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Phylogeographic Relationships of Scotophilus Kuhlii Between Hainan Island and Mainland China

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Phylogeographic Relationships of Scotophilus Kuhlii Between Hainan Island and Mainland China Mammal Study 37: 139–146 (2012) © The Mammal Society of Japan Phylogeographic relationships of Scotophilus kuhlii between Hainan Island and mainland China Wenhua Yu1,3, Zhong Chen3, Yuchun Li2,* and Yi Wu1,* 1 College of Life Science, Guangzhou University, Guangzhou 510006, China 2 Marine College, Shandong University at Weihai, Weihai 264209, China 3 Department of Biology, Hainan Normal University, Haikou 571158, China Abstract. Phylogeographic analysis of Scotophilus kuhlii between Hainan Island and Guangdong Province was conducted to validate the existence of two subspecies separated by the Qiongzhou Strait. A total of 37 individuals from 3 assumed populations (8 roosts) were examined using 617 bp mtDNA control region segments. Nineteen individuals from cross-strait populations of Hainan Island and the mainland shared 3 of 13 haplotypes. Overall nucleotides diversity was 0.003, a low genetic variation level compared to previous reports for other chiropteran species. The neutral test, mismatch distribution, and star-like TCS network suggested a bottleneck effect occurring at 21,000 years BP during the last glacial maximum and a subsequent population expansion at 7,000 years BP, corresponding with a global warming period. AMOVA analysis, intertwined haplotypes in the TCS network, and rejection of “Isolation by Distance” by the Mantel test indicated no distinct population structure among these populations. Three populations seem to have been derived from a single panmictic unit and the Qiongzhou Strait did not hinder gene flow. Our result, a striking difference in population structure compared with other sympatric chiropteran phylogeographic reports, may indicate variations in the barrier effect of the strait in different species. Based on these results, we suggest that the cross-strait population should be classified as one subspecies, namely S. k. consobrinus, instead of two traditional subspecies. Key words: Hainan Island, lesser yellow bat, phylogeography, Scotophilus kuhlii, subspecies. Islands have been described as valuable natural laborato- graphic barrier of the Qiongzhou Strait, comprising 22% ries in the macroevolution and speciation of organisms of chiropteran species of Hainan (Wang 2003). However, (e.g., Darwin 1859; Wallace 1880; MacArthur and most of these subspecies lack validation from phylogeo- Wilson 1967; Diamond 1975). Indeed, island popula- graphic or metrical evidence. Several phylogeographic tions may be less affected by gene flow from continental reports have examined the barrier effect of the Qiong- populations due to the barrier effect of a strait, and zhou Strait in cross-strait populations, such as Grey- rapidly evolve into new subspecies or new species cheeked fulvetta (Alcippe morrisonia) (Zou et al. 2007; under the effective and sufficient time scale of geograph- Song et al. 2009), spiny tree fern (Alsophila spinulosa) ic segregation, genetic drift and mutations (Phillimore (Su et al. 2005), Japanese Pipistrelle (Pipistrellus abra- et al. 2008). mus) (Wei et al. 2010), and intermediate horseshoe bat Hainan Island is the second largest island in China, (Rhinolophus affinis) (Mao et al. 2010). However, these with an area of 34,000 km2, separated from mainland species are all of low dispersal capability; a different China by the Qiongzhou Strait, which is 18–33.5 km in outcome might be expected in examining the genetic width (Yan 2008). Hainan Island is one of the valuable structure of species with strong dispersal capability. tropical areas of China, with the highest abundance of The lesser Asiatic yellow bat (Scotophilus kuhlii), a chiropteran species (Li et al. 2005). Traditionally, 7 vespertilionid species occupying Hainan Island and chiropteran species in Hainan Island have been described southern China (Zhang et al. 1997; Wang 2003), is of as geographic subspecies due to the presumed biogeo- high wing loading and moderately high aspect ratio, *To whom correspondence should be addressed. E-mail: [email protected] or [email protected] 140 Mammal Study 37 (2012) which implies their capability for long distance and Our purposes were: 1) to examine the population genetic steady flight (Norberg and Rayner 1987; Kitchener et al. structure and evolutionary history in cross-strait popula- 1990; Kunz and Fenton 2003; Pottie et al. 2005). This tions of S. kuhlii; 2) to certify the validity of subspecies species could be a good indicator for the examination of differentiation of S. kuhlii on both sides of the Qiong- the variations of the strait barrier effect compared to bats zhou Strait by phylogeographic perspective. with low dispersal capability. Furthermore, their subspe- cies taxonomy is still the subject of debate. Wang (2003) Materials and methods suggested that there are 3 subspecies occupying southern areas of China: Huanan subspecies (S. k. swinhoei Blyth, Samples and DNA extraction 1860), distributed in Guangdong, Guangxi, Fujian, and A total of 37 specimens of S. kuhlii were collected in Hong Kong; Hainan subspecies (S. k. consobrinus Allen, Guangdong and Hainan from 1999 to 2007 (Fig. 1). All 1906), distributed in Hainan (type locality) and Taiwan samples were preserved in 70–100% ethanol for use. For Island; and Thailand subspecies (S. k. gairdneri Kloss, the mainland specimens, we assigned specimens from 1917), distributed in the southern part of Yunnan. How- Guangzhou, Huizhou, Zhongshan, and Longmen to one ever, Smith and Xie (2008) argue that there is only one population, namely the Pearl River Delta population subspecies (S. k. consobrinus) in China. (abbreviated as PRD) because of close distances <200 In this study, we used the control region of mitochon- km among these sites, while specimens from Gaozhou drial DNA (mtDNA) to assess the genetic variation were assigned to Gaozhou population (GZ). Specimens between the populations of Hainan Island and the nearby from Hainan Island were assigned to Hainan population Chinese mainland separated by the Qiongzhou Strait. (HN). Fig. 1. Sampling locales of Scotophilus kuhlii. The specimen number is showed for each locale, and the number of female individual of each locale is showed in parentheses. Yu et al., Phylogeography of S. kuhlii in China 141 DNA sequencing and data analysis The goodness-of-fit test based on the sum of squared Genomic DNA was isolated from approximate 20 mg deviations (SSD) was performed to test for the signifi- of muscle tissue using the Universal Genomic DNA cance of fit of distribution by parametric bootstrapping Extraction Kit (TAKARA). A partial segment of mtDNA (10,000 replicates). For smooth and unimodal distribu- control region was amplified by polymerase chain reac- tion where an expansion model could not be rejected, we tion (PCR) using the primers C (5'-TGA ATT GGA further estimated the time of the expansion from the rela- GGA CAA CCA GT-3') and primer E (5'-CCT GAA tionship τ = 2ut, where u is the mutation rate per locus GTA GGA ACC AGA TG-3') (Wilkinson and Chapman per generation. We used a divergence rate of 20% per 1991). This portion of the control region spans the million years (Ma), which had been widely used in phy- hypervariable domain (HVI), which is of proven impor- logeographic analyses of other bats (Petit et al. 1999; tance in the study of intraspecific variation (Vigilant et Salgueiro et al. 2004; Chen et al. 2006; Mao et al. 2010), al. 1991; Wilkinson and Fleming 1996). PCRs were and a generation time of 1 year based on recapture exper- carried out in a final volume of 50 μl, containing iment and field observations of S. kuhlii in Guangdong approximately 5.0–50 ng DNA, 0.2 mM of each dNTP, from 2003 to 2005. This calibrated rate is consistent 0.4 mM of each primer, 1.5 mM MgCl2 and 2.0 U Taq with several other studies in mammalian species (see polymerase (TAKARA) in the manufacturer’s buffer. Petit et al. 1999) and should provide a rough estimate of Amplification was performed using a MyCycler Thermal divergence time even though it is not so unique at some Cycler (BioRad) with the following profile: 94°C 4 min; extent. Second, we derived Tajima’s D (Tajima 1989) 37 cycles of 94°C for 30 sec, 50°C for 30 sec, 72°C for and Fu’s Fs (Fu 1997) statistics in ARLEQUIN 3.01 and 1 min; 72°C for 5 min. DNA sequencing was performed assessed their significance by simulation (10,000). on an ABI PRISM 3700 DNA Analyser (Applied Bio- Third, we used Bayesian MCMC approach implemented systems). The chromatograms were edited with BIO- in BEAST 1.43 (Drummond and Rambaut 2007) to esti- EDIT (Hall 1999) and aligned using CLUSTAL_X mate the time to the most recent common ancestor (Thompson et al. 1997). (TMRCA) of the whole population. We applied an The number of haplotypes, haplotype diversity (h), HKY model of evolution based on MODELTEST 3.06 and nucleotide diversity (π) for the 3 populations were (Posada and Crandall 1998), and a relaxed-clock model calculated using ARLEQUIN 3.01 (Excoffier et al. with an uncorrelated lognormal distribution for the sub- 2005). In order to estimate the partitioning of genetic stitution rate. We performed two independent runs for variation among 3 different populations and between 2 10 million generations, each with a burn-in of 1 million subspecies, a hierarchical analysis of molecular variation generations, and sampled every 1,000 steps. Both results (AMOVA) (Excoffier et al. 1992) was performed with were then combined in TRACER 1.4 (Rambaut and 1,000 permutations in ARLEQUIN (Excoffier et al. Drummond 2007). To convert the estimates scaled by 2005). Additionally, we used SAMOVA (Dupanloup et mutation rate to calendar years, we used the divergence al. 2002) to determine the maximum partitioning of rate of 20% Ma as applied in the above time estimation. genetic variation. We also calculated pairwise FST and Nm values across all populations using DNASP 4.10 Results (Rozas et al. 2003), and tested for genetic isolation by distance among 7 sampling locales using the Mantel test Sequence characteristics and genetic diversity as implemented in ARLEQUIN (Excoffier et al.
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