Abstract
Numerous termite species have been introduced outside their native ranges by human transport, and some have become invasive. The dampwood termite Zootermopsis nevadensis (Hagen), which is native to western North America, has been introduced to and become established in Kawanishi City, Hyogo Prefecture, Japan. Zootermopsis nevadensis is subdivided into two subspecies based on cuticular hydrocarbon (CHC) phenotypes: Z. nevadensis nevadensis and Z. nevadensis nuttingi (Haverty and Thorne). Here, we identified Z. nevadensis in Japan as hybrids between the two subspecies. Chemical analysis showed the presence of 7,15-dimethylhenicosane and 5,17-dimethylhenicosane in the CHCs of Z. nevadensis in Japan, corresponding to the CHC phenotype of Z. n. nevadensis. Conversely, all mitochondrial cytochrome c oxidase subunit I sequences of Z. nevadensis in Japan were identical to sequences from Z. n. nuttingi and hybrids between the two subspecies from a native hybrid zone in California, USA. In addition, phylogenetic analysis showed that Z. nevadensis in Japan formed a clade with Z. n. nuttingi and hybrids between the two subspecies. Our results show discordance between the chemical and genetic features of Z. nevadensis in Japan, indicating that individuals of Z. nevadensis in Japan are hybrids between the two subspecies.
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References
Abe T (1987) Evolution of life types in termites. In: Kawano S, Connell JH, Hidaka T (eds) Evolution and coadaptation in biotic communities. University of Tokyo Press, Tokyo, pp 125–148
Aldrich BT, Kambhampati S (2007) Population structure and colony composition of two Zootermopsis nevadensis subspecies. Heredity 99:443–451. https://doi.org/10.1038/sj.hdy.6801022
Aldrich BT, Kambhampati S (2009) Preliminary analysis of a hybrid zone between two subspecies of Zootermopsis nevadensis. Insectes Soc 56:439–450. https://doi.org/10.1007/s00040-009-0041-1
Anderson E (1949) Introgressive hybridization. Wiley, New York
Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, Oxford
Bignell DE, Eggleton P (2000) Termites in ecosystems. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic, Dordrecht, pp 363–387
Booth W, Brent CS, Calleri DV, Rosengaus RB, Traniello JFA, Vargo EL (2012) Population genetic structure and colony breeding system in dampwood termites (Zootermopsis angusticollis and Z. nevadensis nuttingi). Insectes Soc 59:127–137. https://doi.org/10.1007/s00040-011-0198-2
Eggleton P (2000) Global patterns of termite diversity. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic, Dordrecht, pp 25–51
Evans TA (2010) Invasive termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 519–562
Evans TA, Forschler BT, Grace JK (2013) Biology of invasive termites: a worldwide review. Annu Rev Entomol 58:455–474. https://doi.org/10.1146/annurev-ento-120811-153554
Glastad KM, Gokhale K, Liebig J, Goodisman MAD (2016) The caste-and sex-specific DNA methylome of the termite Zootermopsis nevadensis. Sci Rep 6:37110. https://doi.org/10.1038/srep37110
Grace JK, Woodrow RJ, Yates JR (2002) Distribution and management of termites in Hawaii. Sociobiology 40:87–94
Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PDN (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proc Natl Acad Sci USA 103:968–971. https://doi.org/10.1073/pnas.0510466103
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Haverty MI, Thorne BL (1989) Agonistic behavior correlated with hydrocarbon phenotypes in dampwood termites, Zootermopsis (Isoptera: Termopsidae). J Insect Behav 2:523–543. https://doi.org/10.1007/BF01053352
Haverty MI, Page M, Nelson LJ, Blomquist GJ (1988) Cuticular hydrocarbons of dampwood termites, Zootermopsis: intra-and intercolony variation and potential as taxonomic characters. J Chem Ecol 14:1035–1058. https://doi.org/10.1007/BF01018791
Haverty MI, Woodrow RJ, Nelson LJ, Grace JK (2000) Cuticular hydrocarbons of termites of the Hawaiian Islands. J Chem Ecol 26:1167–1191. https://doi.org/10.1023/A:1005479826651
Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817. https://doi.org/10.1073/pnas.0406166101
Holt JA, Lepage M (2000) Termites and soil properties. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic, Dordrecht, pp 389–407
Johns PM, Howard KJ, Breisch NL, Rivera A, Thorne BL (2009) Nonrelatives inherit colony resources in a primitive termite. Proc Natl Acad Sci USA 106:17452–17456. https://doi.org/10.1073/pnas.0907961106
Krishna K, Grimaldi DA, Krishna V, Engel MS (2013) Treatise on the Isoptera of the world: 2. Basal families. Bull Am Mus Nat Hist 377:204–621. https://doi.org/10.1206/377.2
Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391. https://doi.org/10.1016/S0169-5347(02)02554-5
Masuoka Y, Maekawa K (2016) Ecdysone signaling regulates soldier-specific cuticular pigmentation in the termite Zootermopsis nevadensis. FEBS Lett 590:1694–1703. https://doi.org/10.1002/1873-3468.12219
Miura T, Koshikawa S, Matsumoto T (2003) Winged presoldiers induced by a juvenile hormone analog in Zootermopsis nevadensis: implications for plasticity and evolution of caste differentiation in termites. J Morphol 257:22–32. https://doi.org/10.1002/jmor.10100
Morimoto K (2000) On the damp-wood termite genus Zootermopsis introduced to Japan. Siroari 122:3–8 (in Japanese)
Noble JC, Müller WJ, Whitford WG, Pfitzner GH (2009) The significance of termites as decomposers in contrasting grassland communities of semi-arid eastern Australia. J Arid Environ 73:113–119. https://doi.org/10.1016/j.jaridenv.2008.08.004
Shellman-Reeve JS (1990) Dynamics of biparental care in the dampwood termite, Zootermopsis nevadensis (Hagen): response to nitrogen availability. Behav Ecol Sociobiol 26:389–397. https://doi.org/10.1007/BF00170895
Suzuki H (2000) Notes on the American common damp-wood termite, Zootermopsis angusticollis (Hagen) found in Kawanishi City, Hyogo Prefecture. House Househ Ins Pest 21:137–144 (in Japanese)
Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods) v4.0b10. Sinauer, Sunderland
Terrapon N, Li C, Robertson HM et al (2014) Molecular traces of alternative social organization in a termite genome. Nat Commun 5:3636. https://doi.org/10.1038/ncomms4636
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Thorne BL, Haverty MI (1989) Accurate identification of Zootermopsis species (Isoptera: Termopsidae) based on a mandibular character of nonsoldier castes. Ann Entomol Soc Am 82:262–266. https://doi.org/10.1093/aesa/82.3.262
Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513
Wilson EO (1990) Success and dominance in ecosystems: the case of the social insects. Ecology Institute, Oldendorf
Yashiro T, Matsuura K, Tanaka C (2011) Genetic diversity of termite-egg mimicking fungi “termite balls” within the nests of termites. Insectes Soc 58:57–64. https://doi.org/10.1007/s00040-010-0116-z
Acknowledgements
We thank Naoto Yoshioka for termite collection; Naoki Mori for providing GC–MS facilities; Nathan Lo for helpful discussion. This work was partly supported by Japanese Society for the Promotion of Science (JSPS) Kiban Kenkyu S Grant No. 25221206 (to K.M.), and a JSPS Postdoctoral Fellowship for Research Abroad No. 558 (to T.Y).
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Yashiro, T., Mitaka, Y., Nozaki, T. et al. Chemical and molecular identification of the invasive termite Zootermopsis nevadensis (Isoptera: Archotermopsidae) in Japan. Appl Entomol Zool 53, 215–221 (2018). https://doi.org/10.1007/s13355-018-0545-0
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DOI: https://doi.org/10.1007/s13355-018-0545-0