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Cytonuclear Diversity and Shared Mitochondrial Haplotypes Among Yin et al. BMC Evolutionary Biology (2018) 18:130 https://doi.org/10.1186/s12862-018-1256-4 RESEARCHARTICLE Open Access Cytonuclear diversity and shared mitochondrial haplotypes among Daphnia galeata populations separated by seven thousand kilometres Mingbo Yin1*, Xiaoyu Wang1, Xiaolin Ma1, Sabine Gießler2, Adam Petrusek3, Johanna Griebel4, Wei Hu1 and Justyna Wolinska4,5 Abstract Background: The zooplanktonic cladocerans Daphnia, present in a wide range of water bodies, are an important component of freshwater ecosystems. In contrast to their high dispersal capacity through diapausing eggs carried by waterfowl, Daphnia often exhibit strong population genetic differentiation. Here, to test for common patterns in the population genetic structure of a widespread Holarctic species, D. galeata, we genotyped two sets of populations collected from geographically distant areas: across 13 lakes in Eastern China and 14 lakes in Central Europe. The majority of these populations were genotyped at two types of markers: a mitochondrial gene (for 12S rRNA) and 15 nuclear microsatellite loci. Results: Mitochondrial DNA demonstrated relatively shallow divergence within D. galeata, with distinct haplotype compositions in the two study regions but one widely distributed haplotype shared between several of the Chinese as well as European populations. At microsatellite markers, clear separation was observed at both large (between China and Europe) and small (within Europe) geographical scales, as demonstrated by Factorial Correspondence Analyses, Bayesian assignment and a clustering method based on genetic distances. Genetic diversity was comparable between the sets of Chinese and European D. galeata populations for both types of markers. Interestingly, we observed a significant association between genetic distance and geographical distance for D. galeata populations in China but not in Europe. Conclusions: Our results indicate relatively recent spread of D. galeata across wide expanses of the Palaearctic, with one mtDNA lineage of D. galeata successfully establishing over large distances. Despite a clear differentiation of Chinese and European D. galeata at a nuclear level, the pattern of genetic variation is nevertheless similar between both regions. Overall, our findings provide insights into the genetic population structure of a cladoceran species with extremely wide geographical range. Keywords: Cyclical parthenogenesis, Cladocera, Genetic variation, Microsatellites, 12S rRNA, Population structure * Correspondence: [email protected] 1MOE Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University, Songhu Road, Shanghai 2005, China Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Yin et al. BMC Evolutionary Biology (2018) 18:130 Page 2 of 12 Background galeata was detected throughout the Holarctic with A major challenge in our understanding of biodiversity is some haplotypes shared over long distances, even be- why certain species have a wide distribution, spanning tween Europe and North America. At the nuclear several biogeographical regions, while others have much marker level, however, New and Old World D. galeata more restricted ranges or are endemic. The cosmopolitan- were clearly differentiated [12]. Moreover, there was a ism view [1] holds that species with large population sizes mismatch between the patterns observed at these and strong dispersal abilities maintain genetic homogen- markers: five nuclear but only four mitochondrial phy- eity across widely dispersed geographical regions. For ex- logroups were detected [12], which was explained by nu- ample, many freshwater invertebrate species were clear introgression from D. dentifera to D. galeata in the considered to be cosmopolitan. This conclusion was based New World. However, populations from China, where on observed morphological similarities of specimens inha- D. galeata is a very common zooplankter [15], were not biting different continents and interpreted as a result of included in that previous survey, in which continental efficient dispersal mechanisms (e.g. [2]). However, the Asia was represented only by Siberian populations. Our classical view of cosmopolitanism has been challenged by recent study of the biogeography and diversity of D. extensive genetic studies. Specifically, despite the morpho- galeata across China revealed low mtDNA variation; a logical similarities across broad geographical ranges, many common D. galeata haplotype (as resolved by sequen- freshwater zooplankton species, including rotifers and cla- cing of 12S rRNA and cytochrome c oxidase subunit I) docerans, have been shown to display strong genetic di- was widespread across China, Japan, Siberia and the vergence not only at a global scale, but even at regional Western Palaearctic [15]. We also detected many rare levels (e.g. [3, 4]). At present, it is possible to detect even local mtDNA haplotypes in China, suggesting either that weak differentiation of population structure within spe- some time has passed since initial colonization, along cies, because of the wide availability of sufficiently variable with subsequent evolutionary change, or that multiple multi-locus nuclear and mitochondrial DNA (mtDNA) introductions occurred [15]. In contrast, nuclear differ- markers. Besides tracing maternal lines via mtDNA, local entiation based on variation of multiple microsatellite adaptation processes can be examined by analysis of nu- loci supported clear spatial differentiation among Chin- clear polymorphism (e.g. [5–7]). ese D. galeata populations even on a relatively small Here, we focus on a common and very widespread geographical scale (within 30 km, [19]). freshwater zooplankton species, the cladoceran Daphnia The aim of the present study was to compare patterns galeata G. O. Sars, 1863, to improve our understanding of in the genetic population structure of the most wide- its dispersal and genetic diversity over small and large geo- spread species of the D. longispina complex, D. galeata graphic scales. Daphnia (Anomopoda: Daphniidae) are [20, 21], between two distant areas, and to identify com- important components of freshwater ecosystems, being mon or potentially distinct features. We compared the grazers of phytoplankton as well as a key prey item of genotypic diversity of two sets of D. galeata populations planktivorous fish [8]. Daphnia are cyclical parthenogens; (from Eastern China and Central Europe) using two females mostly reproduce clonally by giving birth to par- types of markers, a mitochondrial gene (12S rDNA re- thenogenetic daughters. In unfavourable environments, gion) and 15 nuclear microsatellite loci. In the case of however, Daphnia switch to the production of males and mtDNA, we expected pronounced divergence of D. sexual eggs which require fertilization, and then enter dia- galeata between the two study regions, but low variation pause in a gastrula stage [9]. Daphnia galeata,amember within them, as mitochondrial DNA usually has low of the D. longispina complex (taxonomy revised in: [10]), resolution to detect subtle within-species population dif- has a wide Holarctic distribution [11], being common in ferentiation (e.g. [22]). When applying microsatellite freshwater lakes in Europe, North America and Asia (e.g. markers, we expected to observe significant variation [11–16]). This broad geographical range of D. galeata ap- among populations of D. galeata, both within and be- parently results from long-distance passive dispersal of tween remote regions. Genetic diversity in this instance sexually produced diapausing eggs, which can be carried is derived from a high number of fast evolving poly- among water bodies by waterfowl (e.g. [17, 18]). Surpris- morphic loci and, because of their codominant inherit- ingly, despite the high dispersal capacity of anomopod cla- ance, discrimination among populations at high docerans, substantial genetic differentiation has been resolution is possible [23]. detected among studied populations, across different Daphnia species (e.g. [5, 6]). Methods Ishida and Taylor [12] surveyed D. galeata populations Daphnia specimen collection across Holarctic continents, using both a mitochondrial Thirteen Chinese and fourteen European Daphnia DNA (mtDNA) marker and a conservative nuclear galeata localities were analysed in this study (Fig. 1). All marker (i.e. HSP90). One major mtDNA type of D. Chinese lakes are located in the eastern plain (lakes Yin et al. BMC Evolutionary Biology (2018) 18:130 Page 3 of 12 Fig. 1 Location of D. galeata samples from Eastern China (red dots) and Central Europe (green dots) elsewhere in China are mostly inhabited by another spe- using GeneMapper version 3.7 (Applied Biosystems), cies from the D. longispina complex, D. dentifera [15]). and the alleles at each locus were defined by their frag- Among European localities, nine are located in ment length (in
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