Natural toxic impact and thyroid signalling interplay orchestrates riverine adaptive divergence of salmonid fish

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.