Abstract
In China, the status of Hipposideros armiger subspecies remains controversial. To elucidate the H. armiger taxonomy, we conducted a series of surveys of bats in different areas of China between 2011 and 2014. Bats were characterized by 16 external measurements, 25 skull measurements and the sequence analysis of two mitochondrial genes (cytochrome-b and D-loop). Our research indicated that the external and cranial measurements were similar in the samples from the six geographic regions. No obvious differences were detected in H. armiger morphology. Additionally, no significant cytochrome-b sequence divergence existed between the samples within a region (0–0.9%) and among the six regions (0–1.8%). The results obtained for the D-loop were similar, with 0–3.4% divergence within a region and 0–4.5% among the six regions. Moreover, no significant geographic differentiation was observed in the phylogenetic trees. Based on these morphological and molecular results, H. armiger is represented in China by only one subspecies, H. a. armiger.
Acknowledgments
This project was supported by the National Natural Science Foundation of China (NSFC, No. 31172056). We thank all those who helped in the field, especially Songqiang Zhao, Wenzhi Yang, Yankun Zhu, Zongxiao Zhang, Wei Liu, Yanxiao Wang and Xiao Sun. We also thank Lezhen Zhao, Hua Bai for tissue sampling. We are especially grateful to Dr. Xiaojin Zhao, Dr. Lina Jiang, Dr. Yun Shao for help in statistical advice and Dr. Chuanjiang Zhou for help in phylogenetic tree reconstruction.
Appendix
List of specimens examined in the present study for skull morphometrics (see Table 1 and text for abbreviations).
| Location | n | Specimen number |
|---|---|---|
| CE | ||
| Jiujiang City, Jiangxi | 3 | JX13.024 (♂), JX13.026 (♂), JX13.027 (♂) |
| Sanming City, Fujian | 2 | JX13.185 (♂), JX13.186 (♀) |
| CW | ||
| Huaihua City, Hunan | 2 | SX12.069 (♂), SX12.082 (♀) |
| Guangan City, Sichuan | 3 | G13.245 (♂), G13.250 (♀), G13.301 (♂) |
| Anshun and Kaili City, Guizhou | 6 | HG12.009 (♂), HG12.010 (♀), HG12.207 (♂), |
| HG12.209 (♂), HG12.236 (♂), XP14.251 (♂) | ||
| WS | ||
| Chuxiong, Dali, and Zhaotong City, Yunnan | 16 | XP14.029 (♂), XP14.044 (♂), XP14.045 (♂), |
| XP14.047 (♀), XP14.083-XP14.086 (♂), | ||
| XP14.130 (♀), XP14.133 (♀), XP14.138 (♀), | ||
| XP14.194 (♀), XP14.202 (♀), XP14.205 (♀), | ||
| XP14.222 (♀),XP14.223 (♀) | ||
| SM | ||
| Zhangzhou City, Fujian | 3 | JX13.297 (♀), JX13.314 (♀), JX13.322 (♀) |
| Heyuan City, Guangdong | 2 | JX13.400 (♂), JX13.454 (♀) |
| Chihe City, Guangxi | 3 | G13.237 (♀), G13.240 (♀), G13.241 (♀) |
| SY | ||
| Baoshan City, Yunnan | 10 | HG12.258 (♂), HG12.259 (♂), HG12.317 (♀), |
| XP14.142-XP14.145 (♂), XP14.159 (♀), | ||
| XP14.181 (♀), XP14.182 (♂) | ||
| SH | ||
| Baoting County, Hainan | 3 | JX13.748 (♂), JX13.749 (♂), JX13.751 (♀) |
References
Bates, P.J.J. and D.L. Harrison. 1997. Bats of the Indian subcontinent. Harrison Zoological Museum, Sevenoaks, UK. pp. 258.Search in Google Scholar
Bates, P., S. Bumrungsri, C. Francis and G. Csorba. 2008. Hipposideros armiger. The IUCN Red List of Threatened Species. Version 2014.3. www.iucnredlist.org. Downloaded on 15 December 2014.Search in Google Scholar
Bowen, B.W. and W.S. Grant. 1997. Phylogeography of the sardines (Sardinops spp.): assessing biogeographic models and population histories in temperate upwelling zones. Evolution 51: 1601–1610.10.2307/2411212Search in Google Scholar
Bradley, R.D. and R.J. Baker. 2001. A test of the genetic species concept: cytochrome-b sequences and mammals. J. Mammal. 82: 960–973.10.1644/1545-1542(2001)082<0960:ATOTGS>2.0.CO;2Search in Google Scholar
Cai, A.Z. and Q. Shi. 2009. A preliminary investigation into the genesis of Taiwan Strait. Xiamen University Press, Xiamen, China. pp. 200. (in Chinese).Search in Google Scholar
Cheng, H.C. and L.L. Lee. 2002. Postnatal growth, age estimation, and sexual maturity in the Formosan leaf-nosed bat (Hipposideros terasensis). J. Mammal. 83: 785–793.10.1644/1545-1542(2002)083<0785:PGAEAS>2.0.CO;2Search in Google Scholar
Degli Esposti, M., D.S. Vries, M. Crimi, A. Ghelli, T. Patarnello and A. Meyer. 1993. Mitochondrial cytochrome b: evolution and structure of the protein. BBA-Bioenergetics 1143: 243–271.10.1016/0005-2728(93)90197-NSearch in Google Scholar
Douangboubpha, B., S. Bumrungsri, P. Soisook, C. Satasook, N.M. Thomas and P.J. Bates. 2010. A taxonomic review of the Hipposideros bicolor species complex and H. pomona (Chiroptera: Hipposideridae) in Thailand. Acta Chiropterol. 12: 415–438.10.3161/150811010X537990Search in Google Scholar
Hiryu, S., K. Katsura, T. Nagato, H. Yamazaki, L.K. Lin, Y. Watanabe and H. Riquimaroux. 2006. Intra-individual variation in the vocalized frequency of the Taiwanese leaf-nosed bat, Hipposideros terasensis, influenced by conspecific colony members. J. Comp. Physiol. A. 192: 807–815.10.1007/s00359-006-0118-5Search in Google Scholar
Ho, Y.Y. and L.L. Lee. 2003. Roost selection by Formosan leaf-nosed bats (Hipposideros armiger terasensis). Zool. Sci. 20: 1017–1024.10.2108/zsj.20.1017Search in Google Scholar
Horikawa, Y. 1931. Monograph of Taiwanese mammals. Taiwan Natural History Society, Taipei, Taiwan. pp. 21. (in Japanese).Search in Google Scholar
Huelsenbeck, J.P. and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.10.1093/bioinformatics/17.8.754Search in Google Scholar
Irwin, D.M., T.D. Kocher and A.C. Wilson. 1991. Evolution of the cytochrome b gene of mammals. J. mol. Evol. 32: 128–144.10.1007/BF02515385Search in Google Scholar
Kishida, K. 1924. On the bats of Taiwan. Zool. Mag. Tokyo 36: 20–49. (in Japanese).Search in Google Scholar
Kuroda, N. 1940. A monograph of the Japanese mammals. Sanseido, Tokyo & Osaka, Japan. pp. 48. (in Japanese).Search in Google Scholar
Librado, P. and J. Rozas. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.10.1093/bioinformatics/btp187Search in Google Scholar
Lin, A.Q., G. Csorba, L.F. Li, T.L. Jiang, G.J. Lu, V.D. Thong, P. Soisook, K.P. Sun and J. Feng. 2014. Phylogeography of Hipposideros armiger (Chiroptera: Hipposideridae) in the Oriental Region: the contribution of multiple Pleistocene glacial refugia and intrinsic factors to contemporary population genetic structure. J. Biogeogr. 41: 317–327.10.1111/jbi.12163Search in Google Scholar
Mayr, E., E.G. Linsley and R.L. Usinger. 1953. Methods and principles of systematic zoology. McGraw Hill Book Company, New York, NY. pp. 317.Search in Google Scholar
Morii, R. 1975. Collection trip of Chiroptera to Formosa and Ryukyu Islands. J. Mammal Soc. Japan 6: 121–126. (in Japanese).Search in Google Scholar
Pan, Q.H., Y.X. Wang and K. Yan. 2007. A field guide to the mammals of China. China Forestry Publishing House, Beijing, China. pp. 420. (in Chinese).Search in Google Scholar
Posada, D. and K.A. Crandall. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.10.1093/bioinformatics/14.9.817Search in Google Scholar PubMed
Simmons, N.B. 2005. Order Chiroptera. In: (D.E. Wilson and D.A. Reeder, eds.), Mammal species of the World: a taxonomic and geographic reference. 3rd edition. The Johns Hopkins University Press, Baltimore, MD. pp. 312–529.Search in Google Scholar
Smith, A.T. and Y. Xie. 2008. A guide to the mammals of China. Princeton University Press, Princeton, USA. pp. 544.Search in Google Scholar
Sun, K., J. Feng, L. Jin, Y. Liu, L. Shi and T. Jiang. 2009. Structure, DNA sequence variation and phylogenetic implications of the mitochondrial control region in horseshoe bats. Mammal. Biol. 74: 130–144.10.1016/j.mambio.2008.09.002Search in Google Scholar
Swofford, D.L. 2000. PAUP*. Phylogenetic Analysis Using Parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland, MA.Search in Google Scholar
Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731–2739.10.1093/molbev/msr121Search in Google Scholar PubMed PubMed Central
Thompson, J.D., T.J. Gibson, F. Plewniak, F. Jeanmougin and D.G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876–4882.10.1093/nar/25.24.4876Search in Google Scholar PubMed PubMed Central
Thong, V.D., S.J. Puechmaille, A. Denzinger, C. Dietz, G. Csorba, P.J.J. Bates, E.C. Teeling and H.U. Schnitzler. 2012. A new species of Hipposideros (Chiroptera: Hipposideridae) from Vietnam. J. Mammal. 93: 1–11.10.1644/11-MAMM-A-073.1Search in Google Scholar
Wang, Y.X. 2003. A complete checklist of mammal species and subspecies in China: a taxonomic and geographic reference. China Forestry Publishing House, Beijing, China. pp. 394. (in Chinese).Search in Google Scholar
Wang, Z.Z. 2009. The mo1ecu1ar phy1ogenetics of lutjanid fishes of the genus Lutjanus from China. Hunan Normal University, Hunan, China. pp. 103. (in Chinese).Search in Google Scholar
Wang, G., J.L. Wan and E.Q. Wang. 2006. Extensional collapse of the southern part of the Gaoligong Range in the Western Yunnan, China and its tectonic origin. Acta Geol. Sin. 80: 1262–1273. (in Chinese).Search in Google Scholar
Worthington, W.J. and E. Barratt. 1996. A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Res. News 37: 1–3.Search in Google Scholar
Wu, Y., W.R. Hou, J.C. Hu, Y. Cheng and J. Li. 2000. Comparative study on some age characteristic of Hipposideros armiger in Sichuan area. Acta Theriol. Sin. 20: 284–288. (in Chinese).Search in Google Scholar
Xu, L.J., C.F. He, C. Shen, T.L. Jiang, L.M. Shi, K.P. Sun, S.W. Berquist and J. Feng. 2010. Phylogeography and population genetic structure of the great leaf-nosed bat (Hipposideros armiger) in China. J. Hered. 101: 562–572.10.1093/jhered/esq039Search in Google Scholar PubMed
Yang, Q.S., L. Xia, Z.J. Feng, Y. Ma, G.Q. Quan and Y. Wu. 2007. A guide to the measurement of mammal skull, V: Insectivora and Chiroptera. Chin. J. Zool. 42: 56–62. (in Chinese).Search in Google Scholar
Yoshiyuki, M. 1991. Taxonomic status of Hipposideros terasensis Kishida, 1924 from Taiwan (Chiroptera, Hipposideridae). J. Mammal Soc. Japan 16: 27–35.Search in Google Scholar
Zhang, R.Z., S.K. Jin, G.Q. Quan, S.H. Li, Z.Y. Ye, F.G. Wang and M.L. Zhang. 1997. Distribution of mammalian species in China. China Forestry Publishing House, Beijing, China. pp. 281. (in Chinese).Search in Google Scholar
Zhao, H.T., L.R. Wang and J.Y. Yuan. 2007. Origin and time of Qiongzhou Strait. Mar. Geol. Quat. Geol. 27: 33–40. (in Chinese).Search in Google Scholar
Zhen, X.Y. 1987. A survey of the bats (Chiroptera) of Fujian Province. Wuyi Sci. J. 7: 237–242. (in Chinese).Search in Google Scholar
Zhu, Q.W. 2006. Genetic variation of two hipposiderid bats (Hipposideros terasensis and Coelops frithi formosanus) in Taiwan. Tunghai University, Taichung, Taiwan. pp. 59. (in Chinese).Search in Google Scholar
©2017 Walter de Gruyter GmbH, Berlin/Boston
