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Lineage Diversity, Morphological and Genetic Divergence in Daphnia Magna (Crustacea) Among Chinese Lakes at Different Altitudes

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Lineage Diversity, Morphological and Genetic Divergence in Daphnia Magna (Crustacea) Among Chinese Lakes at Different Altitudes Contributions to Zoology 89 (2020) 450-470 CTOZ brill.com/ctoz Lineage diversity, morphological and genetic divergence in Daphnia magna (Crustacea) among Chinese lakes at different altitudes Xiaolin Ma* Ministry of Education, Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University, Songhu Road 2005, Shanghai, China Yijun Ni* Ministry of Education, Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University, Songhu Road 2005, Shanghai, China Xiaoyu Wang Ministry of Education, Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University, Songhu Road 2005, Shanghai, China Wei Hu Ministry of Education, Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University, Songhu Road 2005, Shanghai, China Mingbo Yin Ministry of Education, Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University, Songhu Road 2005, Shanghai, China [email protected] Abstract The biogeography and genetic structure of aquatic zooplankton populations remains understudied in the Eastern Palearctic, especially the Qinghai-Tibetan Plateau. Here, we explored the population-genetic di- versity and structure of the cladoceran waterflea Daphnia magna found in eight (out of 303 investigated) waterbodies across China. The three Tibetan D. magna populations were detected within a small geo- graphical area, suggesting these populations have expanded from refugia. We detected two divergent mi- tochondrial lineages of D. magna in China: one was restricted to the Qinghai-Tibetan Plateau and the * Contributed equally. © Ma et al., 2020 | doi:10.1163/18759866-bja10011 This is an open access article distributed under the terms of the cc by 4.0 license. Downloaded from Brill.com10/07/2021 10:50:12PM via free access GENETIC DIVERSITY OF DAPHNIA MAGNA IN CHINA 451 other was present in lowland China. Several different haplotypes in the Qinghai-Tibetan Plateau were most similar to those from various parts of Siberia, suggesting that as a source region. We also found sub- stantial genetic differentiation between D. magna populations from the Qinghai-Tibetan Plateau and those from lowland China. Moreover, significant morphological differences were identified: D. magna from the Qinghai-Tibetan Plateau had a larger head length, body length and body width than did those from lowland China. Geographical and environmental factors were correlated with the observed morpho- logical variation and genetic divergence of D. magna in China. Our data offer an insight into the diver- gence of freshwater zooplankton due to the uplift of the Qinghai-Tibetan Plateau. Keywords Daphnia magna – genetic divergence – refugia – the Qinghai-Tibetan Plateau Introduction ponents of freshwater ecosystems, being key grazers of phytoplankton as well as main prey Freshwater invertebrates have frequently for planktivorous fish (Lampert, 2011). Daph- been studied to investigate biogeographical nia magna Straus, 1820 has been frequently principles. Of particular interest has been the subjected to ecotoxicological, ecological, evo- genetic diversity across their geographical lutionary, biogeographical and physiological range, which is often very wide (Taylor et al., studies (e.g., De Gelas & De Meester, 2005; 1998) as a consequence of efficient dispersal Koussoroplis et al., 2019; Lee et al., 2019; Sey- mechanisms (e.g., Havel & Shurin, 2004; Mayr, oum & Pradhan, 2019). This species is widely 1963). Indeed, many freshwater invertebrate distributed, being detected in Africa, Asia, species were assumed in the past to be cosmo- Europe and North America (e.g., Bekker et al., politan because of morphological similarities 2018; Brooks, 1957; Fields et al., 2015; Xu et al., of specimens inhabiting different continents 2018). Moderate to high levels of genetic dif- (Mayr, 1963). However, in-depth morphologi- ferentiation within D. magna are often found cal analyses, especially when integrated with between different continents and within con- molecular data, have identified the diagnostic tinents (e.g., De Gelas & De Meester, 2005; characters of specific lineages and thus led to Fields et al., 2015). For example, moderate recognition and description of new species overall genetic divergence (based on a mito- (e.g., Juracka et al., 2010; Kotov et al., 2006; chondrial gene marker) was detected across Zuykova et al., 2018b). The application of mo- the European range, and high genetic dif- lecular tools has also demonstrated substan- ferentiation was even found on a local scale tial genetic divergence among populations of (De Gelas & De Meester, 2005). By using freshwater zooplankton taxa (e.g., Rotifera restriction-site associated DNA sequencing, and Cladocera) not only at global (e.g., Pe- a clear spatial genetic structure of D. magna trusek et al., 2004; Xu et al., 2009), but also at was apparent across its Eurasian range, sug- regional scale (e.g., Gomez et al., 2000; Ni gesting a geographical distance component et al., 2019; Penton et al., 2004). in the genetic differentiation of D. magna on a The many species in the cladoceran genus continental scale (Fields et al., 2015). Applying Daphnia Müller, 1785 (Anomopoda: Daph- synonymous substitutions and microsatellites niidae) are among the most important com- as genetic markers,Downloaded higher from levels Brill.com10/07/2021 of divergence 10:50:12PM via free access 452 MA ET AL. were found among D. magna populations Plateau) to the relatively low-altitude popula- from northern Eurasia relative to those from tions in the east (here collectively termed low- southern/central Eurasia (Walser & Haag, land China). First, we investigated morpho- 2012). A more recent study explored a deep logical variation of D. magna populations split between East Asian and Western Eur- from the Qinghai-Tibetan Plateau relative to asian D. magna lineages by using the whole populations from lowland China. Then, we mitochondrial genomes (Fields et al., 2018). used the mitochondrial COI marker and a set In China, D. magna has been found in the of nuclear microsatellite loci to investigate the Eastern Plain, the Inner Mongolia-Xinjiang genetic diversity and structure of D. magna Plateau, the Northeastern Plain and the Qin- populations from China. We expected to de- ghai-Tibetan Plateau in the 1970s (Chiang & tect substantial genetic divergence between Du, 1979). This distribution suggests that D. D. magna populations from the Qinghai-Ti- magna can occupy a wide range of habitats, betan Plateau and those from lowland China, from relatively high-altitude locations in the given the significant differences in geographi- west (the Qinghai-Tibetan Plateau) to rela- cal and environmental factors between these tively low-altitude regions in the east (lowland regions. China). The Qinghai-Tibetan Plateau, in par- ticular, has a special environment: extremely low temperatures and strong ultraviolet ra- Materials and methods diation (Clewing et al., 2016; Niu et al., 2019). This unique environment should lead to the Sample collection adaptive divergence of local species (Favre Daphnia magna samples were recovered et al., 2015; Hoorn et al., 2013). A recent study from eight of 303 waterbodies across China using DNA barcoding evaluated the species from 2012 to 2018 (during the growing sea- diversity of Daphnia from the Qinghai-Tibet- sons of Daphnia), using a 125-μm plankton an Plateau in China and identified six species net hauled vertically at two or three sites per (or species complexes), including D. tibetana locality, from a boat or from the shore. Sam- Sars, 1903, D. longispina species complex, ples from the same waterbody were pooled D. magna, D. pulex species complex, D. cf. hi- and preserved in 95% ethanol. All D. magna malaya Manca, 2006 and D. similoides Hudec, specimens were identified morphologically 1991 (Xu et al., 2018). Most recently, by applying (Benzie, 2005; Chiang & Du, 1979). The eight a set of high-resolution microsatellite makers, waterbodies containing this species were two we found that D. sinensis Gu, 2013 populations natural lakes, one artificial reservoir and five from Eastern China and the Qinghai-Tibetan ponds, representing five main geographical re- Plateau of Western China were genetically gions of China: Eastern Plain, Inner Mongolia-­ separated from each other (Ma et al., 2019a). Xinjiang Plateau, Northeastern Plain, Yunnan-­ However, there have been no specific studies Guizhou Plateau and Qinghai-Tibetan Plateau on genetic diversity or population structure of (table 1 and fig. 1A). For each locality, the fol- D. magna from the Qinghai-­Tibetan Plateau, lowing information was collected: geographi- or even from China overall. cal position (latitude and longitude), altitude, In this study, we analyzed D. magna popu- habitat origin (natural or artificial), surface lations found in eight out of 303 waterbodies area, maximum depth, predators (presence sampled across China. These populations dif- or absence of fish) and whether the water- fer in their types of habitat, from high-altitude body freezes in winter (this infor­mation was populations in the west (the Qinghai-Tibetan obtained from localDownloaded residents). from Brill.com10/07/2021 Additionally,­ 10:50:12PM via free access GENETIC DIVERSITY OF DAPHNIA MAGNA IN CHINA 453 the trophic status (eutrophic, mesotrophic or 0.005% NP-40. Individuals were incubated oligotrophic) was assigned
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