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Contrasting effects of geographical separation on the genetic population structure of sympatric species of mites in avocado orchards

  • S. Guzman-Valencia (a1), M.T. Santillán-Galicia (a1), A.W. Guzmán-Franco (a1), H. González-Hernández (a1), M.G. Carrillo-Benítez (a1) and J. Suárez-Espinoza (a2)...


Oligonychus punicae and Oligonychus perseae (Acari: Tetranychidae) are the most important mite species affecting avocado orchards in Mexico. Here we used nucleotide sequence data from segments of the nuclear ribosomal internal transcribed spacers (ITS1 and ITS2) and mitochondrial cytochrome oxidase subunit I (COI) genes to assess the phylogenetic relationships between both sympatric mite species and, using only ITS sequence data, examine genetic variation and population structure in both species, to test the hypothesis that, although both species co-occur, their genetic population structures are different in both Michoacan state (main producer) and Mexico state. Phylogenetic analysis showed a clear separation between both species using ITS and COI sequence information. Haplotype network analysis done on 24 samples of O. punicae revealed low genetic diversity with only three haplotypes found but a significant geographical population structure confirmed by analysis of molecular variance (AMOVA) and Kimura-2-parameter (K2P) analyses. In addition, a Mantel test revealed that geographical isolation was a factor responsible for the genetic differentiation. In contrast, analyses of 22 samples of O. perseae revealed high genetic diversity with 15 haplotypes found but no geographical structure confirmed by the AMOVA, K2P and Mantel test analyses. We have suggested that geographical separation is one of the most important factors driving genetic variation, but that it affected each species differently. The role of the ecology of these species on our results, and the importance of our findings in the development of monitoring and control strategies are discussed.


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Aponte, O. & McMurtry, J.A. (1997) Damage on 'Hass' avocado leaves, webbing and nesting behaviour of Oligonychus perseae (Acari: Tetranychidae). Experimental and Applied Acarology 21, 265272.
APROAM (Asociación de Productores de Aguacate de Uruapan Michoacán) (2007). Available from (Page visited on February 8th, 2011).
Bailly, X.A., Migeon, A., & Navajas, M. (2004) Analysis of microsatellite variation in the spider mite pest Tetranychus turkestani (Acari: Tetranychidae) reveals population genetic structure and raises questions about related ecological factors. Biological Journal of the Linnean Society 82, 6978.
Baker, E.W. & Tuttle, D.M. (1994) A Guide to the Spider Mites (Tetranychidae) of the United States. Indira, West Bloomfield, MI.
Balloux, F. & Lugon-Moulin, N. (2002) The estimation of population differentiation with microsatellite markers. Molecular Ecology 11, 155165.
Ben-David, T., Melamed, S., Gerson, U. & Morin, S. (2007) ITS2 sequences as barcodes for identifying and analyzing spider mites (Acari:Tetranychidae). Experimental and Applied Acarology 41, 169181.
Bitume, E.V., Bonte, D., Ronce, O., Bach, F., Flaven, E., Olivieri, I. & Nieberding, C.M. (2013) Density and genetic relatedness increase dispersal distance in subsocial organism. Ecology Letters 16, 430437.
Bolland, H.R., Gutierrez, J. & Flechtmann, C.H.W. (1998) World Catalogue of the Spider Mite Family (Acari: Tetranychidae). Leiden, Brill Academic Publishers.
Carbonnelle, S., Hance, T., Migeon, A., Baret, P., Cros-Arteil, S. & Navajas, M. (2007) Microsatellite markers reveal spatial genetic structure of Tetranychus urticae (Acari: Tetranychidae) populations along a latitudinal gradient in Europe. Experimental and Applied Acarology 41, 225241.
Clement, M., Posada, D. & Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571660.
Cruickshank, R. (2002) Molecular markers for the phylogenetics of mites and ticks. Systematic and Applied Acarology 7, 314.
David, J.K., Huber, A., Failloux, D.R. & Meyran, J. (2003) The role of environment in shaping the genetic diversity of the subalpine mosquito, Aedes rusticus (Diptera, Culicidae). Molecular Ecology 12, 19511961.
Excoffier, L. & Lischer, H.E.L. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564567.
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791.
Gotoh, T., Bruin, J., Sabelis, M.W. & Menken, S.B.J. (1993) Host race formation in Tetranychus urticae: genetic differentiation, host plant preference, and mate choice in a tomato and a cucumber strain. Entomologia Experimentalis et Applicata 68, 171178.
Grbić, M., Van Leeuwen, T., Clark, R.M., Rombauts, S., Rouzé, P., Grbić, V., Osborne, E.J., Dermauw, W., Thi Ngoc, P.K., Ortego, F., Hernández-Crespo, P., Diaz, I., Martinez, M., Navajas, M., Sucena, É., Magalhães, S., Nagy, L., Pace, R.M., Djuranović, S., Smagghe, G., Iga, M., Christiaens, O., Veenstra, J.A., Ewer, J., Mancilla Villalobos, R., Hutter, J.L., Hudson, S.D., Velez, M., Yi, S.V., Zeng, J., Pires-daSilva, A., Roch, F., Cazaux, M., Navarro, M., Zhurov, V., Acevedo, G., Bjelica, A., Fawcett, J.A., Bonnet, E., Martens, C., Baele, G., Wissler, L., Sanchez-Rodriguez, A., Tirry, L., Blais, C., Demeestere, K., Henz, S.R., Gregory, T.R., Mathieu, J., Verdon, L., Farinelli, L., Schmutz, J., Lindquist, E., Feyereisen, R. & Van de Peer, Y. (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479, 487492.
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.
Hamilton, W.D. & May, R.M. (1977) Dispersal in stable habitats. Nature 269, 578581.
Harrison, S. & Hastings, A. (1996) Genetic and evolutionary consequences of metapopulation structure. Trends in Ecology and Evolution 11, 180183.
Hebert, D.N., Cywinska, A., Ball, S.L. & De Waard, R. (2003) Biological identifications through ADN barcodes. Proceeding of the Royal Society of London. Series B 270, 313321.
Helle, W. & Overmeer, W.P.J. (1973) Variability in Tetranychidae mites. Annual Review of Entomology 18, 97120.
Helle, W. & Sabelis, M.W. (1985) Spider Mites: their Biology, Natural Enemies and Control. Amsterdam, Elsevier Science Publisher.
Hinomoto, N. & Takafuji, A. (1994) Studies on the population structure of the two-spotted spider mite, Tetranychus urticae Koch, by allozyme variability analysis. Applied Entomology and Zoology 29, 259266.
Hurtado, M.A., Ansaloni, T., Cros-Arteil, S., Jacas, J.A. & Navajas, M. (2008) Sequence analysis of the ribosomal internal transcribed spacers region in spider mites (Prostigmata: Tetranychidae) occurring in citrus orchards in Eastern Spain: use for species discrimination. Annals of Applied Biology 153, 167174.
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.
Jensen, J., Bohonak, A. & Kelley, S. (2005) Isolation by distance, web service. BMC Genetics 6, 13.
Jeppson, L.R., Keifer, H.H. & Baker, E.W. (1975) Mites Injurious to Economic Plants. Berkeley, University of California Press.
Kerguelen, V. & Hoddle, M.S. (2000) Comparison of the susceptibility of several cultivars of avocado to the persea mite, Oligonychus perseae (Acari: Tetranychidae). Scientia Horticulturae 84, 101114.
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.
Knutsen, H., Rukke, B.A., Jorde, P.E. & Ims, R.A. (2000) Genetic differentiation among populations of the beetle Bolitophagus reticulates (Coleoptera: Tenebrionidae) in a fragmented and a continuous landscape. Heredity 84, 667676.
Krantz, G.W. & Walter, D.E. (2009) A Manual of Acarology. Texas, Texas Tech University Press.
Navajas, M. & Fenton, B. (2000) The application of molecular markers in the study of diversity in acarology: a review. Experimental and Applied Acarology 24, 751774.
Navajas, M., Perrot-Minnot, M.J., Lagnel, J., Migeon, A., Bourse, T. & Cornuet, J.M. (2002) Genetic structure of a greenhouse population of the spider mite Tetranychus urticae: spatio-temporal analysis with microsatellite markers. Insect Molecular Biology 11, 157165.
Nishimura, S., Hinomoto, N. & Takafuji, A. (2005) Gene flow and spatio-temporal genetic variation among sympatric populations of Tetranychus kanzawai (Acari: Tetranychidae) occurring on different host plants, as estimated by microsatellite gene diversity. Experimental and Applied Acarology 35, 5971.
Roeder, C., Harmsen, R. & Mouldey, S. (1996) The effects of relatedness on progeny sex ratio in spider mites. Journal of Evolutionary Biology 9, 143151.
Ruiz, E.A., Rinehart, J.E., Hayes, J.L. & Zuniga, G. (2009) Effect of geographic isolation on genetic differentiation in Dendroctonus pseudotsugae (Coleoptera: Curculionidae). Hereditas 146, 7992.
Sun, J.T., Lian, C., Navajas, M. & Hong, X.Y. (2012) Microsatellites reveal a strong subdivision of genetic structure in Chinese populations of the mite Tetranychus urticae Koch (Acari: Tetranychidae). BMC Genetics 13, 113.
Tamura, K., Paterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.
Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619633.
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.
Tsagkarakou, A., Navajas, M., Papaioannou-Souliotis, P. & Pasteur, N. (1998) Gene flow among Tetranychus urticae (Acari: Tetranychidae) populations in Greece. Molecular Ecology 6, 305–14.
Tsagkarakou, A., Navajas, M., Rousset, F. & Pasteur, N. (1999) Genetic differentiation in Tetranychus urticae (Acari: Tetranychidae) from greenhouses in France. Experimental and Applied Acarology 23, 365378.
van Valen, L. (1971) Group selection and the evolution of dispersal. Evolution 25, 591598.
Weeks, A.R., Van Opijnen, T. & Breeuwer, A.J. (2000) AFLP fingerprinting for assessing intraspecific variation and genome mapping in mites. Experimental and Applied Acarology 24, 775793.
Yuan, M.L., Wang, B.J., Lu, F., Hu, C.X., Wei, D.D., Dou, W. & Wang, J.J. (2011) Evaluation of genetic diversity and population structure of Panonychus citri (Acari: Tetranychidae) in China using ribosomal internal transcribed spacer 1 sequences. Annals of the Entomological Society of America 104, 800807.


Contrasting effects of geographical separation on the genetic population structure of sympatric species of mites in avocado orchards

  • S. Guzman-Valencia (a1), M.T. Santillán-Galicia (a1), A.W. Guzmán-Franco (a1), H. González-Hernández (a1), M.G. Carrillo-Benítez (a1) and J. Suárez-Espinoza (a2)...


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