Skip to main content
SpringerLink
Log in

Evidence of a high level of gene flow among apple trees in Tetranychus urticae

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

The dispersal mechanism of the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) could affect predator–prey population dynamics and the spread of acaricide resistance. To investigate the propensity for spider mite migration in the field, the genetic structure of spider mite populations was studied in two apple orchards using five microsatellite markers. Adult female mites were collected from trees separated by approximately 10–24 m along a line covering a distance of about 100 m. The genetic data suggested that a high population density increased the migration rate among the breeding colonies within a single tree. Spatial autocorrelation analysis suggested a positive genetic structure in the first distance class within the two orchards, which might have been caused by crawling or short-distance aerial dispersal. Meanwhile, mites may also have a large-scale migration system that could cause a high level of gene flow and constrained isolation-by-distance or genetic clines within the approximately 100-m range of the study sites. Therefore, mites might aerially disperse over long distances on a scale of <100 m while also taking shorter trips among nearby trees within a distance of 10–24 m in the apple orchards.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alves EB, Casarin NFB, Omoto C (2005) Dispersal mechanisms of Brevipalpus phoenicis (Geijskes) (Acari: Tenuipalpidae) in citrus groves. Neotrop Entomol 34:89–96

    Google Scholar 

  • Bolland HR, Gutierrez J, Flechtmann CHW (1998) World catalogue of the spider mite family (Acari: Tetranychidae), with references to taxonomy, synonymy, host plants and distribution. Brill Academic Publishers, Leiden

    Google Scholar 

  • Boykin LS, Campbell WV (1984) Wind dispersal of the two-spotted spider mites (Acari: Tetranychidae) in North Carolina peanut fields. Environ Entomol 13:212–227

    Google Scholar 

  • Caprio MA, Tabashnik BE (1992) Gene flow accelerates local adaptation among finite populations—simulating the evolution of insecticide resistance. J Econ Entomol 85:611–620

    Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenic analysis: models and estimation procedures. Am J Hum Genet 19:233–257

    CAS  PubMed  Google Scholar 

  • Chevillon C, Raymond M, Guillemaud T et al (1999) Population genetics of insecticide resistance in the mosquito Culex pipiens. Biol J Lin Soc 68:147–157. doi:10.1111/j.1095-8312.1999.tb01163.x

    Article  Google Scholar 

  • Coad BR (1931) Insects captured by airplane are found at surprising heights. US Dept Agric Yearbk 1931:320–323

    Google Scholar 

  • Croft BA, van de Baan HE (1988) Ecological and genetic factors influencing evolution of pesticide resistance in teranychid and phytoseiid mites. Exp Appl Acarol 4:277–300. doi:10.1007/BF01196191

    Article  CAS  Google Scholar 

  • Dunley JE, Croft BA (1992) Dispersal and gene flow of pesticide resistance traits in phytoseiid tetranychid mites. Exp Appl Acarol 14:313–325. doi:10.1007/BF01200570

    Article  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa L. Skeels) endemic of Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • Endersby NM, McKechnie SW, Ridland PM et al (2006) Microsatellites reveal a lack of structure in Australian populations of the diamondback moth, Plutella xylostella (L.). Mol Ecol 15:107–118. doi:10.1111/j.1365-294X.2005.02789.x

    Article  CAS  PubMed  Google Scholar 

  • Goka K, Okabe K, Yoneda M et al (2001) Bumblebee commercialization will cause worldwide migration of parasitic mites. Mol Ecol 10:2095–2099. doi:10.1046/j.0962-1083.2001.01323.x

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available at http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 29 Apr 2009

  • Grafton-Cardwell EEJ, Granett J, Normington SM (1991) Influence of dispersal from almonds on the population-dynamics and acaricide resistance frequencies of spider mites infesting neighboring cotton. Exp Appl Acarol 10:187–212. doi:10.1007/BF01198650

    Article  Google Scholar 

  • Hinomoto N, Takafuji A (1994) Studies on the population structure of the two-spotted spider mite, Tetranychus urticae Koch, by allozyme variability analysis. Appl Entomol Zool (Jpn) 29:259–266

    Google Scholar 

  • Hinomoto N, Takafuji A (1995) Genetic changes in the population structure of the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), on vinyl-house strawberry. Appl Entomol Zool (Jpn) 30:521–528

    Google Scholar 

  • Hussey NW, Parr WJ (1963) Dispersal of the glasshouse red spider mite Tetranychus urticae Koch (Acari: Tetranychidae). Entomol Exp Appl 6:207–214. doi:10.1007/BF00300527

    Article  Google Scholar 

  • Kielkiewicz M (1996) Dispersal of Tetranychus cinnabarinus on various tomato cultivars. Entomol Exp Appl 80:254–257. doi:10.1007/BF00194769

    Article  Google Scholar 

  • Langella O (2002) POPULATIONS 1.2.28. Population genetic software (individuals or populations distances, phylogenetic trees). Available from http://bioinformatics.org/~tryphon/populations/. Accessed 29 Apr 2009

  • Lawson DS, Nyrop JP, Dennehy TJ (1996) Aerial dispersal of European red mites (Acari: Tetranychidae) in commercial apple orchards. Exp Appl Acarol 20:193–202. doi:10.1007/BF00054511

    Article  Google Scholar 

  • Li J, Margolies DC (1993a) Effects of mite age, mite density, and host quality on aerial dispersal behavior in the two-spotted spider mite. Entomol Exp Appl 68:79–86. doi:10.1007/BF02380584

    Article  Google Scholar 

  • Li J, Margolies DC (1993b) Quantitative genetics of aerial dispersal behavior and life-history traits in Tetranychus urticae. Heredity 70:544–552. doi:10.1038/hdy.1993.78

    Article  Google Scholar 

  • Margolies DC (1995) Evidence of selection on spider mite dispersal rates in relation to habitat persistence in agroecosystems. Entomol Exp Appl 76:105–108. doi:10.1007/BF02382315

    Article  Google Scholar 

  • Margolies DC, Kennedy GG (1988) Fenvalerate-induced aerial dispersal by the two-spotted spider mite. Entomol Exp Appl 46:233–240. doi:10.1007/BF00364194

    Article  Google Scholar 

  • Martinelli S, Clark PL, Zucchi MI et al (2007) Genetic structure and molecular variability of Spodoptera frugiperda (Lepidoptera: Noctuidae) collected in maize and cotton fields in Brazil. Bull Entomol Res 97:225–231. doi:10.1017/S0007485307004944

    Article  CAS  PubMed  Google Scholar 

  • Mitchell R (1973) Growth and population dynamics of a spider mite (Tetranychus urticae K., Acarina: Tetranychidae). Ecology 54:1349–1355. doi:10.2307/1934198

  • Morishita M (1992) Movement of two species of tetranychid mites (Acarina: Tetranychidae) from border vegetation to watermelon fields. Jap J Appl Entomol Zool 36:25–30 (in Japanese with English summary)

    Google Scholar 

  • Morishita M (1997) Intercrop movement of the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) from chrysanthemum to pea field. Jap J Appl Entomol Zool 41:33–38 (in Japanese with English summary)

    Google Scholar 

  • Navajas MJ, Thistlewood HMA, Lagnel J et al (1998) Microsatellite sequences are under-represented in two mite genomes. Insect Mol Biol 7:249–256. doi:10.1111/j.1365-2583.1998.00066.x

    Article  CAS  PubMed  Google Scholar 

  • Navajas M, Perrot-Minnot ML, Lagnel J et al (2002) Genetic structure of a greenhouse population of the spider mite Tetranychus urticae: spatio-temporal analysis with microsatellite markers. Insect Mol Biol 11:157–165. doi:10.1046/j.1365-2583.2002.00320.x

    Article  CAS  PubMed  Google Scholar 

  • Nishimura S, Hinomoto N, Takafuji A (2003) Isolation, characterization, inheritance and linkage of microsatellite markers in Tetranychus kanzawai (Acari: Tetranychidae). Exp Appl Acarol 31:93–103. doi:10.1023/B:APPA.0000005128.70282.a4

    Article  CAS  PubMed  Google Scholar 

  • Osakabe Mh, Komazaki S (1999) Laboratory experiments on a change in genetic structure with an increase of population density in the citrus red mite population, Panonychus citri (McGregor) (Acari: Tetranychidae). Appl Entomol Zool (Jpn) 34:413–420

    Google Scholar 

  • Osakabe Mh, Goka K, Toda S et al (2005) Significance of habitat type for the genetic population structure of Panonychus citri (Acari: Tetranychidae). Exp Appl Acarol 36:25–40. doi:10.1007/s10493-005-1672-1

    Article  PubMed  Google Scholar 

  • Osakabe Mh, Isobe H, Kasai A et al (2008) Aerodynamic advantages of upside down take-off for aerial dispersal in Tetranychus spider mites. Exp Appl Acarol 44:165–183. doi:10.1007/s10493-008-9141-2

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  • Pels B, Sabelis MW (1999) Local dynamics, overexploitation and predator dispersal in an acarine predator–prey system. Oikos 86:573–583. doi:10.2307/3546662

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249

    Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  Google Scholar 

  • Smitley DR, Kennedy GG (1985) Photo-oriented aerial dispersal behavior of Tetranychus urticae (Acari, Tetranychidae) enhances escape from the leaf surface. Ann Entomol Soc Am 78:609–614

    Google Scholar 

  • Smitley DR, Kennedy GG (1988) Aerial dispersal of the tow-spotted spider mite (Tetranychus urticae) from field corn. Exp Appl Acarol 5:33–46. doi:10.1007/BF02053815

    Article  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573. doi:10.1038/sj.hdy.6885180

    Article  PubMed  Google Scholar 

  • Tsagkarakou A, Navajas M, Lagnel J et al (1997) Population structure in the spider mite Tetranychus urticae (Acari: Tetranychidae) from Crete based on multiple allozymes. Heredity 78:84–92. doi:10.1038/hdy.1997.10

    Article  CAS  PubMed  Google Scholar 

  • Tsagkarakou A, Navajas M, Papaioannou-Souliotis P et al (1998) Gene flow among Tetranychus urticae (Acari: Tetranychidae) populations in Greece. Mol Ecol 7:71–79. doi:10.1046/j.1365-294x.1998.00305.x

    Article  CAS  Google Scholar 

  • Tsagkarakou A, Navajas M, Rousset F et al (1999) Genetic differentiation in Tetranychus urticae (Acari: Tetranychidae) from greenhouses in France. Exp Appl Acarol 23:365–378. doi:10.1023/A:1006293627880

    Article  Google Scholar 

  • Uesugi R, Osakabe Mh (2007) Isolation and characterization of microsatellite loci in the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae). Mol Ecol Notes 7:290–292. doi:10.1111/j.1471-8286.2006.01583.x

    Article  CAS  Google Scholar 

  • Uesugi R, Kunimoto Y, Osakabe Mh (2009) The fine-scale genetic structure of the two-spotted spider mite in a commercial greenhouse. Exp Appl Acarol 47:99–109. doi:10.1007/s10493-008-9201-7

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J Org Evol 38:1358–1370. doi:10.2307/2408641

    Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was partially supported by a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology, Japan, a Grant-in-Aid from the twenty-first Century COE Program for Innovative Food and Environmental Studies Pioneered by Entomomimetic Sciences at Kyoto University, and a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (B; no. 2238-19, 2007).

Author information

Authors and Affiliations

  1. Laboratory of Ecological Information, Graduate School of Agriculture, Kyoto University, Oiwake-cho, Sakyo-ku, Kyoto, 606-8502, Japan

    Ryuji Uesugi & Mh. Osakabe

  2. Nagano Fruit Tree Experiment Station, 492 Ogawara, Suzaka, Nagano, 382-0072, Japan

    Terunori Sasawaki

Authors
  1. Ryuji Uesugi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Terunori Sasawaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mh. Osakabe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ryuji Uesugi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Uesugi, R., Sasawaki, T. & Osakabe, M. Evidence of a high level of gene flow among apple trees in Tetranychus urticae . Exp Appl Acarol 49, 281–290 (2009). https://doi.org/10.1007/s10493-009-9267-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-009-9267-x

Keywords

Search

Navigation