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

Abstract

Recent adaptive radiations are powerful evolutionary case studies which can be parsed to reveal the relationship between genomic variation and the origin of distinct phenotypes. Sympatric radiations of the charr complex (genus Salvelinus), present a trove for comparative genomics of craniofacial evolution as charrs have repeatedly diversified into multiple sympatric morphs with distinct feeding specializations, with species flocks frequently manifesting as stereotypical assemblages of two to three resident lineages. In such repeated variation, commonalities in adaptive response can highlight potential constraints in biasing the type of phenotypes available for evolutionary change. A species flock of Dolly Varden charr (Salvelinus malma) in Lake Kronotskoe constitutes a unique case study of charrs as it contains at least seven true-breeding lineages, each with defining morphological and ecological traits. This is the most extensive radiation described for the genus. Here, we performed the first genome-wide analyses of variation within this species flock to provide a working foundation in which to address genetic foundations for adaptive change in character. Our data support distinct reproductively isolated lineages within the lake environment suggesting true breeding morphs and little hybridization. Analysis of changes within the lacustrine lineages, we find specific selection on thyroid and craniofacial genes as key shared genetic basis for the lake radiation. Further, we find a shift in thyroid signaling as a key modulator of subsequent lineage specification. Our data delineate a clear genetic basis for diversification of specialized lineages and provide a new model to understand commonalities in adaptive radiations through constraint on development.