Lake Kronotskoe Research Articles

Phylogenomic analysis of the Lake Kronotskoe species flock of Dolly Varden charr reveals genetic and developmental signatures of sympatric radiation.

Recent adaptive radiations provide experimental opportunities to parse the relationship between genomic variation and the origins of distinct phenotypes. Sympatric radiations of the charr complex (genus Salvelinus) present a trove for phylogenetic analyses as charrs have repeatedly diversified into multiple morphs with distinct feeding specializations. However, charr species flocks normally comprise only two to three lineages. Dolly Varden charr inhabiting Lake Kronotskoe represent the most extensive radiation described for the genus, containing at least seven lineages, each with defining morphological and ecological traits. Here, we perform the first genome-wide analysis of this species flock to parse the foundations of adaptive change. Our data support distinct, reproductively isolated lineages within the clade. We find that changes in genes associated with thyroid signaling and craniofacial development provided a foundational shift in evolution to the lake. The thyroid axis is further implicated in subsequent lineage partitioning events. These results delineate a genetic scenario for the diversification of specialized lineages and highlight a common axis of change biasing the generation of specific forms during adaptive radiation.

Patterns of Ecological Specialisation Among Multiple Piscivorous Morphs of a Diverse Assemblage of Salvelinus Fishes

ABSTRACTAdaptive radiation is considered to be a major source of biodiversity in charrs of the genus Salvelinus. These fishes demonstrate numerous examples of diversification in postglacial lakes and rivers resulting in the emergence of different ecomorphs, including piscivorous. Usually, the number of fish feeders does not exceed two, suggesting the existence of ecological and/or internal factors that prevent further diversification. Under these circumstances, rare instances of increases in the number of piscivorous morphs are of particular interest. Here, we present a comprehensive study of the piscivorous charr assemblage in Lake Kronotskoe, residence of the most diverse species flock of Salvelinus fishes. To unravel the diversity and ecological relationships of piscivorous charrs, we analysed their morphology and microsatellite DNA polymorphism, distribution within the lake, trophic preferences and parasite load, as well as trace element accumulation, stable isotope and free fatty acid ratios. We revealed that, apart from a few strictly benthivorous morphs, the lake is inhabited by four closely related but morphologically and genetically distinct morphs that exhibit a range of piscivorous specialisation: from opportunistic secondary predation to ultra‐specialised primary piscivory. They effectively exploit the spatiotemporal structure of the ecosystem and experience diversifying selection due to niche discordance. Each piscivorous morph develops specific phenotypic, ecological and life history traits that allow it to terminate weakly overlapping branches of the trophic chain and share the energy flows of the lake ecosystem. Our data suggest that Lake Kronotskoe facilitates high level of ecological opportunity that favours niche expansion and allows the piscivorous lineage to simultaneously realise the archetypical modes of ecological diversification available to fishes in cold‐water freshwaters.

DNA Identification of Parasitic Copepods <i>Salmincola</i> (Copepoda, Siphonostomatoida, Lernaeopodidae): Variability and Rate of Evolution of the Mitochondrial Cytochrome c Oxidase Subunit I Gene

The barcode fragment of the COI gene was sequenced in 91 specimens of five species of parasitic Salmincola copepods, sampled from salmonids mainly from the Russian Far East: S. californiensis (mykiss and masu salmon) and S. edwardsii (various species of chars, sockeye salmon from Lake Kronotskoe), S. carpionis (various species of chars), S. markewitschi (whitespotted char), S. stellata (Sakhalin taimen). A total of 41 haplotypes were found with a maximum level of differences of 0.183 nucleotide substitutions per position. The distance between species varied from 0.139 ± 0.014 in the S. markewitschi–S. carpionis pair to 0.179 ± 0.015 in the S. stellata–S. californiensis pair. The intraspecific nucleotide diversity of the COI gene fragment is much lower: for S. californiensis and S. edwardsii, inhabiting the gill cavity and fins of the host – 0.013 ± 0.003 and 0.015 ± 0.003, and for S. stellata, S. markewitschi, and S. carpionis, localized in the buccal cavity of the hosts – 0.002 ± 0.001, 0.004 ± 0.001, and 0.005 ± 0.001, respectively. A comparison of samples of three Salmincola copepod species from different regions of the Russian Far East revealed a significant (Fst = 0.28–0.42, P \( \ll \) 0.001) genetic subdivision. Three subclades of edwardsii-like copepods – S. edwardsii from the Russian Far East, S. edwardsii from the American brook char of eastern North America, and S. siscowet from the lake char of Michigan (COI sequences of copepods from the last two groups are taken from genetic databases) – differed from each other by an average of 9.3–10.9% nucleotide positions, which means the need for a taxonomic revision of S. edwardsii. According to the molecular dating carried out, the divergence of Salmincola lineages started in the Miocene and ended in the early Pliocene. The phylogenetic substitution rate was 0.0228 (95% interval: 0.0132–0.033) nucleotide substitutions/position/million years/lineage. The rate of nucleotide substitutions at the population level is 3.7 times higher – 0.0849 (0.0212–0.170). The high level of variability of the COI gene fragment makes this marker a useful tool both for developing the taxonomy and phylogeny of Salmincola and Lernaeopodidae copepods at the species and genus levels, and for analyzing the differentiation of their populations.

The Ratio of Leukocytes in Peripheral Blood and Immunocompetent Organs of Chars of the Genus Salvelinus (Salmonidae) in the Lake Kronotskoe Basin

The cellular composition of leukocytes in the peripheral blood, head kidney and spleen was studied in individuals of three species of chars of the genus Salvelinus, white char S. albus, long–headed char S. kronocius and long-nosed char S. schmidti, as well as two forms, small-mouth and large-mouth chars living in Lake Kronotskoe. In the studied individuals, the proportion of lymphocytes of leukocytes in the peripheral blood was significant. The forms (species) of chars differed in the proportion of cell types, the size of leukocytes, as well as the intensity of leukopoiesis. The most significant differences in the proportion of different forms of leukocytes were found in the large-mouth char compared to other species and small–mouth char: high content of lymphocytes in blood smears, low content of monocytes in all tissues and organs, blast forms in the blood and neutrophils in the pronephros.

Oxidation Processes and the Content of Immune Complexes in Immunocompetent Organs of Char in the Basin of Kronotskoe Lake

Oxidation Processes and the Content of Immune Complexes in Immunocompetent Organs of Char in the Basin of Kronotskoe Lake

Development of Artificial Hybrid between Two Deepwater Sympatric Forms of Dolly Varden Salvelinus malma complex (Salmonidae) from Lake Kronotskoe (Eastern Kamchatka)

Development of Artificial Hybrid between Two Deepwater Sympatric Forms of Dolly Varden Salvelinus malma complex (Salmonidae) from Lake Kronotskoe (Eastern Kamchatka)

Ambient temperature as a factor contributing to the developmental divergence in sympatric salmonids.

Factors and mechanisms promoting resource-based radiation in animals still represent a main challenge to evolutionary biology. The modifications of phenotype tied with adaptive diversification may result from an environmentally related shift having occurred at the early stage of development. Here, we study the role of temperature dynamics on the reproductive sites in the early-life divergence and adaptive radiation of the salmonid fish Salvelinus malma dwelling in the Lake Kronotskoe basin (North-East Asia). Local sympatric charr ecomorphs demonstrate strict homing behaviour guiding the preordained distribution along tributaries and, hence, further development under different temperatures. We thoroughly assessed the annual temperature dynamics at the spawning grounds of each morph as compared to an ancestral anadromous morph. Then we carried out an experimental rearing of both under naturally diverging and uniformed temperatures. To compare the morphs’ development under the dynamically changing temperatures, we have designed a method based on calculating the accumulated heat by the Arrhenius equation. The proposed equation shows a strong predictive power and, at the same time, is not bias-susceptible when the developmental temperature approximates 0°C. The temperature was found to significantly affect the charrs’ early ontogeny, which underlies the divergence of developmental and growth rates between the morphs, as well as morph-specific ontogenetic adaptations to the spawning site’s temperatures. As opposed to the endemic morphs from Lake Kronotskoe, the anadromous S. malma, being unexposed to selection оn highly specific reproduction conditions, showed a wide temperature tolerance, Our findings demonstrate that the hatch, onset timing of external feeding, and size dissimilarities between the sympatric morphs reveal themselves during the development under contrast temperatures. As a result of the observed developmental disparities, the morphs occupy specific definitive foraging niches in the lake.

Peculiarities of Early Ontogenesis of Nose Char (N1-form), Endemic Lacustrine and Riverine Form of Salvelinus malma Complex (Salmonidae), of the Lake Kronotskoe (Eastern Kamchatka, Russia)

The growth, order of anlage, and features of transitive stages of skeletal elements (cranial bones and serial structures: teeth, gill rakers, fin rays, pterigyophores, vertebrae muscles, predorsalia, and scales) in were studied in pre-larvae, larvae, and fingerlings of the nose char (N1-form), endemic lakustrine-riverine form of the Dolly varden Salvelinus malma complex of the Lake Kronotskoe, reared in the laboratory at a constant temperature. A comparative analysis of the early ontogenesis of sympatric species of nose char and white char of the Lake Kronotskoe evidences on a high similarity in the growth rate and development of the two forms, differing by the body length of free embryos and the larvae coloration.

Interaction among morphological, trophic and genetic groups in the rapidly radiating Salvelinus fishes from Lake Kronotskoe

Adaptive radiation in fishes entering novel post-glacial lakes ubiquitously gives rise to a set of typical forms specializing under the pressure of the same ecological gradients. The world’s most diverse flock of salmonids from Lake Kronotskoe (Kamchatka, N-E Asia) serves as a good model to study evolutionary divergence modes. Eight forms with different feeding types and habitat preferences are known to originate from Salvelinus malma. To determine the phasing of the flock radiation we analyzed morphometry, muscle isotope content, parasite fauna abundance and microsatellite DNA polymorphism in the sympatric forms inhabiting the lake. We found that seven out of eight morphologically independent forms can be distinguished by a stable feeding niche through comparing the stomach content, isotopic status and parasite fauna abundance. Five eco-morphs were found to be genetically independent, while three other morphs fell into one cluster without any significant restriction of the gene flow among the members. Partitioning of the resources in pelagic—benthic, epilimnetic—deepwater and lacustrine—riverine environments leads to divergence of the most genetically and morphologically distant forms. Smaller genetic and morphometric distances were found for the form pairs diverged along one or two of these gradients. The divergence of the last three eco-morphs in feeding tactics within the coastal zone is not associated with differentiation in microsatellite polymorphism suggesting a more recent and/or subtle specialization within this environment.

The Rate of Mitochondrial Cytochrome b Gene Evolution according to the Analysis of Recent (about 12 000 Years) Isolation of Charrs Salvelinus of Lake Kronotskoe

The nucleotide substitution rate of the mitochondrial cytochrome b gene is estimated on the basis of the genetic differences of charr populations (Salvelinus) with a known time of isolation (Upper Pleistocene–Holocene boundary) as 3.11 × 10–8 substitutions/position/year (95% confidence interval: 2.59 × 10–8–3.64 × 10–8). This estimate is about five times higher than the one obtained for this gene when considering long time intervals of divergence of salmonid fishes (phylogenetic rate)—0.66 × 10–8 (0.56 × 10–8–0.77 × 10–8). Thus, the rule of decrease in mtDNA nucleotide substitution rate estimates while moving from the recent calibration dates (thousand years) to the ancient ones (millions of years) applies also to the lineage of salmonid fishes.

Special Traits in Early Ontogenesis of the Endemic Lacustrine Form of the Salvelinus malma Сomplex (Salmonidae), Small-Mouth Form, from Lake Kronotskoe (Eastern Kamchatka)

Growth, sequences of anlage, and special traits of transient states are investigated in skeletal elements (skull bones and serial structures—teeth, gill rakers, fin rays and pterygiophores, vertebral centra, predorsalia, scales) in prolarvae, larvae, and fry of endemic lacustrine form Dolly varden Salvelinus malma сomplex from Lake Kronotskoe in small-mouth char grown in a laboratory at constant temperature. A high individual variation of growth rate, osteogenesis, and head profile of small-month char larvae is observed demonstrating a recent, in relation to other endemic Kronotskoe Lake forms, formation of this deep-water lacustrine morphotype. Comparative analysis in early development of sympatric small-mouth and white char indicated the origin of the more warm-water, small-mouth char from the cold-water white char.

Early Ontogenetic Features in the White Charr Salvelinus malma Complex (Salmonidae) from Lake Kronotskoe, Eastern Kamchatka

The growth, the sequence of formation, and the features of the transitive states of skeletal elements (cranial bones and serial structures, such as teeth, gill rakers, fin rays and pterygiophores, vertebral bodies, predorsalia, and scales) have been studied in prelarvae, larvae, and fingerlings of the lacusrtrine-riverine morphs of the white charr Salvelinus malma complex from Lake Kronotskoe, Eastern Kamchatka, reared in a laboratory at a constant temperature and collected in the Uzon River, at a spawning ground and downstream. A comparative analysis of osteogenesis features in white charr and the original morph, the Northern Dolly Varden Salvelinus malma malma, has been carried out. A high variability in the rate of growth and development of white charr is noted. A delay in calcification of skeleton in prelarvae and a late onset of scale formation (at the end of the second and the beginning of the third year of life) and first annulus in otoliths (by the third year of life) have been revealed. The results indicate the high specialization of early ontogenesis in white charr, a fish endemic to Lake Kronotskoe.

Juvenile divergence in adaptive traits among seven sympatric fish ecomorphs arises before moving to different lacustrine habitats.

Identifying the mechanisms initiating sympatric diversification in vertebrates has remained a conceptual challenge. Here, we analyse an assemblage of sympatric charr (Salvelinus malma) morphs from landlocked Lake Kronotskoe basin as a model to uncover the divergence pathways in freshwater fishes during the early life history stages. All morphs have distinct developmental biology, but a similar developmental rate retardation compared to the ancestor. Our study reveals that adult morphological differences, which acquire functionality at maturation, originate in the early juvenile stages due to heterochrony in skeletogenesis and allometric changes triggered by variation in metabolic activity. The craniofacial differences among the morphs result from asynchronous development of several skeletal modules. The accelerated ossification of teeth-armed bones occurs in predatory feeding morphs, whereas cranial cover ossification is promoted in benthivorous morphs. These contrasting growth patterns have led to seven phenotypes that span a range far beyond the ancestral variability. The most distinct morphs are a riverine spawning, epilimnetic predator and a lacustrine spawning, profundal benthic feeder. Taken together, we argue that the adaptive morphological differentiation in these sympatric freshwater fishes is driven by diverging patterns in ossification rate and metabolic activity against a background of uneven somatic growth. This divergence is primarily associated with basic environmental differences on the nursery grounds that might be unrelated to resource use. This nonheritable phenotype divergence is then exposed to natural selection that could result in further adaptive genetic changes.

Basic description and some notes on the evolution of seven sympatric morphs of Dolly Varden Salvelinus malma from the Lake Kronotskoe Basin.

The study examines the basic morphological and ecological features of Dolly Varden from Lake Kronotskoe (Russia, Kamchatka). Seven valid morphs different in head proportions, feeding, timing, and place of spawning have been determined in this ecosystem. The basic morphometric characteristics clearly separate Lake Kronotskoe morphs from each other, as well as from its potential ancestor (Dolly Varden). According to CVA analysis, the most notable morphological characteristics determining the mouth position are the length of a lower jaw and rostrum. Furthermore, five of seven morphs inhabit different depth zones of the lake and feed on different food resources. Our data suggest that reproductive isolation may be maintained by temporal/spatial isolation for two morphs with lacustrine spawning, and by spatial isolation only for the rest of the morphs with riverine spawning. The sympatric diversity of the Lake Kronotskoe charrs is exceptionally wide, and there are no other examples for seven sympatric morphs of genus Salvelinus to coexist within a single ecosystem. This study puts forward a three‐step hypothetical model of charr divergence in Lake Kronotskoe as a potential ground for future studies.

The riverine dwelling groups of endemic Dolly Varden (Salvelinus malma, Salmonidae) morphs from lake Kronotskoe (Kamchatka, Russia)

The riverine dwelling groups of endemic Dolly Varden (Salvelinus malma, Salmonidae) morphs from lake Kronotskoe (Kamchatka, Russia)

Ecology of Slaty-Backed Gull (Larus schistisagus) Breeding on Kronotskoe Lake, Kamchatka Peninsula

The slaty-backed gull population of Kronotskoe Lake has not been subjected to anthropogenic impact for many decades. The number and distribution of the breeding colonies of the slaty-backed gulls on the islands of this largest freshwater reservoir of the Kamchatka Peninsula are presented. Data on the breeding phenology, the seasonal dynamics of the food composition of breeding gulls, the foraging distance, and breeding success are considered. These data are compared to the results obtained earlier for Kuril’skoe Lake. Both gull populations are unique in that they are the only freshwater colonies within the distribution range of this marine species. The breeding success of the slaty-backed gulls on Kronotskoe Lake suffers from predation, both intra- and interspecific, in the latter case from brown bears and sea eagles. The hatching period and the fledging time of chicks in this population are both shifted to the end of summer, when gulls have the most abundant food available within the lake area, which increases successful survival of the fledglings. Despite considerable differences between the ecosystems of Kronotskoe Lake and Kuril’skoe Lake, there are several common features in the diets of the gull populations living on the lakes: (1) Despite the fact that gulls perform foraging flights to the sea coast, they only take fish and almost never collect marine invertebrates there. (2) Nearly half of all food items are taken within a 40-km distance from the colony. (3) During the growth period of chicks, gulls from both lakes rely on salmonids (anadromous in Kuril’skoe Lake, resident in Kronotskoe Lake) that they hunt in the lakes near their colonies.

Содержание иммунных комплексов и уровень окислительных процессов в крови и органах гольцов оз. Кроноцкое (п-ов Камчатка)

Содержание иммунных комплексов и уровень окислительных процессов в крови и органах гольцов оз. Кроноцкое (п-ов Камчатка)

Diversity of nosed charrs Salvelinus malma (Salmonidae) of Lake Kronotskoe (Kamchatka)

The littoral benthivorous charrs Salvelinus malma with subterminal mouth distributed in Lake Kronotskoe basin are separated into three distinct morphs. These morphs significantly differ in head proportions, jaws' length, skull structure, and degree of gill rakers' reduction. The morphs spawn in distant lake tributaries at the spawning grounds of various types. Joint spawning has never been observed for these morphs in any type of spawning grounds. The differences in the external morphology and growth rate of the morphs become evident during the riverine life stage. The adult charrs inhabit the same sites of the littoral zone. No reliable difference is found in the diet among morphs, since all nosed charrs dominantly feed on amphipods with the exception of a few individuals that fed on chironomid larvae.

Ecological differentiation of resident Dolly Varden Salvelinus malma (Salmonidae) from Lake Dal’nee, Kamchatka

Resident Dolly Varden Salvelinus malma of Lake Dal’nee (Paratunka River basin) is represented by two stable trophic groups: one group feeds on mainly amphipods while another on gastropods. The former group is dominantly infected by Cyathocephalus truncatus and Crepidostomum metoecus, whereas the latter group is infected with Crepidostomum farionis, Ichthyocotylurus erraticus, and Diplostomum spp. The fishes of the former group grow faster and defined by higher fat content of muscular tissue. In addition, they accumulate monoenic fatty acids in the muscles. The fishes of the latter group differ in a high content of omega-3 and omega-6 fatty acids in the muscles. The amphipod foragers are characterized by a larger head with elongated upper jaw and comparatively short fins. A similar ecological differentiation is observed in the littoral benthivorous charrs from Lake Kronotskoe. The group feeding on amphipods was found in both lakes. In Lake Kronotskoe, the second group consumes the most abundant sedentary benthos, mollusks and chironomids.

New endemic deepwater charr morphs of the genus Salvelinus (Salmoniformes: Salmonidae) from Lake Kronotskoe, Kamchatka

Two previously unknown profundal dwelling charr morphs of the genus Salvelinus from Lake Kronotskoe are described in this article. According to their lifestyle peculiarities, these morphs were named the “bigmouth charr” and “smallmouth charr.” The former group is near-bottom benthivorous, while the latter one inhabits the water column and occupies the omnivorous niche. Bigmouth and smallmouth charrs are distinguished from the rest of the sympatric charr morphs by their smaller size, shorter snout, larger eyes, as well as by several craniological traits and lower parasite abundance. Spawning of both morphs takes place directly in the profundal zone and lasts from late October to February. Additional studies are required to determine the systematic status of the new morphs.