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Introgressive hybridization between two phylogenetic lineages of charrs ( Salvelinus : Salmonidae) in northeastern Asia

2021; Wiley; Volume: 59; Issue: 8 Linguagem: Inglês

10.1111/jzs.12563

1439-0469

А. Г. Олейник, Evgeniia I. Bondar, A. D. Kukhlevsky, Л. А. Скурихина, N. E. Kovpak,

Fish Biology and Ecology Studies

Many lacustrine charrs of the genus Salvelinus were described as separate species, and their origin and phylogenetic relationships are still under debate. In this study, we described the genetic variation of charrs from Lake Grand (Elikchan Lake Group, the mainland coast of the Sea of Okhotsk, Russia) and several locations outside of this system based on eight microsatellite (ms) loci and mitochondrial (mt) DNA control region. We tested the hypothesis of the resident charr membership to (a) the Arctic lineage of Salvelinus taranetzi sensu (Oleinik et al., Russian Journal of Genetics, 51, 2015, 55); (b) the Bering lineage of the Northern Dolly Varden Salvelinus malma malma; and (c) the Atlantic lineage of the Arctic charr Salvelinus alpinus. Analysis of phylogenetic relationships based on the mtDNA control region showed that all individuals from Lake Grand grouped with the Bering lineage. Bayesian analysis using msDNA supports the clustering together of charrs from Lake Grand and Arctic lineage, regardless of their mtDNA haplotypes. Incongruence between mtDNA and msDNA markers provided strong evidence of historical mtDNA introgression from S. malma malma to S. taranetzi. Patterns of divergence confirm a postglacial secondary contact of the representatives of Arctic and Bering lineages in the area of the Sea of Okhotsk coast and past hybridization in Lake Grand with the following features: (a) complete fixation of introgressed mtDNA of one species within populations of another and (b) absence of modern population of S. malma malma in the lake. El origen y las relaciones filogenéticas de los salvelinos lacustres del género Salvelinus, muchos de los cuales se han descrito como especies separadas, se están debatiendo actualmente de una forma activa. En este estudio, describimos la variabilidad genética de los salvelinos del lago Grand (el sistema de los lagos de Elikchan en la costa continental del mar de Okhotsk, Rusia) y varias ubicaciones fuera de este sistema, en base a ocho locuses de microsatélites (ms) y una región de control del ADN mitocondrial (mt). Probamos la hipótesis de que el salvelino lacustre pertenece al (1) linaje Arctic del Salvelinus taranetzi sensu Oleinik et al. (2015); (2) linaje Bering del Salvelinus malma malma; (3) linaje Atlantic del Salvelinus alpinus. El análisis de las relaciones filogenéticas basadas en la región de control del mtADN mostró que todos los salvelinos del lago Grand pertenecen al linaje Bering. El análisis bayesiano utilizando msADN admite la la agrupación de salvelinos del lago Grand y el linaje Arctic, independientemente del haplotipo de mtADN. El desajuste entre los marcadores mtADN y msADN ha proporcionado una fuerte evidencia de la introgresión histórica del mtADN de S. malma malma a S. taranetzi. Los modelos de la divergencia detectada confirman el contacto secundario post-glacial de representantes de los linajes Arctic y Bering en la región de la costa del mar de Okhotsk, así como la hibridación histórica en el lago Grand con las siguientes características: (1) fijación completa de mtADN introgresado de una especie en poblaciones de otra; (2) la ausencia de la población moderna de S. malma malma en el lago. Alignment S1. MtDNA CR alignment (960 bp) comprising sequences of 185 individuals. Table S1. List of mtDNA CR sequences from Genbank with accession numbers included in molecular analyses in the present study. Table S2. List of mtDNA haplotypes from charrs (Salvelinus) used in the study with the original source ('New' means our study report this haplotype for the first time), and GenBank accession number. Table S3. Locus name, forward and reverse primer sequences, repeat motif, GenBank Accession number, annealing temperature (°C) for nine microsatellite loci used for analysis. Table S4. Divergence values (Dxy ± SE) estimated across mtDNA CR between the charr samples: average number of nucleotide substitution per site between samples—below diagonal, standard errors—above diagonal. Table S5. Divergence values (Da ± SE) estimated across mtDNA CR between the charr samples: number of net nucleotide substitution per site between samples—below diagonal, standard errors—above diagonal. Table S6. Mean p-distances between charr taxa based on mtDNA CR. Table S7. Genetic diversity statistics for eight microsatellite loci for the eight charr samples. Figure S1. Natural distribution areas of S. malma malma, S. taranetzi, S. alpinus, and S. curilus around the Sea of Okhotsk according to Esin and Markevich (2017), and population locations of Salvelinus sp. 7 and Salvelinus sp. 4 used for genetic analyses. Figure S2. Neighbor-joining (NJ) tree based on 185 sequences of charrs (Salvelinus) of 960 bp fragment of mtDNA CR. Figure S3. Maximum-likelihood (ML) tree for haplotypes of charrs (Salvelinus) including GenBank samples, resulting from analysis of 960 bp fragment of mtDNA CR. The tree was constructed using T92 plus gamma plus invariant sites model of nucleotide substitution. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.