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Characterization of Novel Microsatellite Markers of the Emei Yang et al. Avian Res (2017) 8:13 DOI 10.1186/s40657-017-0071-8 Avian Research RESEARCH Open Access Characterization of novel microsatellite markers of the Emei Shan Liocichla using restriction site‑associated DNA sequencing Ailin Yang1, De Chen1, Pengcheng Wang1, Yiqiang Fu2* and Zhengwang Zhang1* Abstract Background: The Emei Shan Liocichla (Liocichla omeiensis) is an endemic bird species to southwestern China with a small geographic range. However, little was known about the genetic status of this threatened species. Methods: We applied restriction-site-associated DNA sequencing (RAD-Seq) for rapid mass identifcation of micros- atellite markers of the Emei Shan Liocichla. Results: A total of 11,564 microsatellite sequences were obtained, 600 random loci were designed for screening and 24 polymorphic microsatellite loci were selected for further validation. The average allele number, average observed heterozygosity and average expected heterozygosity were relatively low in our samples, which were 6.08, 0.6618 and 0.7048, respectively, indicating that the Emei Shan Liocichla might have lost some genetic diversity. Further analyses suggested that the populations distributed on two mountains (Daxiangling and Xiaoliangshan) showed a modest degree of genetic diferentiation. Conclusions: These novel microsatellite markers provided valuable preliminary knowledge regarding the genetic status of the Emei Shan Liocichla and can be useful in further studies, as well as in the management and conservation of this species. Keywords: Liocichla omeiensis, Fragmentation, Nuclear markers, Genetic diversity, Gene fow Background inbreeding depression (Keller and Waller 2002; Arm- Genetic diversity is crucial for the sustainability of spe- strong and Seddon 2008; Jamieson 2011). It is, therefore, cies, especially for threatened species (Mefe and Car- necessary to assess the genetic diversity and inbreeding roll 1994). Habitat fragmentation, a common cause of level, and to determine whether a population is geneti- endangering threatened species, can lead to reductions cally fragmented before undertaking the genetic manage- in the population size and gene fow among patches, ment actions for threatened species, which are important which leads to a loss of genetic diversity and an increase in biodiversity conservation (Frankham et al. 2002). in inbreeding (Frankham et al. 2002). Te loss of genetic Microsatellites have a higher mutation rate compared diversity associated with inbreeding has two impor- to mitochondrial DNA and nuclear introns (Ryman tant consequences: it reduces the ability of populations and Leimar 2008), a feature that can provide a power- to adapt to environmental/climate change, and it can ful tool for detecting genetic diferences, especially in result in a direct and immediate loss in ftness through small and fragmented populations (Li et al. 2002; Dun- can et al. 2016). Microsatellite markers have been widely applied in molecular ecology and conservation genetic *Correspondence: [email protected]; [email protected] 1 Ministry of Education Key Laboratory for Biodiversity and Ecological studies since the 1990s (Bruford and Wayne 1993; Jarne Engineering, College of Life Sciences, Beijing Normal University, and Lagoda 1996; Chapuis et al. 2015; Faria et al. 2016). Beijing 100875, China Although cross-species amplifcation works for a few 2 College of Life Sciences, Leshan Normal University, Leshan, Sichuan 614000, China closely related taxa (Dawson et al. 2010; Gu et al. 2012), © The Author(s) 2017. 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. Yang et al. Avian Res (2017) 8:13 Page 2 of 8 the major drawback of microsatellites is that they need Shan Liocichla that can be useful for further studies, and to be independently isolated from most species (Sud- tried to understand some preliminary genetic status to heer et al. 2010). Most microsatellites must be identifed help the management and conservation of this vulner- by screening genomic libraries with appropriate probes able species using our incomplete sampling by answering or enrichment protocols, which are inefcient and time- the following questions: (1) how much genetic diversity consuming (Zane et al. 2002). Whereas the Illumina next is there in our sampling populations? (2) are the popula- generation sequencing (NGS) platform, which can pro- tions sufering from inbreeding? (3) are the populations duce moderately long paired-end reads (up to 150 bp from two mountains already genetically fragmented? and with the HiSeq 2500 platform), is an efective method for (4) what we can do for conservation of the Emei Shan obtaining reliable microsatellites, even for birds that have Liocichla? few microsatellite loci (Castoe et al. 2012). Te restric- tion-site-associated DNA (RAD) method (Miller et al. Methods 2007) with Illumina sequencing (RAD-Seq) can further Sample collection and DNA purifcation reduce the cost and improve the average depth per locus Fifty-one samples containing 38 blood and 13 tissue sam- (Baird et al. 2008). Unlike other methods for generating ples, were collected from six sites distributed in Daxi- genome-wide data, RAD-Seq does not require any prior angling Mountain and Xiaoliangshan Mountain located genomic information of the taxa being studied (Andrews in southwestern Sichuan, China (Fig. 1). Blood samples et al. 2016). To date, several studies have shown that were collected from the brachial vein and stored in abso- paired-end RAD-Seq is a powerful tool for obtaining lute ethanol. All the captured individuals were released microsatellites in both model and non-model species immediately after the blood samples were obtained. (Miller et al. 2007; Pfender et al. 2011). Tissue samples were collected opportunistically from Te vulnerable (VU) Emei Shan Liocichla (Liocichla individuals that died naturally and dead chicks in nests. omeiensis) is an endemic passerine bird found on Daxi- Permission for the sampling was granted by the Sichuan angling Mountain and Xiaoliangshan Mountain in south- Forestry Department and the Laojunshan National western China. It lives on the edges or gaps of natural Nature Reserve of Sichuan Province, China. Te samples broadleaf forests between an elevation of 1450 and 2150 m were frozen in the feld and preserved at −80 °C in the (Fu et al. 2011). Tis bird is resident and moves vertically lab. Total genomic DNA was extracted using TIANamp between seasons (Fu and Zhang 2011). Additionally, the Genomic DNA Kit DP304-2 (Tiangen, China) following Emei Shan Liocichla is socially monogamous and pro- the manufacturer’s recommendations. tects its territory continually throughout the year, with a territory range of approximately 10,000 m2 (Fu, unpub- RAD‑Seq and microsatellite characterization lished data). However, the population of the Emei Shan In total, 3 µg of genomic DNA from a single male was Liocichla is suspected to be declining at a moderate rate, sent to Novogene Bioinformatics Technology Co., Ltd. which is in line with the accelerated habitat loss and deg- (Beijing, China) for the DNA library preparation and radation within its range (BirdLife International 2017). Te sequencing to obtain sequencing data for microsatellite natural broadleaf forests in its habitat have been cleared or screening. We used P1 and P2 adaptors for the restric- replaced by non-native coniferous forests and tea planta- tion enzyme sites to construct a DNA sequencing library tions, which might lead to habitat fragmentation as a pre- vious study has shown the Emei Shan Liocichla did not use these types of vegetation (Fu et al. 2011). Habitat loss and fragmentation are regarded as the major factors contribut- ing to the population decline in many bird species (Ribon et al. 2003; Gill 2007). In addition, during our sampling period, we witnessed a number of captures of these birds for sale, which will also damage the population. Although conservation actions have been taken since 1999, little is known about the genetic status of this vulnerable species and its populations. Terefore, to carry out genetic diag- noses before undertaking genetic management actions (Frankham et al. 2002), a set of suitable genetic markers, such as microsatellites, are urgently needed. In this study, we utilized Illumina paired-end RAD-Seq Fig. 1 Sample locations of the Emei Shan Liocichla (Liocichla omeien- to isolate highly polymorphic microsatellites of the Emei sis) Yang et al. Avian Res (2017) 8:13 Page 3 of 8 with a size range of 300–700 bp. Paired-end 125 bp reads (FIS) were conducted by Arlequin 3.5.2.2 (Excofer and were obtained from separate lanes of the Hiseq 2500 Lischer 2010). Te resulting p values were adjusted Genome Analyzer. Poor-quality reads were cleaned and by applying a sequential Bonferroni correction using adapter reads were trimmed using Trimmomatic 0.36 SGoF+ 3.8 (Carvajal-Rodriguez and de Uña-Alvarez (Bolger et al. 2014) with default settings. Reads con- 2011). A maximum-likelihood estimate of the fre- taining RAD tags were clustered by diferent RAD tags quency of null alleles and allelic dropout was calculated using cd-hit-est (Li and Durbin 2009), and RAD tags for each locus using Micro-Checker 2.2.3 (Van Ooster- containing 10‒400 reads were considered repetitive and hout et al. 2004). Genetic diferential index (FST) for the removed. Te remaining paired-end reads from each populations between two mountains was estimated in RAD site were then sent to Velvet (Zerbino and Birney GENETIX 4.05.2 using 1000 bootstraps to calculate sig- 2008) to assemble contigs with the following parameters nifcance (Belkhir et al. 2004). We used BayesAss 3.03 to settings: VelvetOptimiser.pl -s 23 -e 31 -x 4.
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