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Comparative Genetic Analysis of Grayling (Thymallus Spp. Salmonidae)

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Comparative Genetic Analysis of Grayling (Thymallus Spp. Salmonidae) Comparative genetic analysis of grayling (Thymallus spp. Salmonidae) across the paleohydrologically dynamic river drainages of the Altai-Sayan mountain region Steven Weiss, Jacqueline Grimm, Duarte V. Gonçalves, Giulia Secci- Petretto, Gernot K. Englmaier, Mirgaliy Baimukanov, et al. Hydrobiologia The International Journal of Aquatic Sciences ISSN 0018-8158 Hydrobiologia DOI 10.1007/s10750-020-04273-3 1 23 Your article is published under the Creative Commons Attribution license which allows users to read, copy, distribute and make derivative works, as long as the author of the original work is cited. You may self- archive this article on your own website, an institutional repository or funder’s repository and make it publicly available immediately. 1 23 Hydrobiologia https://doi.org/10.1007/s10750-020-04273-3 (0123456789().,-volV)( 0123456789().,-volV) PRIMARY RESEARCH PAPER Comparative genetic analysis of grayling (Thymallus spp. Salmonidae) across the paleohydrologically dynamic river drainages of the Altai-Sayan mountain region Steven Weiss . Jacqueline Grimm . Duarte V. Gonc¸alves . Giulia Secci-Petretto . Gernot K. Englmaier . Mirgaliy Baimukanov . Elsa Froufe Received: 26 November 2019 / Revised: 19 March 2020 / Accepted: 21 April 2020 Ó The Author(s) 2020 Abstract A high number of grayling (Thymallus) We integrated these data with mtDNA sequences from species have been described from the Altai-Sayan eight other grayling species, including two of geo- mountain region, for which little to no genetic graphic proximity to the study area. Phylogenetic information is available. We investigated genetic results revealed three pairs of reciprocally mono- relationships within this genus of salmonid fishes phyletic sister species, two of which were phyloge- using mtDNA and microsatellite markers. The anal- netically juxtaposed across isolated drainage systems. ysis focused on three putative species, Markakol Based on microsatellite analysis (up to 10 loci) no grayling (T. brevicephalus), Upper Ob grayling (T. evidence of hybridization or introgression was found nikolskyi) and Mongolian grayling (T. brevirostris). 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. Handling editor: Christian Sturmbauer The genetic data support the distinction of these species and underscore the importance of paleohydro- Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10750-020-04273-3) con- logical dynamics in this biogeographically complex tains supplementary material, which is available to authorized region. Well-documented mega-flood events in the users. region provide a model of how the contemporary S. Weiss (&) Á J. Grimm Á G. K. Englmaier cross-basin distribution of these species may have Institute of Biology, University of Graz, Universita¨tsplatz evolved. 2, 8010 Graz, Austria e-mail: [email protected] Keywords Lake Markakol, Western Mongolia Á D. V. Gonc¸alves Á G. Secci-Petretto Á E. Froufe Historical biogeography Á Pleistocene Á Salmonidae CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixo˜es, Avenida General Norton de Matos, S/N, 4450-208 Matosinhos, Portugal Introduction G. Secci-Petretto Department of Biology, Faculty of Sciences, U. Porto - Paleoclimatic processes have played a major role in University of Porto, Porto, Portugal shaping species distributions and diversity (Wiens & M. Baimukanov Donoghue, 2004). A better understanding of the Institute of Hydrobiology and Ecology, 75 Rakhmetov St, legacies of such processes is crucial for conserving Irgely Village, Almaty, Kazakhstan biodiversity and modeling predictions of how species, 123 Hydrobiologia as well as ecosystems, will respond to anthropogenic magnitude of the paleohydrological dynamics of climate change (Svenning et al., 2015). The interplay Siberian rivers (e.g. Komatsu et al., 2016; Margold between climatic processes and evolution may be et al., 2018). markedly different for freshwater compared to terres- Thus far, salmonid fishes, including Thymallus, trial organisms, as drainage position and historical have proved to be good models for investigating the connectivity play a larger role in explaining both interplay between such large-scale paleohydrological species ranges and phylogeographic structure (Dias processes and biological diversification (Koskinen et al., 2014; Carvajal-Quintero et al., 2019). The et al., 2002; Froufe et al., 2005; Weiss et al., generalization that paleohydrological dynamics and 2006, 2007; Froufe et al., 2008; Weiss et al., 2020). historical connectivity can strongly influence contem- These studies highlight the shifting phases of hydro- porary species diversity and distributions is supported logical isolation and historical connectivity within and by many studies of freshwater fishes in North America between major river drainage networks such as the (Griffiths, 2015; Matamoros et al., 2016), Europe (Buj Amur, Lena, Enisei and Ob. These paleohydrological et al., 2017; Levin et al., 2019), New Zealand (Craw insights are congruent with the description of specific et al., 2007), Australia (Waters et al., 2019), Asia events (e.g. mega-floods) that have helped shape the (Froufe et al., 2003, 2008; de Bruyn et al., 2013) and distributions of freshwater organisms (e.g. Ivanov South America (Scho¨nhuth et al., 2011). The origins of et al., 2016; Komatsu et al., 2016; Arzhannikov et al., this conceptual development began with a large 2018). number of phylogeographic studies that attempted to Nevertheless, there is still much uncertainty con- link phylogeographic patterns with contemporary cerning the biological consequences of paleohydro- drainage networks and ocean basins. In Europe, such logical dynamics, especially where knowledge of studies on freshwater fishes began with brown trout faunal diversity and distributions is incomplete. The Salmo trutta Linnaeus, 1758 (Bernatchez et al., 1992), Altai-Sayan mountain region, in particular, has been European chub Squalius cephalus (Linneaus, 1758) insufficiently investigated concerning the distribution (Durand et al., 1999), European perch Perca fluviatilis and systematics of its aquatic fauna, including Linnaeus, 1758 (Nesbo et al., 1999) and European grayling. Here, the headwaters of the Ob and Enisei grayling Thymallus thymallus (Linnaeus, 1758) river drainages are juxtaposed with the endorheic (Weiss et al., 2002). basin of the Khovd and Zavkahn river drainages Similar studies were carried out throughout Eur- (Fig. 1). These rivers harbor several putative grayling asia, including Siberia (Stepien et al., 1998; Froufe species with unclear evolutionary relationships (i.e. T. et al., 2003). Thymallus spp. (graylings) were the baicalensis Dybowski, 1874; T. brevirostris Kessler, target of one of the first broad-scale phylogeographic 1879; T. nikolskyi Kaschenko, 1899; T. nigrescens analyses of freshwater fishes in Siberia (Koskinen Dorogostaisky, 1923; T. brevicephalus Mitrofanov, et al., 2002). While the general phylogeographic 1971 and T. svetovidovi Knizhin & Weiss, 2009). patterns uncovered in that study largely reflected Thymallus nigrescens is endemic to Lake Chuvsgol, contemporary drainage networks, results also agreed located in the upper Enisei River drainage in Mongo- with a cataclysmic paleohydrological event involving lia, whereas T. svetovidovi is found in another branch ancient Lake Baikal. Subsequent studies on the of the Enisei drainage (Knizhin & Weiss, 2009) that is diversity and distribution of graylings in Siberia took geographically close to Lake Chuvsgol, but in terms of advantage of the growing knowledge of large-scale the contemporary hydrological network, very distant. river network dynamics in this area, associated with Thymallus nikolskyi, first described over 100 years Quaternary climatic oscillations and glacial cycles. ago (Kaschenko, 1899) is reported from several While the paleogeological history of Lake Baikal has tributaries of the adjacent upper Ob River drainage attracted considerable research interest, elsewhere in (Romanov et al., 2016; Dyldin et al., 2017), whereas T. Siberia the potential effects of Pleistocene glaciations brevicephalus is found in the nearby Irtysh River on the hydrological network were underestimated or branch of the Ob River drainage, in Lake Markakol understudied. However, beginning with the contro- (Mitronfanov, 1971) as well as in adjacent tributaries versial perspectives of Grosswald (1998), there has flowing from the Altai Mountains to the Irtysh. been an increased understanding of the large scope and Thymallus baicalensis is the commonly occurring 123 Hydrobiologia Fig. 1 a Overview map of Asia showing the location of the blue = T. nikolskyi (same as in Fig. 3). Shown are the study area in a box, and the flow of three major Siberian river approximate distribution ranges of these species along with systems; Altai-Sayan mountain region in grey; b overview of the those of T. svetovidovi, T. baicalensis and T. nigrescens as well upper Ob and Enisei River drainages as well as the adjacent as several hypothesized mega-flood events shown with black endorheic basin of Western Mongolia, including the focal area arrows. These events are (a) Tunguska–Enisei shortcut; (b) Altai of this study. The numbered sample sites are color-coded to as shown in Komatsu et al., 2016); (c) Mogen–Buren valley represent the three grayling species
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