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.
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.
Six postglacial lakes were studied along both sides of the Kamchatka central mountain range, Russia. Pairs of local morphotypes of species of Arctic charrs, Salvelinus spp., have previously been described from the southernmost lakes while the fish fauna of the four northernmost lakes was studied here for the first time. Phenotypic data support the division of Kamchatkan lacustrine charrs into two groups according to the number of gill rakers and pyloric caeca, as well as snout-dorsal and snout-ventral distances (MANOVA, P < 0·001). These groups respectively correspond to phenotypes commonly referred to as Salvelinus malma and Salvelinus taranetzi. To clarify the identity of these groups, D-loop and cytochrome b (cytb) region sequences were analysed. Haplotype network analysis of mtDNA shows the salmonids inhabiting four lakes on the south and north are phylogenetically close to either Beringian S. malma or to S. taranetzi from the Chukotka and Kolyma River basins (the mean ± s.e. pairwise per cent sequence divergence is 0·006 ± 0·001). Phenotype-genotype discordance suggests that mitochondrial introgression between species has occurred in the two smallest lakes (<0·5 km ) in the central part of the peninsula. Identical haplotypes of D-loop and cytb regions were found for the populations of S. taranetzi from the most distant southern and northern lakes, indicating all lakes were colonized by both species simultaneously after the last glacial maximum. Salvelinus taranetzi may have colonized the Kamchatka peninsula from one or both of two different source regions: the Arctic Beringia and the northern coast of the Okhotsk Sea.
Adaptive radiation in fishes has been actively investigated over the last decades. Along with numerous well‐studied cases of lacustrine radiation, some examples of riverine sympatric divergence have been recently discovered. In contrast to the lakes, the riverine conditions do not provide evident stability in the ecological gradients. Consequently, external factors triggering the radiation, as well as developmental mechanisms underpinning it, remain unclear. Herein, we present the comprehensive study of external and internal drivers of the riverine adaptive divergence of the salmonid fish Salvelinus malma. In the Kamchatka River, north‐east Asia, this species splits in the reproductively isolated morphs that drastically differ in ecology and morphology: the benthivorous Dolly Varden (DV) and the piscivorous stone charr (SC). To understand why and how these morphs originated, we performed a series of field and experimental work, including common‐garden rearing, comparative ontogenetic, physiological and endocrinological analyses, hormonal ‘engineering’ of phenotypes and acute toxicological tests. We revealed that the type of spawning ground acts as the decisive factor driving the radiation of S. malma. In contrast to DV spawning in the leaf krummholz zone, SC reproduces in the zone of coniferous forest, which litter has a toxic impact on developing fishes. SC enhances resistance to the toxicants via metabolism acceleration provided by the elevated thyroid hormone expenditure. These physiological changes lead to the multiple heterochronies resulting in a specific morphology and ecology of SC. Salvelinus malma represents a notable example of how the thyroid axis contributes to the generation of diverse phenotypic outcomes underlying the riverine sympatric divergence. Our findings, along with the paleoecology data concerning spruce forest distribution during the Pleistocene, provide an opportunity to reconstruct a scenario of S. malma divergence. Taken together, obtained results with the data of the role of thyroid hormones in the ontogeny and diversification of fishes contribute a resource to consider the thyroid axis as a prime director orchestrating the phenotypic plasticity promoting evolutionary diversification under the changing environmental conditions.
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