in postglacial European whitefish: rapid adaptive radiations into the littoral,pelagic, and profundal lake habitats

Understanding how a monophyletic lineage of a species diverges into several adaptive forms has received increased attention in recent years, but the underlying mechanisms in this process are still under debate. Postglacial fishes are excellent model organisms for exploring this process, especially the initial stages of ecological speciation, as postglacial lakes represent replicated discrete environments with variation in available niches. Here, we combine data of niche utilization, trophic morphology, and 17 microsatellite loci to investigate the diversification process of three sympatric European whitefish morphs from three northern Fennoscandian lakes. The morphological divergence in the gill raker number among the whitefish morphs was related to the utilization of different trophic niches and was associated with reproductive isolation within and across lakes. The intralacustrine comparison of whitefish morphs showed that these systems represent two levels of adaptive divergence: (1) a consistent littoral–pelagic resource axis; and (2) a more variable littoral–profundal resource axis. The results also indicate that the profundal whitefish morph has diverged repeatedly from the ancestral littoral whitefish morph in sympatry in two different watercourses. In contrast, all the analyses performed revealed clustering of the pelagic whitefish morphs across lakes suggesting parallel postglacial immigration with the littoral whitefish morph into each lake. Finally, the analyses strongly suggested that the trophic adaptive trait, number of gill rakers, was under diversifying selection in the different whitefish morphs. Together, the results support a complex evolutionary scenario where ecological speciation acts, but where both allopatric (colonization history) and sympatric (within watercourse divergence) processes are involved.     

Different growth trends of whitefish (Coregonus lavaretus) forms in the northern Baltic Sea

The sea growth of two whitefish forms, anadromous (Coregonus lavaretus lavaretus) and sea‐spawning (Coregonus lavaretus widegreni), was analysed using samples collected from the commercial sea catch in the Gulf of Bothnia (GoB) in the northern Baltic Sea during 1998–2014. In the GoB area, these two forms are possible to identify because the gill‐raker number and size at maturity vary between forms. The growth rate of the forms is linked to their feeding area. Sea‐spawning whitefish, which has a feeding migration near its home site, was shorter in the northern GoB (66°N–64°N) at the ages of 3–11 than those in the southern GoB (64°N–60°30′N). In the data, most whitefish were caught with gill nets in the GoB. The mesh sizes of gill nets capturing the anadromous form were mostly 35–45 mm, while those capturing the sea‐spawning form were <35 mm in the northern GoB. It is likely that the different growth trends for small and large whitefish were connected with differences in their recruitment for fishing. The length of anadromous females at the age of four sea years increased significantly, but the length of six‐year‐old anadromous female whitefish decreased over the catch years from 1998–2014. In contrast, the length of slow‐growing sea‐spawning whitefish of six years or older increased significantly in relation to the catch year in the gill‐net catch. The increase in the growth of young age groups in both forms was probably associated with the increasing temperature and the low fishing pressure on small fish. The decreasing age at capture for both forms and the depression of the mean size of old anadromous whitefish are signs of high fishing pressure with a high gill‐net effort that selectively removes the largest and oldest individuals of both forms.     

MULTIPLE MODES OF SPECIATION INVOLVED IN THE PARALLEL EVOLUTION OF SYMPATRIC MORPHOTYPES OF LAKE WHITEFISH (COREGONUS CLUPEAFORMIS,SALMONIDAE)

We performed a phylogenetic analysis of mtDNA variation among seven sympatric pairs of dwarf and normal morphotypes of whitefish from northern Québec and the St. John River drainage to address three questions relevant to understanding their radiation. Are all sympatric pairs reproductively isolated? Do phylogenetic analyses confirm that sympatric whitefish morphotypes found in eastern North America represent the outcome of polyphyletic evolutionary events? If so, did all sympatric pairs from the St. John River drainage originate from the same scenario of allopatric divergence and secondary contact? The hypothesis of genetic differentiation was supported for all sympatric pairs from the St. John River drainage, whereas lack of mtDNA diversity precluded any test of reproductive isolation for northern Québec populations. Patterns of mtDNA variation confirmed that dwarf and normal morphotypes evolved in parallel among independent, yet closely related, lineages, thus providing indirect evidence for the role of natural selection in promoting phenotypic radiation in whitefish. Patterns of mtDNA diversity among sympatric pairs of the St. John River indicated a complex picture of whitefish evolution that implied sympatric divergence and multiple allopatric divergence/secondary contact events on a small geographic scale. These results suggests that ecological opportunities, namely trophic niche availability, may promote population divergence in whitefish.     

Genomic insights into the vulnerability of sympatric whitefish species flocks

The erosion of habitat heterogeneity can reduce species diversity directly but can also lead to the loss of distinctiveness of sympatric species through speciation reversal. We know little about changes in genomic differentiation during the early stages of these processes, which can be mediated by anthropogenic perturbation. Here, we analyse three sympatric whitefish species (Coregonus spp) sampled across two neighbouring and connected Swiss pre‐alpine lakes, which have been differentially affected by anthropogenic eutrophication. Our data set comprises 16,173 loci genotyped across 138 whitefish using restriction‐site associated DNA sequencing (RADseq). Our analysis suggests that in each of the two lakes, the population of a different, but ecologically similar, whitefish species declined following a recent period of eutrophication. Genomic signatures consistent with hybridization are more pronounced in the more severely impacted lake. Comparisons between sympatric pairs of whitefish species with contrasting ecology, where one is shallow benthic and the other one more profundal pelagic, reveal genomic differentiation that is largely correlated along the genome, while differentiation is uncorrelated between pairs of allopatric provenance with similar ecology. We identify four genomic loci that provide evidence of parallel divergent adaptation between the shallow benthic species and the two different more profundal species. Functional annotations available for two of those loci are consistent with divergent ecological adaptation. Our genomic analysis indicates the action of divergent natural selection between sympatric whitefish species in pre‐alpine lakes and reveals the vulnerability of these species to anthropogenic alterations of the environment and associated adaptive landscape.     

Fecundity of whitefish (Coregonus lavaretus) during the eu-and oligotrophication of Lake Constance

About 20 ovaries of the whitefish 'Blaufelchen' ( Coregonus lavaretus L.) of Lake Constance (Bodensee) were collected annually from 1964-1991. Absolute and relative fecundity peaked in the early 1980s, lagging about 2 years behind the maximum of total-P in the water (during the circulation period). Out of the biological time-series of Lake Constance, whitefish fecundity is the only one known to follow the phosphorus curve, and this may be the first time-series documented case of parallel trend reversal in the trophic state of a lake and fish biology. It is concluded that fish fecundity serves, at best, as an unspecific monitor of the overall well-being of the fish.     

CORRELATED TROPHIC SPECIALIZATION AND GENETIC DIVERGENCE IN SYMPATRIC LAKE WHITEFISH ECOTYPES (COREGONUS CLUPEAFORMIS): SUPPORT FOR THE ECOLOGICAL SPECIATION HYPOTHESIS

There is ample empirical evidence that phenotypic diversification in an adaptive radiation is the outcome of divergent natural selection related to differential resource use. In contrast, the role of ecological forces in favoring and maintaining reproductive isolation in nature remains poorly understood. If the same forces driving phenotypic divergence are also responsible for speciation, one would predict a correlation between the extent of trophic specialization (reflecting variable intensity of divergent natural selection) and that of reproductive isolation being reached in a given environment. We tested this hypothesis by comparing the extent of morphological and genetic differentiation between sympatric dwarf and normal whitefish ecotypes (Coregonus sp.) from six lakes of the St. John River basin (eastern Canada and northern Maine). Eight meristic variables, 19 morphometric variables, and six microsatellite loci were used to quantify morphological and genetic differentiation, respectively. Dwarf and normal ecotypes in each lake differed primarily by traits related to trophic specialization, but the extent of differentiation varied among lakes. Significant but variable genetic divergence between ecotypes within lakes was also observed. A negative correlation was observed between the extent of gene flow between ecotypes within a lake and that of their morphological differentiation in trophic-related traits. The extent of reproductive isolation reached between dwarf and normal whitefish ecotypes appears to be driven by the potential for occupying distinct trophic niches and, thus, by the same selective forces driving tropic specialization in each lake. These results therefore support the hypothesis of ecological speciation.     

Parallelism in the oxygen transport system of the lake whitefish: the role of physiological divergence in ecological speciation

In North America, populations of lake whitefish (Coregonus clupeaformis) have evolved sympatric 'dwarf' and 'normal' ecotypes that are associated with distinct trophic niches within lakes. Trophic specialization should place diverging physiological demands on individuals, and thus, genes and phenotypes associated with energy production represent ideal candidates for studies of adaptation. Here, we test for the parallel divergence of traits involved in oxygen transport in dwarf and normal lake whitefish from Québec, Canada and Maine, USA. We observed significant differences in red blood cell morphology between the ecotypes. Specifically, dwarfs exhibited larger nuclei and a higher nucleus area/total cell area than normal whitefish in all of the lakes examined. In addition, isoelectric focusing gels revealed variation in the haemoglobin protein components found in whitefish. Dwarf and normal whitefish exhibited a similar number of protein components, but the composition of these components differed, with dwarf whitefish bearing a greater proportion of cathodic components compared to the normals. Furthermore, dwarf whitefish showed significant haemoglobin gene upregulation in the brain compared with the levels shown in normals. Together, our results indicate that metabolic traits involved in oxygen transport differ between the whitefish ecotypes and the strong parallel patterns of divergence observed across lakes implicates ecologically driven selection pressures. We discuss the function of these traits in relation to the differing trophic niches occupied by the whitefish and the potential contributions of trait plasticity and genetic divergence to energetic adaptation.     

Physiological stress response of Mountain Whitefish (<Emphasis Type="Italic">Prosopium williamsoni</Emphasis>) and White Sucker (<Emphasis Type="Italic">Catostomus commersoni)</Emphasis> sampled along a gradient of temperature and agrichemicals in the Oldman River,Alberta

Species differences in tolerance to environmental stressors can contribute to differences in species distribution and abundance along river gradients. Climate change and intensive agriculture are likely to have major effects on fish populations in temperate zones, yet understanding of the interactions between temperature and chemical stressors on fish physiology is limited. The objective of this study was to compare the stress responses of the Mountain Whitefish, (Prosopium williamsoni, a cold-water fish) and White Sucker (Catostomus commersoni, a cool-water fish), along a temperature and pesticide gradient in the Oldman River, Southern Alberta in spring and summer. Fish were seined, placed into an enclosure, and plasma cortisol, glucose, liver glycogen, and condition factor were measured. Plasma acetylcholinesterase (AChE) activity was used as an indicator of exposure to organophosphate and carbamates pesticides. Whitefish had lower plasma AChE activity and lower liver glycogen reserves compared to suckers at all sites and all sampling times but the differences in plasma cortisol were not species-specific and there were no differences in plasma glucose levels, except at one site. Plasma cortisol increased, and plasma glucose decreased along a downstream river gradient in whitefish in both spring and summer; in sucker only plasma cortisol fluctuated and only in the summer. Liver glycogen decreased along the river gradient in both species at both seasons. Our study detected important species-specific differences in AChE activities and responses of the physiological stress axis, suggesting that whitefish are more sensitive to temperature and pesticide stress than suckers.     

The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp. Salmonidae) species pairs

Adaptive evolutionary change is contingent on variation and selection; thus, understanding adaptive divergence and ultimately speciation requires information on both the genetic basis of adaptive traits as well as an understanding of the role of divergent natural selection on those traits. The lake whitefish (Coregonus clupeaformis) consists of several sympatric "dwarf" (limnetic) and normal (benthic) species pairs that co-inhabit northern postglacial lakes. These young species pairs have evolved independently and display parallelism in life history, behavioral, and morphological divergence associated with the use of distinct trophic resources. We identified phenotype-environment associations and determined the genetic architecture and the role of selection modulating population genetic divergence in sympatric dwarf and normal lake whitefish. The genetic architecture of 9 adaptive traits was analyzed in 2 hybrid backcrosses individually phenotyped throughout their life history. Significant quantitative trait loci (QTL) were associated with swimming behavior (habitat selection and predator avoidance), growth rate, morphology (condition factor and gill rakers), and life history (onset of maturity and fecundity). Genome scans among 4 natural sympatric pairs, using loci segregating in the map, revealed a signature of selection for 24 loci. Loci exhibiting a signature of selection were associated with QTL relative to other regions of the genome more often than expected by chance alone. Two parallel QTL outliers for growth and condition factor exhibited segregation distortion in both mapping families, supporting the hypothesis that adaptive divergence contributing to parallel reductions of gene flow among natural populations may cause genetic incompatibilities. Overall, these findings offer evidence that the genetic architecture of ecological speciation is associated with signatures of selection in nature, providing strong support for the hypothesis that divergent natural selection is currently maintaining adaptive differentiation and promoting ecological speciation in lake whitefish species pairs.     

Using the δ13C and δ15N of whitefish scales for retrospective ecological studies: changes in isotope signatures during the restoration of Lake Geneva, 1980–2001

The scales of whitefish Coregonus lavaretus were used in place of dorsal muscle, which necessitates killing the fish, to study food webs from the δ¹³C and δ¹⁵N isotopic ratios in the organic fraction. As scales are composed of both organic and calcified fractions, a protocol for scale decalcification was first devised. The δ¹³C and δ¹⁵N values of the decalcified scales were then shown to be closely correlated to those of the dorsal muscle, demonstrating that scales could be used in place of muscle to study food webs. Changes in the δ¹³C of whitefish were determined from a scale collection that extended over the period during which the trophic state of Lake Geneva was recovering.