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Population genetic structure and migration patterns of Liriomyza sativae in China: moderate subdivision and no Bridgehead effect revealed by microsatellites

Published online by Cambridge University Press:  30 November 2015

X.-T. Tang ,
Y. Ji ,
Y.-W. Chang ,
Y. Shen ,
Z.-H. Tian ,
W.-R. Gong  and
Y.-Z. Du
X.-T. Tang
Affiliation:
School of Horticulture and Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou 225009, China
Y. Ji
Affiliation:
School of Horticulture and Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou 225009, China Agricultural Technology Extension Service Center of Dantu District, Zhenjiang 212000, China
Y.-W. Chang
Affiliation:
School of Horticulture and Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou 225009, China
Y. Shen
Affiliation:
Agriculture and Forestry Bureau of Binhu District, Wuxi 214071, China
Z.-H. Tian
Affiliation:
Plant Protection Station of Jiangsu Province, Nanjing 21003, China
W.-R. Gong
Affiliation:
Plant Protection Station of Jiangsu Province, Nanjing 21003, China
Y.-Z. Du*
Affiliation:
School of Horticulture and Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou 225009, China
*
*Author for correspondence Phone: 0086-514-87971854 Fax: 0086-514-87347537 E-mail: yzdu@yzu.edu.cn
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Abstract

While Liriomyza sativae (Diptera: Agromyzidae), an important invasive pest of ornamentals and vegetables has been found in China for the past two decades, few studies have focused on its genetics or route of invasive. In this study, we collected 288 L. sativae individuals across 12 provinces to explore its population genetic structure and migration patterns in China using seven microsatellites. We found relatively low levels of genetic diversity but moderate population genetic structure (0.05 < FST < 0.15) in L. sativae from China. All populations deviated significantly from the Hardy–Weinberg equilibrium due to heterozygote deficiency. Molecular variance analysis revealed that more than 89% of variation was among samples within populations. A UPGMA dendrogram revealed that SH and GXNN populations formed one cluster separate from the other populations, which is in accordance with STRUCTURE and GENELAND analyses. A Mantel test indicated that genetic distance was not correlated to geographic distance (r = −0.0814, P = 0.7610), coupled with high levels of gene flow (M = 40.1–817.7), suggesting a possible anthropogenic influence on the spread of L. sativae in China and on the effect of hosts. The trend of asymmetrical gene flow was from southern to northern populations in general and did not exhibit a Bridgehead effect during the course of invasion, as can be seen by the low genetic diversity of southern populations.

Keywords

Liriomyza sativaemicrosatellitepopulation genetic structuregenetic diversitymigration patterns
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 1 , February 2016 , pp. 114 - 123
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Copyright
Copyright © Cambridge University Press 2015 

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References

Ahern, R.G., Hawthorne, D.J. & Raupp, M.J. (2009) Founder effects and phenotypic variation in Adelges cooleyi, an insect pest introduced to the eastern United States. Biological Invasions 11, 959–971.Google Scholar
Amin, S., Scheffer, S.J., Lewis, M.L., Pasha, M.K. & Bhuiya, B.A. (2014) DNA barcoding of the vegetable leafminer Liriomyza sativae Blanchard (Diptera: Agromyzidae) in Bangladesh. DNA Barcodes 2, 29–33.Google Scholar
Araujo, E.L., Nogueira, C.H.F., Menezes Netto, A.C. & Bezerra, C.E.S. (2013) Biological aspects of the leafminer Liriomyza sativae (Diptera: Agromyzidae) on melon (Cucumis melo L.). Ciência Rural 43, 579–582.Google Scholar
Ascunce, M.S., Yang, C.C., Oakey, J., Calcaterra, L., Wu, W.J., Shih, C.J., Goudet, J., Ross, K.G. & Shoemaker, D. (2011) Global invasion history of the fire ant Solenopsis invicta . Science 331, 1066–1068.Google Scholar
Bai, Y.C., Gu, X.S., Xu, W.H., Hu, X.X., Hao, Y.J. & Liu, B.M. (2009) Susceptibility of the parasitoids populations of Liriomyza sativae Blanchard to chemicals commonly used in vegetable crops. Acta Agriculturae Boreali-Sinica 3, 017.Google Scholar
Baker, D.A., Loxdale, H.D. & Edwards, O.R. (2003) Genetic variation and founder effects in the parasitoid wasp, Diaeretiella rapae (M'intosh) (Hymenoptera: Braconidae: Aphidiidae), affecting its potential as a biological control agent. Molecular Ecology 12, 3303–3311.Google Scholar
Beerli, P. (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22, 341–345.Google Scholar
Chen, X.X., Lang, F.Y., XU, Z.H., He, J.H. & Ma, Y. (2003) The occurrence of leafminers and their parasitoids on vegetables and weeds in Hangzhou area, Southeast China. Biocontrol 48, 515–527.Google Scholar
Chu, D., Gao, C.S., De Barro, P., Wan, F.H. & Zhang, Y.J. (2011) Investigation of the genetic diversity of an invasive whitefly (Bemisia tabaci) in China using both mitochondrial and nuclear DNA markers. Bulletin of Entomological Research 101, 467–475.Google Scholar
Cornuet, J.M. & Luikart, G. (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.Google Scholar
Di Rienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M. & Freimer, N.B. (1994) Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences of the United States of America 91, 3166–3170.Google Scholar
Du, Y.Z., Wang, L.P., Lu, Y.J., Zheng, F.S. & Lu, Z.Q. (2008) Differentiation of different host-populations and geo-populations of Liriomyza sativae Blanchard based on beta -tubulin gene sequences. Scientia Agricultura Sinica 41, 1542–1547.Google Scholar
Du, Y.Z., Tang, X.T., Wang, L.P., Shen, Y. & Chang, Y.W. (2014) Genetic differentiation of geographical populations of Liriomyza sativae (Diptera: Agromyzidae) in China based on mitochondrial COI gene sequences. Mitochondrial DNA doi: 10.3109/19401736.2014.987271.Google Scholar
Estoup, A. & Cornuet, J.M. (2000) Microsatellite evolution: inferences from population data. pp. 49–65 in Goldstein, D.B. & Schlotterer, C. (Eds) Microsatellites: Evolution and Applications. Oxford, Oxford University Press.Google Scholar
Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.Google Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1, 47.Google Scholar
Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.Google Scholar
Felsenstein, J. (1995) PHYLIP (Phylogeny Inference Packages). Version 3.57c. Seattle, Washington, USA, University of Washington.Google Scholar
Gao, Y.L., Reitz, S.R., Wei, Q.B., Yu, W.Y. & Lei, Z.R. (2012) Insecticide-mediated apparent displacement between two invasive species of leafminer fly. PLoS ONE 7, e36622.Google Scholar
Glaubitz, J.C. (2004) Convert: a user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Molecular Ecology Notes 4, 309–310.CrossRefGoogle Scholar
Guillot, G., Estoup, A., Mortier, F. & Cosson, J.F. (2005 a) A spatial statistical model for landscape genetics. Genetics 170, 1261–1280.Google Scholar
Guillot, G., Mortier, F., & Estoup, A. (2005 b) GENELAND: a computer package for landscape genetics. Molecular Ecology Notes 5, 712–715.Google Scholar
Guo, S.W. & Thompson, E.A. (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48, 361–372.Google Scholar
Jakobsson, M. & Rosenberg, N.A. (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.Google Scholar
Jensen, J.L., Bohonak, A.J. & Kelley, S.T. (2005) Isolation by distance, web service. BMC Genetics 6, 13.Google Scholar
Ji, Y. & Du, Y.Z. (2013) Isolation and characterization of microsatellite loci for Liriomyza sativae (Diptera: Agromyzidae) (in permanent genetic resources added to molecular ecology resources database 1 February 2013–31 March 2013). Molecular Ecology Resources 13, 760–762. http://dx.doi.org/10.1111/1755-0998.12121 Google Scholar
Johnson, M.W. (1993) Biological control of Liriomyza leafminers in the Pacific Basin. Micronesica 4, 81–92.Google Scholar
Kang, L. (1996) Ecology and Sustainable Control of Serpentine Leafminer. Beijing, Science Press.Google Scholar
Lozier, J.D., Roderick, G.K. & Mills, N.J. (2009) Tracing the invasion history of mealy plum aphid, Hyalopterus pruni (Hemiptera: Aphididae), in North America: a population genetics approach. Biological Invasions 11, 299–314.Google Scholar
Maruyama, T. & Fuerst, A. (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111, 675–689.Google Scholar
Murphy, S.T. & LaSalle, J. (1999) Balancing biological control strategies in the IPM of New World invasive Liriomyza leafminers in field vegetable crops. Biocontrol News and Information 20, 91–104.Google Scholar
Petitt, F.L. & Wietlisbach, D.O. (1994) Laboratory rearing and life history of Liriomyza sativae (Diptera: Agromyzidae) on lima bean. Environmental Entomology 23, 1416–1421.Google Scholar
Piry, S., Luikart, G. & Cornuet, J.M. (1999) Bottleneck: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90, 502–503.Google Scholar
Primmer, C.R., Saino, N., Møller, A.P. & Ellegren, H. (1998) Unraveling the processes of microsatellite evolution through analysis of germ line mutations in barn swallows Hirundo rustica . Molecular Biology and Evolution 15, 1047–1054.Google Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.Google Scholar
Rauf, A., Shepard, B.M. & Johnson, M.W. (2000) Leafminers in vegetables, ornamental plants and weeds in Indonesia: surveys of host crops, species composition and parasitoids. International Journal of Pest Management 46, 257–266.Google Scholar
Reitz, S.R., Kund, G.S., Carson, W.G., Phillips, P.A. & Trumble, J.T. (1999) Economics of reducing insecticide use on celery through low-input pest management strategies. Agriculture, Ecosystems & Environment 73, 185–197.Google Scholar
Saberfar, F., Garjan, A.S., Naseri, B. & Rashid, M. (2012) Comparative toxicity of abamectin, cyromazine and spinosad against the leaf-miner fly, Liriomyza sativae (Dip.: Agromyzidae). Journal of Entomological Society of Iran 32, 125–133.Google Scholar
Saryazdi, G.A., Hejazi, M.J., Rashidi, M.R. & Ferguson, S. (2014) Incidence and characterization of resistance to fenpropathrin in some Liriomyza sativae (Diptera: Agromyzidae) populations in Iran. Journal of Economic Entomology 107, 1908–1915.Google Scholar
Scheffer, S.J. (2005) Invasive Diptera: using molecular markers to investigate cryptic species and the global spread of flies. pp. 371–387 in Wiegmann, B.M. & Yeates, D.K. (Eds) The Evolutionary Biology of Flies. New York, Columbia University Press.Google Scholar
Scheffer, S.J. & Lewis, M.L. (2005) Mitochondrial phylogeography of vegetable pest Liriomyza sativae (Diptera: Agromyzidae): divergent clades and invasive populations. Annals of the Entomological Society of America 98, 181–186.Google Scholar
Scheffer, S.J., Lewis, M.L. & Joshi, R.C. (2006) DNA barcoding applied to invasive leafminers (Diptera: Agromyzidae) in the Philippines. Annals of the Entomological Society of America 99, 204–210.Google Scholar
Schmitt, T., Cizek, D. & Konvicka, M. (2005) Genetics of a butterfly relocation: large, small and introduced populations of the mountain endemic Erebia epiphron silesiana . Biological Conservation 123, 11–18.Google Scholar
Shiao, S.F. (2004) Morphological diagnosis of six Liriomyza species (Diptera: Agromyzidae) of quarantine importance in Taiwan. Applied Entomology and Zoology 39, 27–39.Google Scholar
Spencer, K.A. (1973) Agromyzidae (Diptera) of Economic Importance, Series Entomologica, 9. The Hague, The Netherlands, Dr. W. Junk B.V.Google Scholar
Spencer, K.A. (1990) Host Specialization in the World Agromyzidae (Diptera) , Series Entomologica, Vol. 45. Dordrecht, The Netherlands, Kluwer.Google Scholar
Suarez, A.N. & Tsutsui, N.D. (2008) The evolutionary consequences of biological invasions. Molecular Ecology 17, 351–360.Google Scholar
Tang, X.T., Tao, H.H., Wang, J.R. & Du, Y.Z. (2014 a) Microsatellite markers for Aleurocanthus spiniferus (Hemiptera: Aleyrodidae) and their potential use in whiteflies. Florida Entomologist 97, 1035–1040.Google Scholar
Tang, X.T., Xu, J., Sun, M., Xie, F.F. & Du, Y.Z. (2014 b) First Microsatellites from Sesamia inferens (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 107, 866–871.Google Scholar
Tang, X.T., Tao, H.H. & Du, Y.Z. (2015) Microsatellite-based analysis of the genetic structure and diversity of Aleurocanthus spiniferus (Hemiptera: Aleyrodidae) from tea plants in China. Gene 560, 107–113.Google Scholar
Tian, X.T., Zhang, J., Li, D. & Cheng, W.N. (2013) Effects of exogenous jasmonic acid on resistance of kidney bean to Liriomyza sativae . Acta Phytophylacica Sinica 40, 345–349.Google Scholar
Van oosterhout, C., Hutchinson, W.f., Wills, D.P. & Shipley, P. (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology 4, 535–538. http://www.uga.edu/srel/DNA_Lab/protocols.htm Google Scholar
Wan, X., Nardi, F., Zhang, B. & Liu, Y. (2011) The oriental fruit fly, Bactrocera dorsalis, in China: origin and gradual inland range expansion associated with population growth. PLoS ONE 6, e25238.Google Scholar
Wang, K.G. (2013) Influences of Temperature and Host Plants on Interspecific Competition Between Liriomyza sativae and Liriomyza trifolii. Beijing, Chinese Academy of Agricultural Sciences, pp. 10–14.Google Scholar
Wang, C.L. & Zhao, S.Q. (1998) IPM of pests and diseases of vegetables: occurrence and control of Liriomyza sativae . China Vegetables 3, 54–56.Google Scholar
Wang, L.P., Du, Y.Z., He, Y.T., Zheng, F.S. & Lu, Z.Q. (2008) Genetic variation of host populations of Liriomyza sativae Blanchard. Agricultural Sciences in China 7, 585–590.Google Scholar
Wright, S. (1938) Size of population and breeding structure in relation to evolution. Science 87, 430–443.Google Scholar
Xiang, J.C., Lei, Z.R., Wang, H.H. & Gao, Y.L. (2012) Interspecific competition among three invasive Liriomyza species. Acta Ecologica Sinica 32, 1616–1622.Google Scholar
Yang, F., Du, Y.Z., Wang, L.P., Cao, J.M. & Yu, W.W. (2011) The complete mitochondrial genome of the leafminer Liriomyza sativae (Diptera: Agromyzidae): Great difference in the A+ T-rich region compared to Liriomyza trifolii . Gene 485, 7–15.Google Scholar
Yang, X.M., Sun, J.T., Xue, X.F., Li, J.B. & Hong, X.Y. (2012) Invasion genetics of the western flower thrips in China: evidence for genetic bottleneck, hybridization and bridgehead effect. PLoS ONE 7, e34567.Google Scholar
Yang, F., Du, Y., Cao, J. & Huang, F. (2013) Analysis of three leafminers’ complete mitochondrial genomes. Gene 529, 1–6.Google Scholar
Yeh, F.C., Yang, R.C. & Boyle, T. (1999) Popgene Version 1.31 Quick User Guide. Canada, University of Alberta, and Centre for International Forestry Research.Google Scholar
Yi, H. (2014) Studies on Interspecific Competition Between Liriomyza sativae and Liriomyza trifolii. Shaanxi, Shaanxi Normal University, pp. 37–45.Google Scholar
Yildirim, E.M., Civelek, H.S., Dursun, O. & Eskin, A. (2012) The parasitism rate of Diglyphus isaea (Hymenoptera: Eulophidae) on Liriomyza sativae Blanchard (Diptera: Agromyzidae) in Mugla Province. Journal of Applied Biological Sciences 6, 21–23.Google Scholar
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