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Population Genetics and Sympatric Divergence of the Freshwater Gudgeon, Gobiobotia Filifer, in the Yangtze River Inferred from Mitochondrial DNA

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Population Genetics and Sympatric Divergence of the Freshwater Gudgeon, Gobiobotia Filifer, in the Yangtze River Inferred from Mitochondrial DNA Received: 14 November 2018 | Revised: 9 September 2019 | Accepted: 16 September 2019 DOI: 10.1002/ece3.5746 ORIGINAL RESEARCH Population genetics and sympatric divergence of the freshwater gudgeon, Gobiobotia filifer, in the Yangtze River inferred from mitochondrial DNA Dengqiang Wang1 | Lei Gao1 | Huiwu Tian1 | Weiwei Dong1,2 | Xinbin Duan1 | Shaoping Liu1 | Daqing Chen1 1Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Science, Abstract Wuhan, China The ecosystem and Pleistocene glaciations play important roles in population de- 2 School of Life Science, Southwest mography. The freshwater gudgeon, Gobiobotia filifer, is an endemic benthic fish in University, Chongqing, China the Yangtze River and is a good model for ecological and evolutionary studies. This Correspondence study aimed to decode the population structure of G. filifer in the Yangtze River and Daqing Chen, Yangtze River Fisheries Research Institute, Chinese Academy of reveal whether divergence occurred before or after population radiation. A total of Fishery Science, Wuhan, Hubei 430223, 292 specimens from eight locations in the upper and middle reaches of the Yangtze China. Email: [email protected] River were collected from 2014 to 2016 and analyzed via mitochondrial DNA Cyt b gene sequencing. A moderately high level of genetic diversity was found without Funding information National Natural Science Foundation of structures among the population. However, phylogenetic and network topology China, Grant/Award Number: 31602161; showed two distinct haplotype groups, and each group contained a similar propor- The Ministry of Agriculture and Rural Affairs, the People's Republic of China tion of individuals from all sampled sites. This suggested the existence of two geneti- cally divergent source populations in G. filifer. We deduced that a secondary contact of distinct glacial refugia was the main factor creating sympatric populations of G. fil- ifer, and climate improvement promoted population expansion and colonization. KEYWORDS Cyt b, genetic structure, Gobiobotia filifer, sympatric population 1 | INTRODUCTION fishes, and many fishes are only endemic in special sections or trib- utaries. Consequently, the genetic structures among populations The Yangtze River is the longest river in China and the third lon- are important for interpreting adaptation to heterogeneous envi- gest in the word, and it occupies various types of ecosystems. ronments. Additionally, the Pleistocene glaciations have had pro- According to the river characteristics, the river section above found effects on the phylogeography and historical demography Yichang City, Hubei Province, is considered the upper reaches, of species (Dynesius & Jansson, 2000; Hewitt, 2000). Freshwater and the section below Yichang City the middle and lower reaches. fishes were restricted in rivers or lakes and experienced a fluctu- There are approximately 361 fish species inhabiting the river ant landscape of intermittently connected and isolated watersheds basin, 177 of which are endemic (Fu, Wu, Chen, Wu, & Lei, 2003). and glacial refugia, which provides many opportunities to study Distribution patterns across the river are different for different phylogeography and speciation (Ruskey & Taylor, 2016; Ruzzante, This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2019;00:1–9. www.ecolevol.org | 1 2 | WANG ET AL. Walde, Macchi, Alonso, & Barriga, 2011; Taylor, 1999; Zhou, Song, Own to the specialized position in phylogeny and relatively broad Wang, Jie, & Gao, 2016). distribution, G. filifer is a good mode for studying the local adaptation The subfamily Gobiobotinae (Cyprinidae, Cypriniformes) is a and the effect of dam on fish. For the last decades, mitochondrial group of small freshwater gudgeon distributed in the rivers of East DNA has been proven to be an important tool in population history, Asia in Korea and China (Chen, 1998). Only two genera, Gobiobotia biogeography, genetic structure, and species delimitation (Hebert, and Xenophysogobio, with 17 species belong to this subfamily, and all Penton, Burns, Janzen, & Hallwachs, 2004; Moore, 1995). In this the fishes are benthic. He (1991) examined the skeletons and classi- study, we used cytochrome b (Cyt b) to examine population genetic fied Xenophysogobio as a primitive species and Gobiobotia filifer as a diversity of G. filifer. We aimed to (a) reveal whether genetic diver- specialized species. Wang, He, and Chen (2002) used mitochondrial gence occurred within the population and (b) determine whether di- DNA (mtDNA) data to construct the phylogenetic relationship that vergence occurred before or after population radiation. supported this idea. They also inferred that Gobiobotinae originated in the upper reaches of the Yangtze River. At present, four fishes, including X. boulengeri, X. nudicorpa, G. abbreviata, and G. filifer, live 2 | MATERIALS AND METHODS in the upper reaches of the Yangtze River. However, except for these four fishes, sympatric habitation among Gobiobotinae fishes is rare, 2.1 | Sampling and DNA extraction indicating that they could have quickly adapted and specialized to new ecological environments. A total of 292 individuals of G. filifer were collected from eight loca- Gobiobotia filifer is endemic to the Yangtze River basin (Chen, tions from 2014 to 2016; four locations were in the upper reaches of 1998), and the limits of its native range extend from the Yibin City the Yangtze River and four in the middle reaches (Table 1; Figure 1). to downstream, including tributary rivers such as Min River, Chishui A small fin sample was clipped and preserved in 95% ethanol for River, Hanjiang River, and Xiangjiang River (Figure 1). This fish pro- each specimen. duces drifting eggs in spawning reason (Liu et al., 2018; Tian et al., Genomic DNA was extracted using an easy-DNA Kit (Omega) 2017) and feeds on benthic organisms. The Gezhouba Dam was following the manufacturer's instructions. completed in 1988 in Yichang City, and then, the Three Gorges Dam with 175 m of water deep was completed in 2006, which form physical and ecological barriers to genetic exchange among pop- 2.2 | PCR and sequencing ulations. Recent surveys found that the abundance of G. filifer in upper Yangtze River was relatively high comparing with that before The cytochrome b (Cyt b) gene was amplified using polymerase chain the construction of the Three Gorges Dam (Fan, Ba, & Duan, 2012; reaction (PCR) with primers L14742 and H15915 (Xiao, Zhang, & Liu, Xiong, Liu, Duan, Liu, & Chen, 2015; Yang, Xin, Ma, Kong, & Liu, 2001). Each 50 μl PCR contained 1–10 ng of template DNA, 5 μl of 2010). However, it was less common in section and tributary rivers 10 × PCR buffer, 1 μl of dNTP mix (10 mM), 10 pmol of each primer, below the dams now (Fan et al., 2012). and 2 U of rTaq polymerase (TaKaRa). PCRs were conducted in a FIGURE 1 Map showing the eight sampling locations (black dots), sample sizes, abbreviated as in Table 1, with the relative frequency of the two HapGroups (HapGroup 1 and HapGroup 2) WANG ET AL. | 3 TABLE 1 Sampled sites and sizes, population genetic parameters, and neutrality tests for the Gobiobotia filifer populations Geographical Sample Haplotype Haplotype Nucleotide Sampling location Abbreviation coordinates size number diversity, Hd diversity, π Tajima's D Fu's Fs Yibin City, Yangtze YYB 28°76′N 104°63′E 67 18 0.877 0.0076 0.9775 0.171 River Hejiang County, YHJ 28°81′N 105°83′E 14 3 0.692 0.0052 0.7419 6.439 Yangtze River Jiangjin City, Yangtze YJJ 29°27′N 106°28′E 70 17 0.815 0.0064 0.7364 −0.109 River Chishui City, Chishui CCS 28°58′N 105°69′E 54 15 0.827 0.0068 0.5177 0.474 River Jingzhou City, Yangtze YJZ 30°30′N 112°24′E 24 16 0.946 0.0080 −0.1841 −3.530* River Jianli County, Yangtze YJL 29°53′N 112°93′E 31 14 0.886 0.0068 −0.0845 −0.928 River Honghu City, Yangtze YHH 30°07′N 114°01′E 18 10 0.935 0.0083 0.8021 0.384 River Miluo City, Xiangjiang XXJ 28°85′N 112°89′E 14 13 0.989 0.0088 0.2064 −4.737** River HapGroup 1 203 34 0.803 0.0020 −2.1016* −27.182** HapGroup 2 89 32 0.891 0.0025 −1.4959 −27.454** Total 292 66 0.893 0.0072 −0.736 −28.076** *Significant level at p < .05. **Extremely significant at p < .01. thermal cycler (T100; Bio-Rad) with the following program: one cycle Kimura 2-parameter distance method was carried out in MEGA of denaturation at 95°C for 4 min; 30 cycles at 94°C for 30 s, 56°C 7.0 (Kumar, Stecher, & Tamura, 2016). The tree nodes and branch for 30 s, and 72°C for 90 s; and one final cycle at 72°C for 10 min. lengths were statistically tested using the bootstrap method with Successful PCR products were separated by electrophoresis on a 1,000 replicates and an interior branch test, respectively. BI analy- 1.0% agarose gel and purified using the Agarose Gel Purification Kit sis was carried out using MrBayes v3.1.2 (Ronquist & Huelsenbeck, (Qiagen). 2003). Best-fit models for the Bayesian analysis were inferred by hi- Several samples with distinct phylogenetic clades were also used erarchical likelihood ratio tests on the IQ-TREE Web server (http:// to test the existence of cryptic species using COI gene. The primers iqtree.cibiv.univie.ac.at/). and PCR information were as Ward, Zemlak, Innes, Last, and Hebert Pairwise FST values and analysis of molecular variance (AMOVA) (2005). were used to assess the population configuration in Arlequin v3.5 Purified products then were sequenced with an ABI PRISM (Excoffier & Lischer, 2010).
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