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Allopatric Divergence and Hybridization Within Cupressus Chengiana (Cupressaceae), a Threatened Conifer in the Northern Hengduan Mountains of Western China

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Allopatric Divergence and Hybridization Within Cupressus Chengiana (Cupressaceae), a Threatened Conifer in the Northern Hengduan Mountains of Western China See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/339803645 Allopatric divergence and hybridization within Cupressus chengiana (Cupressaceae), a threatened conifer in the northern Hengduan Mountains of western China Article in Molecular Ecology · March 2020 DOI: 10.1111/mec.15407 CITATIONS READS 11 547 9 authors, including: Jialiang Li Richard Ian Milne Sichuan University The University of Edinburgh 18 PUBLICATIONS 62 CITATIONS 170 PUBLICATIONS 4,040 CITATIONS SEE PROFILE SEE PROFILE Dafu Ru Jibin Miao Sichuan University Sichuan University 9 PUBLICATIONS 103 CITATIONS 7 PUBLICATIONS 19 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Phylogenetic and biogeographic studies on Pyroloideae View project Evolutionary Genetics View project All content following this page was uploaded by Wenjing Tao on 12 November 2020. The user has requested enhancement of the downloaded file. Received: 13 September 2019 | Revised: 21 February 2020 | Accepted: 26 February 2020 DOI: 10.1111/mec.15407 ORIGINAL ARTICLE Allopatric divergence and hybridization within Cupressus chengiana (Cupressaceae), a threatened conifer in the northern Hengduan Mountains of western China Jialiang Li1 | Richard I. Milne2 | Dafu Ru3 | Jibin Miao1 | Wenjing Tao1 | Lei Zhang1 | Jingjing Xu1 | Jianquan Liu1 | Kangshan Mao1 1Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, Abstract College of Life Sciences, State Key Having a comprehensive understanding of population structure, genetic differentia- Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, tion and demographic history is important for the conservation and management of Chengdu, China threatened species. High-throughput sequencing (HTS) provides exciting opportuni- 2 Institute of Molecular Plant Sciences, The ties to address a wide range of factors for conservation genetics. Here, we gener- University of Edinburgh, Edinburgh, UK 3State Key Laboratory of Grassland Agro- ated HTS data and identified 266,884 high-quality single nucleotide polymorphisms Ecosystem, Institute of Innovation Ecology, from 82 individuals of Cupressus chengiana, to assess population genomics across Lanzhou University, Lanzhou, China the species' full range, comprising the Daduhe River (DDH), Minjiang River (MJR) Correspondence and Bailongjiang River (BLJ) catchments in western China. ADMIXTURE, principal com- Kangshan Mao, Key Laboratory of Bio- Resource and Eco-Environment of Ministry ponents analysis and phylogenetic analyses indicated that each region contains a of Education, College of Life Sciences, State distinct lineage, with high levels of differentiation between them (DDH, MJR and Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, BLJ lineages). MJR was newly distinguished compared to previous surveys, and evi- Chengdu 610065, Sichuan, China. dence including coalescent simulations supported a hybrid origin of MJR during the Emails: [email protected]; [email protected] Quaternary. Each of these three lineages should be recognized as an evolutionarily significant unit (ESU), due to isolation, differing genetic adaptations and different Funding information Fundamental Research Funds for the demographic history. Currently, each ESU faces distinct threats, and will require dif- Central Universities of Sichuan University, ferent conservation strategies. Our work shows that population genomic approaches Grant/Award Number: SCU2018D006 and SCU2019D013; National Basic Research using HTS can reconstruct the complex evolutionary history of threatened species in Program of China, Grant/Award Number: mountainous regions, and hence inform conservation efforts, and contribute to the 2014CB954100; National Natural Science Foundation of China, Grant/Award Number: understanding of high biodiversity in mountains. 31370261, 31590821 and 31622015 KEYWORDS evolutionarily significant units, hybridization, mountainous regions, population genomics, threatened species 1 | INTRODUCTION taxonomic status can avoid both underestimation of the necessary protection status for endangered species, and wasted effort on Resolving taxonomic uncertainties and identifying conservation abundant species (Frankham, Ballou, & Briscoe, 2010). Moreover, units (CUs) are crucial for the conservation of biological diversity, a species may comprise several genetically distinct evolutionary providing managers and policy-makers with a clear understanding units, each of which warrants conservation in its own right (Palsbøll, of the population unit boundaries of endangered species (Funk, Berube, & Allendorf, 2007). In recent decades, genetic markers that McKay, Hohenlohe, & Allendorf, 2012). Accurate determination of have been used to define CUs have included microsatellite loci (short Molecular Ecology. 2020;00:1–17. wileyonlinelibrary.com/journal/mec © 2020 John Wiley & Sons Ltd | 1 2 | LI ET AL. sequence repeats; Wang, Liang, Hao, Chen, & Liu, 2018), nuclear specific habitats that are also rare and threatened, such as Larix mas- DNA (nrDNA; Shang et al., 2015), chloroplast DNA (cpDNA; Feng, tersiana, Cephalotaxus lanceolata and Parakmeria omeiensis (Fu, 1992; Xu, & Wang, 2018; Petit, El Mousadik, & Pons, 1998) and mitochon- Yong, Bing, & Njenga, 2017). The genetic structure and demographic drial DNA (Moritz, 1994; Torres-Cambas, Ferreira, Cordero-Rivera, history of species in the HDMs have been shaped by local orogenetic & Lorenzo-Carballa, 2017). However, these markers only yield a few events and climate oscillations (Favre et al., 2015; Liu, Duan, et al., variable loci, and so are generally inadequate for characterizing the 2014). Mountain uplifts generated geographical barriers that limited population genetic structure of species with complex demographic gene flow among populations, affecting the divergence of lineages, history and adaptive patterns (Funk et al., 2012). genetic structure and the evolution of alpine plants (Liu, Sun, Ge, Hybridization, including subsequent introgression, either be- Gao, & Qiu, 2012; Shahzad, Jia, Chen, Zeb, & Li, 2017; Wen, Zhang, tween species or across intraspecific lineages, can complicate the Nie, Zhong, & Sun, 2014). This region was also affected by a series of identification of taxonomic and CUs, and hence the assignment of Quaternary glaciations (Zheng, Xu, & Shen, 2002; Zhou & Li, 1998), priorities when allocating conservation efforts (Allendorf, Leary, among which the two largest on the QTP were the Xixiabangma Spruell, & Wenburg, 2001; Naciri & Linder, 2015). Nevertheless, Glaciation and the Naynayxungla Glaciation, which occurred around hybridization among diverging lineages is prevalent in nature, and 1.2–0.8 and 0.72–0.5 million years ago (Ma), respectively (Zheng about 25% of plant and 10% of animal species are known to have et al., 2002; Zhou & Li, 1998). Many tree species on the QTP moved undergone hybridization (Mallet, 2007). Hybridization becomes south and/or to lower altitudes during the ice ages (Liu, Duan, et al., a conservation issue when gene flow erodes population distinc- 2014; Qiu, Fu, & Comes, 2011), which could drive intraspecific di- tions, especially when the distinctness of a rare species or race is vergence, or hybridization if diverged lineages share a refugium (Du, threatened by introgression from a commoner, sometimes alien, Hou, Wang, Mao, & Hampe, 2017; Liu, Abbott, Lu, Tian, & Liu, 2014; species or race (Allendorf et al., 2001). Equally, however, hybrid- Liu et al., 2013; Ren et al., 2017; Sun et al., 2014). Hence species ization is increasingly recognized as a generator of adaptation and distributed in the HDMs may have complex evolutionary histories, biodiversity (Lamichhaney et al., 2018; Rieseberg, 2019). For exam- necessitating large numbers of markers to accurately delimit both ple, adaptive traits transferred between species by introgression closely related species and intraspecific lineages. can promote adaptive radiations (Edelman et al., 2019; Rieseberg, The Minjiang cypress, Cupressus chengiana S.Y. Hu, is a threat- 2019). Combining distinct genomes in novel ways, coupled with ened conifer that occurs around the northern HDMs, where it is a stabilization and isolation from parents, may form new lineages or vital ecological component of arid valley ecosystems, and is reg- species very quickly (Barrera-Guzman, Aleixo, Shawkey, & Weir, ularly used for house construction and furniture production. It 2018; Lamichhaney et al., 2018), which can result in rapid speciation. has suffered a sharp decline in range and population size because Thus, hybridization has played an important role in the evolution of of logging (Hao et al., 2006; Zeng & Yang, 1992), and is now clas- many species/lineages (Goulet, Roda, & Hopkins, 2017). Therefore, sified as “Vulnerable” by the IUCN (Zhang & Christian, 2013), and policy-making requires an understanding of the roles hybridization as a “Second-Class Endangered Plant” of China (Fu, 1992). Early has played in any threatened species. However, detection of hybrid- studies using three regions of chloroplast genome (Xu et al., 2010), ization is difficult using traditional molecular markers (Allendorf, six pairs of nuclear microsatellite markers (Lu et al., 2014) and 10 Hohenlohe, & Luikart, 2010), with hundreds of markers usually re- nrDNA sequence loci (Xu et al., 2017) demonstrated clear genetic quired for accurate determination of the dynamics of hybridization
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