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

IF 4.6 2区环境科学与生态学 Q1 BIODIVERSITY CONSERVATION

Diversity and Distributions Pub Date : 2024-04-25 DOI:10.1111/ddi.13845

Gernot K. Englmaier, Nuria Viñuela Rodríguez, Jernej Bravničar, Lukas Zangl, Henri Persat, Saša Marić, Clemens Ratschan, Bo Delling, Duarte V. Gonçalves, Giulia Secci-Petretto, Elsa Froufe, Steven J. Weiss

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引用次数: 0

Abstract

Aim

Paleohydrological 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.

Location

Freshwater systems in Europe.

Methods

Based 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.

Results

The 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 Conclusions

The 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.

Abstract Image

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基于 SNP 的欧洲胸腺鱼属（鲑科）分析揭示了与生物地理推断、分类和保护相关的广泛的有丝分裂-核不一致性

目的欧洲河流系统的古水文动态已得到充分记录，促进了其水生动物群的隔离和连接阶段的转变。这些条件加上淡水鱼类中发现的高杂交率可能会带来相当大的复杂性和潜在的系统发育模式的有丝分裂-核分裂不一致。我们首次大规模分析了欧洲白鲑（Thymallus）物种的核SNPs，并与mtDNA数据进行了比较，从而评估了这一假设，目的是重新评估这一类嗜流变鱼类的进化历史。方法基于线粒体（有丝分裂基因组、控制区）和核（ddRADseq）数据，我们应用种群遗传学、系统发生学和生物地理学工具来评估古水文变化背景下的鱼系多样性。结果结果证实了之前公认的高水平的种系多样性，但也揭示了一些有丝分裂-核不一致的情况，以及欧洲胸腺鞘氨醇主要种间和种内种系之间的历史（自然）和人类介导的引种信号。基于核 SNP 数据的时间校准系统发育和祖先区域估计支持该属在欧洲的上新世晚期分化，并表明该属早期在黑海盆地定居，随后扩散到中欧和西欧。有几个核-丝不一致的例子强调了在一个动态的古水文景观中异源系的频繁接触，并揭示了仅根据 mtDNA 的推断来进行分类和保护决策的弱点。多瑙河和莱茵河流域被推断为不同系统地理系之间的重要接触区。此外，我们的数据还对濒危的 T. aeliani 的遗传完整性提出了质疑。尽管 T. aeliani 的 mtDNA 相互单系，但通过核 SNPs 分析，它与 T. thymallus 的分化似乎微乎其微。

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来源期刊

Diversity and Distributions 环境科学-生态学

CiteScore

8.90

自引率

4.30%

发文量

195

审稿时长

8-16 weeks

期刊介绍： Diversity and Distributions is a journal of conservation biogeography. We publish papers that deal with the application of biogeographical principles, theories, and analyses (being those concerned with the distributional dynamics of taxa and assemblages) to problems concerning the conservation of biodiversity. We no longer consider papers the sole aim of which is to describe or analyze patterns of biodiversity or to elucidate processes that generate biodiversity.