Skip to main content
SpringerLink
Log in

Ventral coloration differentiation and mitochondrial sequences of the Chinese Cobra (Naja atra) in Taiwan

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Differences in coloration between eastern and western populations of the Chinese cobra (Naja atra) in Taiwan have been noted by snake collectors, snake keepers, and users of Chinese traditional medicine, but have never been verified by scientific research. In this study, we quantified the amount of black pigment on ventral scales, and found prominent differences in ventral coloration of populations across Taiwan; populations in eastern Taiwan have black ventral scales while populations in the west are predominantly white. Previous studies have shown a similar east-west population differentiation in regards to venom components. We supplement these data with mitochondrial control region sequences, which show extremely low nucleotide diversity. Black-ventral and white-ventral snakes share major haplotypes and show no genetic differentiation. Nevertheless, moderate Fst and low Nm values between populations indicate low levels of gene flow. With a morphological fixation earlier than mitochondrial sequences on a relatively short evolutionary time scale, ventral coloration is potentially a result of local adaptation. Based upon the results of this study, along with traditional observations, we strongly recommend treating each of the four populations of the Chinese cobra in Taiwan as distinct ESUs. Reintroducing confiscated snakes from the illegal trade back into the wild needs to be halted to prevent artifical gene flow.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, London

    Google Scholar 

  • Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates, Inc., Sunderland, MA

    Google Scholar 

  • Bittner TD, King RB, Kerfin JM (2002) Effects of body size and melanism on the thermal biology of garter snakes (Thamnophis sirtalis). Copeia 2002:477–482

    Article  Google Scholar 

  • Camin JH, Ehrlich PR (1958) Natural selection in water snakes (Natrix sipedon L.) on islands in Lake Erie. Evolution 12:504–511

    Article  Google Scholar 

  • Chen I-S, Fang L-S (1999) The freshwater and estuarine fishes of Taiwan. National Museum of Marine Biology and Aquarium, Taiwan

    Google Scholar 

  • Chen T-S, Chung F-Y, Tjong S-C, Goh K-S, Huang W-N, Chien K-Y, Wu P-L, Lin H-C, Chen C-J, Wu W-G (2005) Structural difference between Group I and Group II cobra cardiotoxins: X-ray, NMR, and CD analysis of the effect of cis-proline conformation on three-fingered toxins. Biochemistry 44:7414–7426

    Article  PubMed  CAS  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary process in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  Google Scholar 

  • Creer S, Malhotra A, Thorpe RS, Chou W-H (2001) Multiple causation of phylogeographical pattern as revealed by nested clade analysis of the bamboo viper (Trimeresurus stejnegeri) within Taiwan. Mol Ecol 10:1967–1981

    Article  PubMed  CAS  Google Scholar 

  • Dodd CK (1987) Status, conservation and management. In: Seigel RA, Collins JT, Novak SS (eds) Snakes: ecology and evolutionary biology. McGraw-Hill, New York

    Google Scholar 

  • Ehrlich PR, Camin JH (1960) Natural selection in Middle Island water snakes (Natrix sipedon L.). Evolution 14:136

    Article  Google Scholar 

  • Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136:343–359

    PubMed  CAS  Google Scholar 

  • Fang Y-P, Lee L-L (2002) Re-evaluation of the Taiwanese white-toothed shrew, Crocidura tadae Tokuda and Kano, 1936 (Insectivora, Soricidae) from Taiwan and two offshore islands. J Zool 257:145–154

    Article  Google Scholar 

  • Gemmell NJ, Akiyama S (1996) An efficient method for the extraction of DNA from vertebrate tissues. Trend Genet 12:338–339

    Article  CAS  Google Scholar 

  • Gibson AR, Falls JB (1979) Thermal biology of the common garter snake Thamnophis sirtalis (L.) II. The effects melanism Oecol 43:99–109

    Google Scholar 

  • Grant WAS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

  • Guo Q-H (2002) Population genetic structure of Sphenomorphus taiwanensis. Master dissertation, National Taiwan Normal University, Taipei

  • Hachisuka M, Udagawa T (1950) Contributions to the ornithology of Formosa, Part 1. Q J Taiwan Museum 3:187–280

    Google Scholar 

  • Harrison SP, Yu G, Takahara H, Prentice IC (2001) Palaeovegetation (Communications arising): diversity of temperate plants in east Asia. Nature 413:129–130

    Article  PubMed  CAS  Google Scholar 

  • Hope G, Kershaw AP, Kaars S, Sun X, Liew P-M, Heusser LE, Takahara H, McGlone M, Miyoshi N, Moss PT (2004) History of vegetation and habitat change in the Austral-Asian region. Quaternary Int 118–119:103–126

    Article  Google Scholar 

  • Huelsenbeck JP, Crandall KA (1997) Phylogeny estimation and hypothesis testing using maximum likelihood. Annu Rev Ecol Syst 28:437–466

    Article  Google Scholar 

  • Hung DZ (2004) Taiwan’s venomous snakebite: epidemiological, evolution and geographic differences. Trans R Soc Trop Med Hyg 98:96–101

    Article  PubMed  Google Scholar 

  • IUCN (2002) Guidelines for the placement of confiscated animals. Prepared by the IUCN/SSC Re-introduction Specialist Group. IUCN, Gland, Switzerland and ERWDA, Abu Dhabi, UAE. 24pp

  • King RB (1988) Polymorphic populations of the garter snake Thamnophis sirtalis near Lake Erie. Herpetologica 44:451–458

    Google Scholar 

  • King RB (1992) Morph and age specific crypsis in Lake Eris water snakes. Evolutionary Ecology 6:115–124

    Article  Google Scholar 

  • King RB (1993) Color-pattern variation in Lake Erie water snakes: prediction and measurement of natural selection. Evolution 47:1819–1833

    Article  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinformatics 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Kuntz CRE (1963) Snakes of Taiwan. Q J Taiwan Museum 16:1–80

    Google Scholar 

  • Liau M-Y (1991) Studies on the toxoids and antivenins of Formosan venomous snakes. Dissertation, National Taiwan University, Taipei

  • Liau M-Y, Huang R-J (1997) Toxoids and antivenoms of venomous snakes in Taiwan. J Toxicol Toxin Rev 16:163–175

    CAS  Google Scholar 

  • Liew PM, Chung NJ (2001) Vertical migration of forests during the last glacial period in subtropical Taiwan. West Pacific Ear Sci 1:405–414

    Google Scholar 

  • Lin HC (1997) The commercial use and harvesting survey of snakes in Taiwan. Taipei Zoo Bulletin 9:53–65

    Google Scholar 

  • Lin S-M (2003) Phylogeny and phylogeographic studies of Takydromus in Taiwan and adjacent regions (Squamata: Lacertidae). Ph. D. dissertation, Department of Biology, National Taiwan Normal University, Taipei

  • Lin S-M, Chen CA, Lue K-Y (2002) Molecular phylogeny and biogeography of the grass lizards genus Takydromus (Reptilia: Lacertidae) of East Asia. Mol Phylogenet Evol 22:276–288

    Article  PubMed  CAS  Google Scholar 

  • Lin S-M, Chang W-S, Chen S-L, Shang G, Lue K-Y (2003) Taxonomic status of the Legless Lizard Ophisaurus (Squamata: Anguidae) in Taiwan: molecular data, morphology and literature review. Zool Stud 42:411–419

    CAS  Google Scholar 

  • Lue K-Y, Lai J-S (1991) Wildlife data bank of Taiwan (3) Lizards (I). Council of Agriculture, Taiwan, Taipei, Taiwan

    Google Scholar 

  • Lue K-Y, Tu M-C, Shang G (1999) A field guide to the amphibians and reptiles of Taiwan. SWAN Pub. Co., Taipei, Taiwan

    Google Scholar 

  • Majerus MEN (1998) Melanism: evolution in action. Oxford University Press, Oxford, U.K

    Google Scholar 

  • Moritz C (1994a) Applications of mitochondrial DNA analysis in conservation: a critical review. Mol Ecol 3:401–411

    Article  CAS  Google Scholar 

  • Moritz C (1994b) Defining “evolutionarily significant units” for conservation. Trends Ecol Evol 9:373–375

    Article  Google Scholar 

  • Ota H (2000) The current geographic faunal pattern of reptiles and amphibians of the Ryukyu Archipelago and adjacent regions. Tropics 10:51–62

    Article  Google Scholar 

  • Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45

    Article  PubMed  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Ryder OA (1986) Species conservation and the dilemma of subspecies. Trends Ecol Evol 1:9–10

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. Ver 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva, Geneva, Switzerland

    Google Scholar 

  • Shang G (1997) Phylogenetic relationships and biogeography in the genus Japalura of Taiwan based on the variation of mtDNA sequences. Master dissertation, National Sun Yat-Sen University, Kaohsiung

  • Swofford DL (2002) PAUP 4.0b10: Phylogenetic analysis using parsimony and other methods. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Tsai C-Y (1999) Population phylogeny of Gekko hokouensis based on mitochondrial 12S rRNA and cytochrome b sequences. Master dissertation, National Sun Yat-Sen University, Kaohsiung

  • Tzeng C-S (1986) The freshwater fishes of Taiwan. Department of Education, Taiwan Province, R.O.C., Keelung, Taiwan

    Google Scholar 

  • Waples RS (1991) Pacific salmon, Oncorhynchus spp., and the definition of “species” under the endangered species act. Mar Fish Rev 53:11–22

    Google Scholar 

  • Warrell DA (1995) Clinical toxicology of snakebite in Asia. In: Meier J, White J (eds) Handbook of clinical toxicology of animal venoms and poisons. CRC Press, Boca Raton

    Google Scholar 

  • Whitaker R (1997) Utilization of lizards and snakes. In: Roth HR, Merz G (eds) Wildlife resources: a global account of economic use. Springer-Verlag, New York

    Google Scholar 

  • Wu C-S (2003) Comparison and identification of venomous components between eastern and western Taiwan cobra (Naja atra) by two dimensional high performance liquid chromatography (2D-HPLC) and electrospray ionization mass spectrometry (EMI-MS). Dissertation, National Tsing Hua University, Hsinchu

  • Yu G, Liew PM, Xue B, Li Z (2003) Surface pollen and vegetation reconstruction from central and northern mountains of Taiwan. Chin Sci Bull 48:291–295

    Article  Google Scholar 

  • Zhao E, Huang M-H, Zong Y (1998) Fauna Sinica, Reptilia Vol. 3: Squamata, Serpentes. Science Press, Beijing

    Google Scholar 

Download references

Acknowledgements

We thank Miss Po-Juan Hsieh and Miss Hsin-Yi Hong for their assistance in data analyses and systematically organizing the progress of this research. We thank Mr. Ching-Feng Lin for his skilled work in keeping and measuring the snakes. We are also thankful for Miss Mei-Ju Lin and Hsin-Yi Hong for their great help in laboratory works. This study was based on the funding (93AS-4.1.1-FB-e2) given to Hua-Ching Lin from the Council of Agriculture, Taiwan.

Author information

Authors and Affiliations

  1. Department of Life Science, National Taiwan Normal University, 88 Tingzhou Road, Sec. 4, Taipei, 116, Taiwan, ROC

    Hua-Ching Lin & Shou-Hsien Li

  2. Taipei Zoo, 30 Xinguang Road, Sec. 2, Taipei, 116, Taiwan, ROC

    Hua-Ching Lin

  3. Musem of Vertebrate Zoology, University of California Berkeley, Berkeley, CA, 94720, USA

    Jonathan Fong

  4. Department of Life Science, Chinese Culture University, 55 Huagang Road, Taipei, 111, Taiwan, ROC

    Si-Min Lin

Authors
  1. Hua-Ching Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shou-Hsien Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jonathan Fong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Si-Min Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Si-Min Lin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lin, HC., Li, SH., Fong, J. et al. Ventral coloration differentiation and mitochondrial sequences of the Chinese Cobra (Naja atra) in Taiwan. Conserv Genet 9, 1089–1097 (2008). https://doi.org/10.1007/s10592-007-9418-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-007-9418-8

Keywords

Search

Navigation