Biological Invasions

, Volume 13, Issue 9, pp 1951–1967 | Cite as

The bioinvasion of Guam: inferring geographic origin, pace, pattern and process of an invasive lizard (Carlia) in the Pacific using multi-locus genomic data

  • Christopher C. Austin
  • Eric N. Rittmeyer
  • Lauren A. Oliver
  • John O. Andermann
  • George R. Zug
  • Gordon H. Rodda
  • Nathan D. Jackson
Original Paper


Invasive species often have dramatic negative effects that lead to the deterioration and loss of biodiversity frequently coupled with the burden of expensive biocontrol programs and subversion of socioeconomic stability. The fauna and flora of oceanic islands are particularly susceptible to invasive species and the increase of global movements of humans and their products since WW II has caused numerous anthropogenic translocations and increased the ills of human-mediated invasions. We use a multi-locus genomic dataset to identify geographic origin, pace, pattern and historical process of an invasive scincid lizard (Carlia) that has been inadvertently introduced to Guam, the Northern Marianas, and Palau. This lizard is of major importance as its introduction is thought to have assisted in the establishment of the invasive brown treesnake (Boiga irregularis) on Guam by providing a food resource. Our findings demonstrate multiple waves of introductions that appear to be concordant with movements of Allied and Imperial Japanese forces in the Pacific during World War II.


Boiga Brown Treesnake Marianas Micronesia New Guinea Palau World War II 



We thank the people from the many different village communities where we were given the privilege to conduct fieldwork on their land. We thank B. Roy, V. Kula, and B. Wilmot from the PNG Department of Environment and Conservation, J. Robins from the PNG National Research Institute. Jim Animiato, Ilaiah Bigilale, and Bulisa Iova from the PNG National Museum provided research assistance in Papua New Guinea. Robert Reed kindly provided samples from the Marianas and Ben Evans and Iqbal Setiadi kindly provided samples from Halmahera. Ken Tighe provided information on dates of first collections and discussions with Ron Crombie provided valuable information. This manuscript was improved from comments from the Austin lab group and Leslie Austin. Fieldwork by GZ in PNG was supported by the Smithsonian Research Awards Program and subsequent museum studies of Carlia by the Smithsonian’s Scholarly Studies Program and Research Opportunities Awards. Research was carried out under LSU IACUC protocol 06-071. This research was funded by National Science Foundation grants DEB 0445213 and DBI 0400797 to CCA.


  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723CrossRefGoogle Scholar
  2. Arèvalo E, Davis SK, Sites JW Jr (1994) Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in Central Mexico. Syst Biol 43:387–418Google Scholar
  3. Austin CC, Rittmeyer EN, Richards SJ, et al (2010a) Phylogeny, historical biogeography and body size evolution in Pacific Island Crocodile skinks Tribolonotus (Squamata; Scincidae). Mol Phylogenet Evol 57:227–236Google Scholar
  4. Austin CC, Spataro M, Peterson S, et al (2010b) Conservation genetics of Boelen’s python (Morelia boeleni) from New Guinea: reduced genetic diversity and divergence of captive and wild animals. Conserv Genet 11:889–896CrossRefGoogle Scholar
  5. Bryant D, Moulton V (2004) Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265PubMedCrossRefGoogle Scholar
  6. Case TJ, Bolger DT (1991) The role of introduced species in shaping the distribution and abundance of island reptiles. Evol Ecol 5:272–290CrossRefGoogle Scholar
  7. Crombie RI, Pregill GK (1999) A checklist of the herpetofauna of the Palau islands (Republic of Belau), Oceania. Herpetol Monogr 13:29–80CrossRefGoogle Scholar
  8. Dolman G, Hugall AF (2008) Combined mitochondrial and nuclear data enhance resolution of a rapid radiation of Australian rainbow skinks (Scincidae: Carlia). Mol Phylogenet Evol 49:782–794PubMedCrossRefGoogle Scholar
  9. Dolman G, Phillips BP (2004) Single copy nuclear DNA markers characterized for comparative phylogeography in Australian wet tropics rainforest skinks. Mol Ecol Notes 4:185–187Google Scholar
  10. Donnellan SC, Couper PJ, Saint KM, et al (2009) Systematics of the Carlia ‘fusca’ complex (Reptilia: Scincidae) from northern Australia. Zootaxa 2227:1–31Google Scholar
  11. Fetzner FWJ (1999) Extracting high-quality DNA from shed reptile skins: a simplified method. BioTechniques 26:1052–1054PubMedGoogle Scholar
  12. Fritts TH, Rodda GH (1998) The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annu Rev Ecol Syst 29:113–140CrossRefGoogle Scholar
  13. Fuerst GS, Austin CC (2004) Population genetic structure of the prairie Skink (Eumeces septentrionalis): nested clade analysis of post Pleistocene populations. J Herpetol 38:257–268CrossRefGoogle Scholar
  14. Gailey HA (2004) MacArthur’s victory: the war in New Guinea, 1943–1944. Presidio Press, New YorkGoogle Scholar
  15. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  16. Huson DH, Bryand D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267PubMedCrossRefGoogle Scholar
  17. Jackson ND, Austin CC (2010) The combined effects of rivers and refugia generate extreme cryptic fragmentation within the common ground skink (Scincella lateralis). Evolution 64:409–428Google Scholar
  18. Joly S, Bruneau A (2006) Incorporating allelic variation for reconstructing the evolutionary history of organisms from multiple genes: an example from Rosa in North America. Syst Biol 55:623–636PubMedCrossRefGoogle Scholar
  19. Kocher TD, Thomas WK, Meyer A, et al (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the United States of America 86:6196–6200Google Scholar
  20. Kraus F (2009) Alien reptiles and amphibians: a scientific compendium and analysis. Springer Science, New YorkGoogle Scholar
  21. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948PubMedCrossRefGoogle Scholar
  22. Maddison WP, Maddison DR (2010) Mesquite: a modular system for evolutionary analysis. Version 2.73
  23. McKeown S (1996) A field guide to reptiles and amphibians of the Hawaiian islands. Diamond Head Publishing, Los OsosGoogle Scholar
  24. Morison SE (1953) History of United States naval operations in world war II volume 8: New Guinea and the Marianas, March 1944–August 1944. University of Illinois Press, UrbanaGoogle Scholar
  25. Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583PubMedCrossRefGoogle Scholar
  26. Ota H (1999) Introduced amphibians and reptiles of the Ryukyu Archipelago, Japan. In: Rodda GH, Sawai Y, Chiszar D, Tanaka H (eds) Problem snake management: the Habu an the brown treesnake. Comstock Publishing Associates, Ithaca, pp 439–452Google Scholar
  27. Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420PubMedCrossRefGoogle Scholar
  28. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256PubMedCrossRefGoogle Scholar
  29. Rambaut A, Drummond AJ (2007) Tracer v1.4. Available from
  30. Rodda GH, Fritts TH, Reichel JD (1991) Distributional patterns of reptiles and amphibians in the Mariana Islands. Micronesica 24:195–210Google Scholar
  31. Rodda GH, Sawai Y, Chiszar D, Tanaka H (1999) Problem snake management: the Habu an the brown treesnake. Comstock Publishing Associates, IthacaGoogle Scholar
  32. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  33. Smith SA, Austin CC, Shine R (2001) A phylogenetic analysis of variation in reproducive mode within an Australian lizard (Saiphos equalis, Scincidae). Biol J Linn Soc 74:131–139CrossRefGoogle Scholar
  34. Stuart-Fox DM, Hugall AF, Moritz C (2002) A molecular phylogeny of rainbow skinks (Scincidae: Carlia): taxonomic and biogeographic implications. Aust J Zool 50:39–51Google Scholar
  35. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and Other Methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  36. Urban MC, Phillips BL, Skelly DK, Shine R (2008) A toad more traveled: the heterogeneous invasion dynamics of cane toads in Australia. Am Nat 171:134–148CrossRefGoogle Scholar
  37. Zug GR (2004) Systematics of the Carlia “fusca” lizards of New Guinea and nearby islands. Bishop Museum Press, HonoluluGoogle Scholar
  38. Zug GR, Allison A (2006) New Carlia fusca complex lizards (Reptilia: Squamata: Scincidae) from New Guinea, Papua-Indonesia. Zootaxa 1237:27–44Google Scholar
  39. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, The University of Texas, Austin. Available from:

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Christopher C. Austin
    • 1
  • Eric N. Rittmeyer
    • 1
  • Lauren A. Oliver
    • 1
  • John O. Andermann
    • 1
  • George R. Zug
    • 2
  • Gordon H. Rodda
    • 3
  • Nathan D. Jackson
    • 1
  1. 1.Department of Biological Sciences, Museum of Natural Science, 119 Foster HallLouisiana State UniversityBaton RougeUSA
  2. 2.Department of Vertebrate ZoologyNational Museum of Natural HistoryWashingtonUSA
  3. 3.USGS Fort Collins Science CenterFort CollinsUSA

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