Comparative genetic analysis of grayling (Thymallus spp. Salmonidae) across the paleohydrologically dynamic river drainages of the Altai-Sayan mountain region

Abstract

A high number of grayling (Thymallus) species have been described from the Altai-Sayan mountain region, for which little to no genetic information is available. We investigated genetic relationships within this genus of salmonid fishes using mtDNA and microsatellite markers. The analysis focused on three putative species, Markakol grayling (T. brevicephalus), Upper Ob grayling (T. nikolskyi) and Mongolian grayling (T. brevirostris). We integrated these data with mtDNA sequences from eight other grayling species, including two of geographic proximity to the study area. Phylogenetic results revealed three pairs of reciprocally monophyletic sister species, two of which were phylogenetically juxtaposed across isolated drainage systems. Based on microsatellite analysis (up to 10 loci) no evidence of hybridization or introgression was found among species, supporting the mtDNA phylogeny. Based on a time-calibrated tree, divergence times between the focal taxa ranged from 0.36 to 1.1 MY. The genetic data support the distinction of these species and underscore the importance of paleohydrological dynamics in this biogeographically complex region. Well-documented mega-flood events in the region provide a model of how the contemporary cross-basin distribution of these species may have evolved.

Global systematic diversity, range distributions, conservation and taxonomic assessments of graylings (Teleostei: Salmonidae; Thymallus spp.)

“…While some of these hypothesised colonization events are pre-Pleistocene, our knowledge at least of Pleistocene paleodynamics across Russia reveals numerous events of paleohydrological connectivity (via large paleo-lakes and mega floods) across Siberia and through the Ponto-Caspian region into Europe (Komatsu et al 2016). These events have already served hypotheses concerning the phylogeographic structure of Thymallus, Hucho and Brachymystax across their Siberian range (Koskinen et al 2002;Froufe et al 2003a;Weiss et al 2020a). Nonetheless, much work remains in matching the timing of specific events of dispersal and vicariance with specific paleo-events promoting cross-drainage connectivity and isolation.…”

“…Besides the baicalensis/ nigrescens species pair, two other pairwise distances in our data under these thresholds are between sister species pairs in the Altai-Sayan mountain region (T. brevirostris and T. brevicephalus; and T. nikolskyi and T. svetovidovi). These species pairs span allopatric drainages subject to catastrophic paleo-hydrological flooding (Weiss et al 2020a), which may have played a role in their cross-basin colonization history.…”

“…Haplotypes LC168675 and MT063035 (Fig. 2) stem from samples in the upper Irtysh River drainage; population genetic analysis shows close affinity with samples from the Kara-Kaba River (Weiss et al 2020a) (Fig. 1).…”

“…Siberia's complex paleo-hydrology has shaped the diversity and distribution of grayling throughout Eurasia (Koskinen et al 2002;Froufe et al 2003aFroufe et al , 2005. This is illustrated by the phylogeographic patterns in the Altai-Sayan mountain region (Knizhin and Weiss 2009;Weiss et al 2020a) or the three sympatric species with allopatric origins found in the Bureya River, Amur River drainage (Weiss et al 2020b). High phylogeographic complexity is also found in Europe within the Danube River drainage as well as the larger Ponto-Caspian basin (Weiss et al 2002(Weiss et al , 2013Gum et al 2009;Marić et al 2012Marić et al , 2014.…”

“…For instance, Knizhin et al (2008) demonstrated that different grayling phenotypes in the endorheic basin of Western Mongolia can be phylogenetically assigned to T. brevirostris. Thymallus brevicephalus found in the upper Irtysh River drainage in Kazakhstan is the sister taxon to T. brevirostris (Weiss et al 2020a). While such studies combined single-gene mtDNA analysis with population genetic and morphological analysis, they may lack phylogenetic resolution due to the limited length of the mtDNA sequence analysed.…”