Evaluating a species phylogeny using ddRAD SNPs: Cyto-nuclear discordance and introgression in the salmonid genus Thymallus (Salmonidae)

Secci‐Petretto, Giulia; Englmaier, Gernot K.; Weiss, Steven; Antonov, A. L.; Persat, H.; Denys, Gaël P.J.; Schenekar, Tamara; Романов, В. И.; Taylor, Eric B.; Froufe, Elsa

doi:10.1016/j.ympev.2022.107654

Cited by 4 publications

References 94 publications

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SNP‐based analysis of European Thymallus spp. (Salmonidae) reveals extensive mito‐nuclear discordance relevant for biogeographic inferences, taxonomy and conservation

Englmaier,

Rodríguez,

Bravničar

et al. 2024

Diversity and Distributions

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AimPaleohydrological dynamics are well‐documented for European river systems, promoting shifting phases of isolation and connectivity of their aquatic fauna. These conditions coupled with high rates of hybridisation found in freshwater fishes may introduce considerable complexity and potential mito‐nuclear discordance of phylogenetic patterns. We evaluate this hypothesis using the first large‐scale analysis of nuclear SNPs in European species of grayling (Thymallus) compared to mtDNA data with the aim of reassessing the evolutionary history of this group of rheophilic fishes.LocationFreshwater systems in Europe.MethodsBased on mitochondrial (mitogenomes, control region) and nuclear (ddRADseq) data, we applied population‐genetic, phylogenetic, and biogeographic tools to evaluate lineage diversity in the context of paleohydrological alterations.ResultsThe results corroborated previously recognised high levels of lineage diversity, but revealed several cases of mito‐nuclear discordance and signals of both historical (natural) and human‐mediated introgression among major inter‐ and intraspecific lineages of Thymallus in Europe. A time‐calibrated phylogeny and ancestral area estimation, based on nuclear SNP data, supported a late Pliocene diversification of the genus in Europe and suggested an early colonisation of the Black Sea basin with subsequent dispersal into Central and Western Europe.Main ConclusionsThe genetic structure of Thymallus in Europe recovered by nuclear SNPs contrasts considerably with that supported by mtDNA. Several instances of mito‐nuclear discordance underscore frequent contact of allopatric lineages in a dynamic paleohydrological landscape and reveal the weakness of basing both taxonomic and conservation decisions on inferences based on mtDNA alone. The Danube and Rhine drainages were inferred as important zones of contact between divergent phylogeographic lineages. Additionally, our data cast doubt on the genetic integrity of the endangered T. aeliani. Its divergence from T. thymallus, using nuclear SNPs, appears minimal as samples of T. aeliani group within Danubian lineages, despite carrying highly divergent reciprocally monophyletic mtDNA.

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SNP‐based analysis of European Thymallus spp. (Salmonidae) reveals extensive mito‐nuclear discordance relevant for biogeographic inferences, taxonomy and conservation

Englmaier,

Rodríguez,

Bravničar

et al. 2024

Diversity and Distributions

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Multiple secondary contacts and historic hybridization between glacial lineages of charr (Salvelinus, Salmonidae) in northeastern Asia

Bondar,

Oleinik,

Kukhlevsky

et al. 2024

Ecology of Freshwater Fish

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Arctic regions of northeastern Asia represent areas of secondary contact of the glacial phylogenetic lineages of charrs belonging to the genus Salvelinus (Salmoniformes: Salmonidae). However, the post‐glacial dispersion of charr across Arctic regions is poorly understood, as knowledge of populations from Chukotka and its neighbouring areas remains limited. Specifically, there is no clear understanding of which charr species inhabit significant regions of Chukotka from the sea coasts to the Kolyma drainage. In this study, we explored the affiliation of lacustrine charrs from the Chukotka area with (1) the Arctic lineage of Taranetz' charr (Salvelinus taranetzi); (2) the Bering lineage of Northern Dolly Varden (Salvelinus malma malma) and (3) the Siberia and Atlantic lineages of Arctic charr (Salvelinus alpinus). We analysed sequence variation of the mitochondrial DNA control region (mtDNA CR; 960 base pairs) and genotyped seven microsatellite loci of nuclear DNA from charr collected at 13 sampling sites. We found different consequences of secondary contact: (1) complete fixation of introgressed mtDNA (mitochondrial capture) and (2) preservation of several mtDNA lineages with the absence of contemporary gene flow between resident populations. Combining the distribution patterns, phylogenetic network topology and knowledge of the glaciation history of the region, we propose two zones of secondary contact of the glacial lineages in Chukotka–Kolima‐Chukotka River system and Paleo‐Amguema River–from where charrs with introgressed genomes spread throughout this range. However, in some cases, the process of foreign mtDNA capture likely occurs in a more localised manner.

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An integrative approach highlights the discrepancy in the genetic, phenotypic, and presumptive taxonomic structure of Phoxinus (Actinopterygii, Leuciscidae, Phoxininae) in Bulgaria

Palandačić,

Diripasko,

Kirchner

et al. 2024

Journal of Fish Biology

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The present drainage network of Bulgaria is the result of a complex Neogene and Quaternary evolution. Karst, which has developed on 23% of the territory, further complicates the hydrological pattern. Fresh waters of Bulgaria drain into the Black Sea and the Aegean Sea basins and can be roughly divided into the Danube (Middle and Lower Danube), non‐Danube Black Sea, East Aegean, and West Aegean hydrological regions. Phoxinus, a small leuciscid fish, has a mosaic distribution in all four of these regions, inhabiting small mountainous and semi‐mountainous streams. Based on morphology, it was identified as three species, Phoxinus phoxinus in the Danube, Phoxinus strandjae in the non‐Danube, and Phoxinus strymonicus in West Aegean region. Later, molecular data revealed Phoxinus csikii and Phoxinus lumaireul in the Middle Danube and P. csikii in the Lower Danube. Phoxinus has been the focus of many studies, showing a high molecular and morphological diversity, which is not entirely consistent with previous morphology‐only‐based taxonomic concepts. In this study, molecular (a mitochondrial marker and a nuclear marker) and morphological data from both historical and recently sampled collections were analysed to assess the applicability of the integrative approach in Phoxinus. The results showed a significant influence of the complex paleo‐ and recent hydrology on the currently observed genetic structure of the considered populations and species. Furthermore, the study also demonstrated a strong influence of phenotypic plasticity on the morphological analysis of Phoxinus and the lack of a clear differentiation between P. csikii and P. strandjae. A barcoded specimen was designated as neotype to fix the species named P. strandjae in the current taxonomic concept. Finally, a significant discordance between genetically delimited clades and phenotypic groups did not allow a proper delineation of the species distributed in Bulgaria, demonstrating that more molecular markers are needed for further taxonomic study of the Phoxinus complex.

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Evaluating a species phylogeny using ddRAD SNPs: Cyto-nuclear discordance and introgression in the salmonid genus Thymallus (Salmonidae)

Cited by 4 publications

References 94 publications

SNP‐based analysis of European Thymallus spp. (Salmonidae) reveals extensive mito‐nuclear discordance relevant for biogeographic inferences, taxonomy and conservation

SNP‐based analysis of European Thymallus spp. (Salmonidae) reveals extensive mito‐nuclear discordance relevant for biogeographic inferences, taxonomy and conservation

Multiple secondary contacts and historic hybridization between glacial lineages of charr (Salvelinus, Salmonidae) in northeastern Asia

An integrative approach highlights the discrepancy in the genetic, phenotypic, and presumptive taxonomic structure of Phoxinus (Actinopterygii, Leuciscidae, Phoxininae) in Bulgaria

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