Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-23T04:27:27.388Z Has data issue: false hasContentIssue false

Multiple origins of outbreak populations of a native insect pest in an agro-ecosystem

Published online by Cambridge University Press:  21 December 2010

T. Kobayashi*
Affiliation:
National Agricultural Research Center for Tohoku Region, Yotsuya, Daisen, Akita 014-0102, Japan
T. Sakurai
Affiliation:
National Agricultural Research Center for Tohoku Region, Shimo-kuriyagawa, Morioka, Iwate 020-0198, Japan
M. Sakakibara
Affiliation:
National Agricultural Research Center for Tohoku Region, Shimo-kuriyagawa, Morioka, Iwate 020-0198, Japan
T. Watanabe
Affiliation:
National Agricultural Research Center, Kan-nondai, Tsukuba, Ibaraki, 305-8666, Japan
*
*Author for correspondence Fax: +81 29 838 6109 E-mail: [email protected]

Abstract

Native insects can become epidemic pests in agro-ecosystems. A population genetics approach was applied to analyze the emergence and spread of outbreak populations of native insect species. Outbreaks of the mirid bug, Stenotus rubrovittatus, have rapidly expanded over Japan within the last two decades. To characterize the outbreak dynamics of this species, the genetic structure of local populations was assessed using polymorphisms of the mtDNA COI gene and six microsatellite loci. Results of the population genetic analysis suggested that S. rubrovittatus populations throughout Japan were genetically isolated by geographic distance and separated into three genetic clusters occupying spatially segregated regions. Phylogeographic analysis indicated that the genetic structure of S. rubrovittatus reflected post-glacial colonization. Early outbreaks of S. rubrovittatus in the 1980s occurred independently of genetically isolated populations. The genetic structure of the populations did not fit the pattern of an outbreak expansion, and therefore the data did not support the hypothesis that extensive outbreaks were caused by the dispersal of specific pestiferous populations. Rather, the historical genetic structure prior to the outbreaks was maintained throughout the increase in abundance of the mirid bug. Our study indicated that changes in the agro-environment induced multiple outbreaks of native pest populations. This implies that, given suitable environmental conditions, local populations may have the potential to outbreak even without invasion of populations from other environmentally degraded areas.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anstead, J.A., Burd, J.D. & Shufran, K.A. (2002) Mitochondrial DNA sequence divergence among Schizaphis graminum (Hemiptera: Aphididae) clones from cultivated and non-cultivated hosts: haplotype and host associations. Bulletin Entomological Research 92, 1724.CrossRefGoogle ScholarPubMed
Aoki, K., Kato, M. & Murakami, N. (2008) Glacial bottleneck and postglacial recolonization of a seed parasitic weevil, Curculio hilgendorfi, inferred from mitochondrial DNA variation. Molecular Ecology 17, 32763289.CrossRefGoogle ScholarPubMed
Avise, J.C. (2000) Phylogeography: The History and Formation of Species. Cambridge, MA, USA, Harvard University Press.CrossRefGoogle Scholar
Berryman, A.A. (1987) The theory and classification of outbreaks?. pp. 330 in Barbosa, P. & Schults, J.C. (Eds) Insect Outbreaks. San Diego, CA, USA, Academic Press.CrossRefGoogle Scholar
Brower, A.V. (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Sciences of the USA 91, 64916495.CrossRefGoogle ScholarPubMed
Cavalli-Sforza, L.L. & Edwards, A.W.F. (1967) Phylogenetic analyses: models and estimation procedures. Evolution 32, 550570.CrossRefGoogle Scholar
Charles, M. & Schneider, J.C. (1987) Genetic change and insect outbreaks. pp. 505527 in Barbosa, P. & Schults, J.C. (Eds) Insect Outbreaks. San Diego, CA, USA, Academic Press.Google Scholar
Chapuis, M.P. & Estoup, A. (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621631.CrossRefGoogle ScholarPubMed
Chapuis, M.P., Lecoq, M., Michalakis, Y., Loiseau, A., Sword, G.A., Piry, S. & Estoup, A. (2008) Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles. Molecular Ecology 17, 36403653.CrossRefGoogle ScholarPubMed
Chapuis, M.P., Loiseau, A., Michalakis, Y., Lecoq, M., Franc, A. & Estoup, A. (2009) Outbreaks, gene flow and effective population size in the migratory locust, Locusta migratoria: a regional-scale comparative survey. Molecular Ecology 18, 792800.CrossRefGoogle ScholarPubMed
Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571659.CrossRefGoogle ScholarPubMed
Corander, J. & Marttinen, P. (2006) Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology 15, 28332843.CrossRefGoogle ScholarPubMed
Cornuet, J.M. & Luikart, G. (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 20012014.CrossRefGoogle ScholarPubMed
Dakin, E.E. & Avise, J.C. (2004) Microsatellite null alleles in parentage analysis. Heredity 93, 504509.CrossRefGoogle ScholarPubMed
Davies, N., Villablanca, F.X. & Roderick, G.K. (1999) Bioinvasions of the medfly Ceratitis capitata: source estimation using DNA sequences at multiple intron loci. Genetics 153, 351360.CrossRefGoogle ScholarPubMed
de la Poza, M., Farinós, G.P., Beroiz, B., Ortego, F., Hernández-Crespo, P. & Castañera, P. (2008) Genetic structure of Sesamia nonagrioides (Lefebvre) populations in the Mediterranean area. Environmental Entomology 37, 13541360.CrossRefGoogle ScholarPubMed
Dieringer, D. & Schlötterer, C. (2003) Microsatellite analyser (MSA), a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes 3, 167169.CrossRefGoogle Scholar
Endersby, N.M., McKechnie, S.W., Ridland, P.M. & Weeks, A.R. (2006) Microsatellites reveal a lack of structure in Australian populations of the diamondback moth, Plutella xylostella (L.). Molecular Ecology 15, 107118.CrossRefGoogle ScholarPubMed
Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479491.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. & Schneider, S. (2007) Arlequin (Version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 4750.Google ScholarPubMed
Felsenstein, J. (1993) PHYLIP: Phylogeny Inference Package, version 3.5c. Seattle, WA, USA, Department of Genetics, University of Washington.Google Scholar
Fu, Y.-X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915925.CrossRefGoogle ScholarPubMed
Goudet, J. (1995) FSTAT (Version 1.2): A computer program to calculate F-Statistics. Journal of Heredity 86, 485486.CrossRefGoogle Scholar
Goto, J., Ito, Y. & Shishido, M. (2000) Relationship between barn grass in rice paddies and spotted rice caused by Stenotus rubrovittatus (Matsumura) Annual Report of the Society of Plant Protection of North Japan 51, 162164.Google Scholar
Guillot, G., Estoup, A., Mortier, F. & Cosson, J.F. (2005) A spatial statistical model for landscape genetics. Genetics 170, 12611280.CrossRefGoogle ScholarPubMed
Hayashi, H. (1986) Ecology and control of the Sorghum plant bug (Stenotus rubrovittatus MATSUMURA) causeing the pecky rice. Plant Protection 40, 321326.Google Scholar
Hewitt, G.M. (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society, Series B: Biological Sciences 359, 183195.CrossRefGoogle ScholarPubMed
Hutchinson, D.W. & Templeton, A.R. (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53, 18981914.CrossRefGoogle Scholar
Johnstone, R.A. & Hurst, G.D.D. (1996) Maternally inherited male-killing microorganisms may confound interpretation of mitochondrial DNA variability. Biological Journal of the Linnean Society 58, 453470.CrossRefGoogle Scholar
Kakizaki, M. (2004) Investigation on the occurrences of the Sorghum plant bug, Stenotus rubrovittatus (Matsumura), in the gramineous forage grass fields of southern Hokkaido in 2003. Annual Report of the Society of Plant Protection of North Japan 51, 162164.Google Scholar
Kalinowski, S.T. (2004) Counting alleles with rarefaction: Private alleles and hierarchical sampling designs. Conservation Genetics 5, 539543.CrossRefGoogle Scholar
Kalinowski, S.T. (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes 5, 187189.CrossRefGoogle Scholar
Katase, M., Shimizu, K., Shiina, S., Hagiwara, K. & Iwai, H. (2007) Seasonal occurrence of rice bugs in the northern part of Chiba prefecture. Annual Report of Kanto-Tosan Plant Protection 54, 99104.Google Scholar
Kawai, M., Shoda-Kagaya, E., Maehara, T., Zhou, Z., Lian, C., Iwata, R., Yamane, A. & Hogetsu, T. (2006) Genetic structure of pine sawyer Monochamus alternatus (Coleoptera: Cerambycidae) populations in Northeast Asia: consequences of the spread of pine wilt disease. Environmental Entomology 35, 569579.CrossRefGoogle Scholar
Kim, K.S., Cano-Ríos, P. & Sappington, T.W. (2006) Using genetic markers and population assignment techniques to infer origin of boll weevils (Coleoptera: Curculionidae) unexpectedly captured near an eradication zone in Mexico. Environmental Entomology 35, 813826.CrossRefGoogle Scholar
Kiritani, K. (2006) Predicting impacts of global warming on population dynamics and distribution of arthropods in Japan. Population Ecology 48, 512.CrossRefGoogle Scholar
Kobayashi, T. (2008) Development of polymorphic microsatellite markers for the sorghum plant bug, Stenotus rubrovittatus (Heteroptera: Miridae). Molecular Ecology Resources 8, 690691.CrossRefGoogle ScholarPubMed
Kolar, C.S. & Lodge, D.M. (2001) Progress in invasion biology: predicting invaders. Trends in Ecology and Evolution 16, 199204.CrossRefGoogle ScholarPubMed
Mantel, N. (1967) The detection of disease clustering and generalized regression approach. Cancer Research 27, 209220.Google ScholarPubMed
Meng, X.F., Shi, M. & Chen, X.X. (2008) Population genetic structure of Chilo suppressalis (Walker) (Lepidoptera: Crambidae): strong subdivision in China inferred from microsatellite markers and mtDNA gene sequences. Molecular Ecology 17, 28802897.CrossRefGoogle Scholar
Mopper, S. (1996) Adaptive genetic structure in phytophagous insect populations. Tree 11, 235237.Google ScholarPubMed
Morimoto, N. & Kiritani, K. (1995) Fauna of exotic insects in Japan. Bulletin of National Institute of Agro-Environmental Sciences 12, 87120.Google Scholar
Mun, J., Bohonak, A.J. & Roderick, G.K. (2003) Population structure of the pumpkin fruit fly Bactrocera depressa (Tephritidae) in Korea and Japan: Pliocene allopatry or recent invasion? Molecular Ecology 12, 29412951.CrossRefGoogle ScholarPubMed
Nei, M. & Tajima, F. (1983) Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105, 207217.CrossRefGoogle ScholarPubMed
Novak, S.J. (2007) The role of evolution in the invasion process. Proceedings of the National Academy of Sciences of the USA 104, 36713672.CrossRefGoogle ScholarPubMed
Page, R.D. (1996) TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357358.Google ScholarPubMed
Porretta, D., Canestrelli, D., Bellini, R., Celli, G. & Urbanelli, S. (2007) Improving insect pest management through population genetic data : a case study of the mosquito Ochlerotatus caspius (Pallas). Journal of Applied Ecology 44, 682691.CrossRefGoogle Scholar
R Development Core Team (2005) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Raymond, M. & Rousset, F. (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248249.CrossRefGoogle Scholar
Shufran, K.A., Burd, J.D., Anstead, J.A. & Lushai, G. (2000) Mitochondrial DNA sequence divergence among greenbug (Homoptera: aphididae) biotypes: evidence for host-adapted races. Insect Molecular Biology 9, 179184.CrossRefGoogle ScholarPubMed
Slatkin, M. (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457462.CrossRefGoogle ScholarPubMed
Sota, T., Hayashi, M. & Iwai, D. (2004) Phylogeography of the leaf beetle Chrysolina virgata in wetlands of Japan inferred from the distribution of mitochondrial haplotypes. Entomological Science 7, 381388.CrossRefGoogle Scholar
Tada, R. (1998) Japanese Archipelago of last glacial period. Iden 52, 1015.Google Scholar
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595.CrossRefGoogle ScholarPubMed
Takahashi, F., Nagano, T. & Sato, T. (1985) Occurrence of spotted rice by Sorghum plant bug, Stenotus rubrovittatus MATSUMURA, in the north of Miyagi prefecture. Annual Report of Plant Protection of North Japan 36, 3840.Google Scholar
Tanaka, H., Chiba, T., Fujioka, S., Chiba, T., Ito, M. & Nakaminami, H. (1988) Occurrence of the rice bugs and spotted rice in Iwate prefecture. Annual Report of the Society of Plant Protection of North Japan 39, 162166.Google Scholar
van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535538.CrossRefGoogle Scholar
Wallner, W.E. (1987) Factors affecting insect population dynamics: differences between outbreak and non-outbreak species. Annual Review of Entomology 32, 317340.CrossRefGoogle Scholar
Watanabe, T. & Higuchi, H. (2006) Recent occurrence and problem of rice bugs. Plant Protection 60, 201203.Google Scholar
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 13581370.Google ScholarPubMed
Yasunaga, T., Takai, M., Kawasawa, T. & Nakatani, Y. (2001) A Field Guide to Japanese Bugs II. Tokyo, Zenkoku Noson Kyouiku Kyoukai.Google Scholar
Yu, H., Frommer, M., Robson, M.K., Meats, A.W., Shearman, D.C. & Sved, J.A. (2001) Microsatellite analysis of the Queensland fruit fly Bactrocera tryoni (Diptera: Tephritidae) indicates spatial structuring: implications for population control. Bulletin of Entomological Research 91, 139147.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Kobayashi Supplementary Material

Fig1.pdf

Download Kobayashi Supplementary Material(PDF)
PDF 393 KB
Supplementary material: PDF

Kobayashi Supplementary Material

Fig2.pdf

Download Kobayashi Supplementary Material(PDF)
PDF 146.2 KB
Supplementary material: PDF

Kobayashi Supplementary Material

Table1.pdf

Download Kobayashi Supplementary Material(PDF)
PDF 97.4 KB
Supplementary material: PDF

Kobayashi Supplementary Material

Table2.pdf

Download Kobayashi Supplementary Material(PDF)
PDF 30.9 KB
Supplementary material: PDF

Kobayashi Supplementary Material

Table3.pdf

Download Kobayashi Supplementary Material(PDF)
PDF 18.8 KB