Skip to main content
SpringerLink
Log in

Phylogeography of the Asian rice gall midge Orseolia oryzae (Wood Mason) (Diptera: Cecidomyiidae) in Thailand

  • Original Paper
  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The Asian rice gall midge (RGM) Orseolia oryzae (Wood Mason) (Diptera: Cecidomyiidae) is a major pest of rice, leading to yield losses in Thailand and many Asian countries. Despite an increasing number of reported midge outbreaks and the presence of many susceptible rice varieties, only a few studies have focused on the genetic variation of the midges. Therefore, we analyzed the phylogeography among Thai RGM populations covering north, northeast and central Thailand. Two mitochondrial DNA genes, cytochrome C oxidase I (COI) and 12S, and a non-coding repeat region (RR) situated just before COI were amplified. Overall, the haplotype diversity for COI and 12S genes of the Thai population was high, but the nucleotide diversity was quite low. Altogether, the phylogenetic tree and pairwise F st values indicated that Thai RGM populations recently expanded and were homogeneously distributed throughout the country, except for some populations in the north, which most likely became recently isolated from the main population. Two non-coding repeat motifs, that were recently observed in the mitogenome of RGM in India, were absent in Thai populations and replaced by an 89 bp non-coding sequence. Tandem nucleotide repeats of the sequence TA were also observed. The repeat copy number varied from 2 to 11 and was not correlated with geographical repartition of the midge. Finally, COI barcoding divergence between Indian and Thai populations was high (6.3% in average), giving insights into the potential existence of an RGM species complex in Asia.

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

Similar content being viewed by others

References

  • Atray I, Bentur JS, Nair S (2015) The Asian rice gall midge (Orseolia oryzae) mitogenome has evolved novel gene boundaries and tandem repeats that distinguish its biotypes. PloS one 10:e0134625

    Article  PubMed  PubMed Central  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Beard CB, Hamm D, Collins FH (1993) The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Mol Biol 2:103–124

    Article  CAS  PubMed  Google Scholar 

  • Beckenbach AT, Joy JB (2009) Evolution of the mitochondrial genomes of gall midges (Diptera: Cecidomyiidae): Rearrangement and severe truncation of tRNA genes. Genome Biol Evol 1:278–287

    Article  PubMed  PubMed Central  Google Scholar 

  • Behura SK, Sahu SC, Rajamani S, Devi A, Mago R, Nair S, Mohan M (1999) Differentiation of Asian rice gall midge, Orseolia oryzae (Wood-Mason), biotypes by sequence characterized amplified regions (SCARs). Insect Mol Biol 8:391–397

    Article  CAS  PubMed  Google Scholar 

  • Bennett J, Cohen MB, Katiyar SK, Ghareyazie B, Khush GS (1997) Enhancing insect resistance in rice through biotechnology. In: Carozzi N, Koziel M (eds) Advances in insect control: the role of transgenic plants. CRC Press, New York, pp 75–93

    Google Scholar 

  • Bentur JS, Sinha DK, Padmavathy C, Revathy C, Muthulakshmi M, Nagaraju J (2011) Isolation and characterization of microsatellite loci in the Asian rice gall midge (Orseolia oryzae) (Diptera: Cecidomyiidae). Int J Mol Sci 12:755–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bentur JS, Rawat N, Divya D, Sinha DK, Agarrwal R, Atray I, Nair S (2016) Rice–gall midge interactions: battle for survival. J Insect Physiol 84:40–49

    Article  CAS  PubMed  Google Scholar 

  • Briggs CJ, Latto J (2000) The effect of dispersal on the population dynamics of a gall-forming midge and its parasitoids. J Anim Ecol 69:96–105

    Article  Google Scholar 

  • Bush GL (1992) Host race formation and sympatric speciation in Rhagoletis fruit flies (Diptera: Tephritidae). Psyche 99:335–357

    Article  Google Scholar 

  • Chiengwattana N, Pattrasudhi R, Seangyai P, Pattawatang P, Kotcharerk J, Hintang P (2008) Monitoring and forecasting of rice gall midge (Orseolia oryzae Wood-Mason) dynamics in the infested areas of northern Thailand. In: Proceedings of rice and temperate cereal crops annual conference volume 2/2, 2008. Bangkok, Thailand, pp 263–284 (in Thai)

  • Clayton DA (1992a) Transcription and replication of animal mitochondrial DNAs. Int Rev Cytol 141:217–232

  • Clayton DA (1992b) Structure and function of the mitochondrial genome. J Inherit Metab Dis 15:439–447

  • Cornuet JM, Garnery L, Solignac M (1991) Putative origin and function of the intergenic region between COI and COII of Apis mellifera L. mitochondrial DNA. Genetics 128:393–403

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cywinska A, Hunter F, Hebert PD (2006) Identifying Canadian mosquito species through DNA barcodes. Med Vet Entomol 20:413–424

    Article  CAS  PubMed  Google Scholar 

  • Dutta SS, Divya D, Durga RC, Dayakar RT, Visalakshmi V, Cheralu C, Ibohal Singh K, Bentur JS (2014) Characterization of gall midge resistant rice genotypes using resistance gene specific markers. J Exp Biol Agric Sci 2:439–446

    Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • FAO (2013) Suivi du marché du riz; nov 2013. http://www.fao.org/3/a-as201f.pdf. Accessed 4 December 2016

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299

    CAS  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gagné RJ (1985) A taxonomic revision of the Asian rice gall midge Orseolia oryzae Wood-Mason and its relatives (Diptera: Cecidomyiidae). Entomography 3:127–162

    Google Scholar 

  • Goddard JM, Wolstenholme DR (1980) Origin and direction of replication in mitochondrial DNA molecules from the genus Drosophila. Nucleic Acids Res 8:741–757

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R (2010) A new bioinformatics analysis tools framework at EMBL–EBI. Nucleic Acids Res 38:W695–W699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

  • Gutiérrez MAC, Vivero RJ, Vélez ID, Porter CH, Uribe S (2014) DNA barcoding for the identification of sand fly species (Diptera, Psychodidae, Phlebotominae) in Colombia. PloS One 9:e85496

    Article  Google Scholar 

  • Harris M, Stuart J, Mohan M, Nair S, Lamb R, Rohfritsch O (2003) Grasses and gall midges: plant defense and insect adaptation. Ann Rev Entomol 48:549–577

    Article  CAS  Google Scholar 

  • Hebert PD, Gregory TR (2005) The promise of DNA barcoding for taxonomy. Syst Biol 54:852–859

    Article  PubMed  Google Scholar 

  • Hebert PD, Cywinska A, Ball SL (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321

    Article  CAS  Google Scholar 

  • Heinrichs EA (ed) (1994) Host plant resistance. In: Biology and management of rice insects. Wiley Eastern Limited, New Delhi, pp 517–547

  • Herdt RW (1991) Research priorities for rice biotechnology. In: Khush GS, Toenniesen GH T (eds) Rice biotechnology. Wallingford (UK). Commonwealth Agricultural Bureau International, Manila, pp 19–54

    Google Scholar 

  • Hidaka T, Ya-Klai V, Chantaraprapha N, Chantarasa-Art S (1978) Serious incidence of the rice gall midge in the central plain of Thailand. Appl Entomol Zool 13:260–263

    Google Scholar 

  • Hong G, Jiang S, Yu M, Yang Y, Li F, Xue F, Wei Z (2009) The complete nucleotide sequence of the mitochondrial genome of the cabbage butterfly, Artogeia melete (Lepidoptera: Pieridae). Acta Biochimi Biophys Sin 41:446–455

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Hillis DM (1993). Success of phylogenetic methods in the four-taxon case. Syst Biol 42:247–264

    Article  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: Managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Inthavong S, Schiller JM, Sengsoulivong V, Inthapanya P (2004) Status of gall midge in Lao PDR. In: Bennett J, Bentur JS, Pasalu IC, Krishnaiah K (eds) New approach to gall midge resistance in rice. Proceedings of the International Workshop 22–24 November, 1998. Hyderabad, India, pp 77–87

  • Jagadeesha Kumar BJ, Chakravarthy AK, Doddabasappa B, Basavaraju BS (2009) Biology of the rice gall midge, Orseolia oryzae (Wood-Mason) in southern Karnataka. Karnataka J of Agric Sci 22:535–537

    Google Scholar 

  • Jahn GC, Bunnarith K (2004) Gall midge in Cambodian lowland rice. In: Bennett J, Bentur JS, Pasalu IC, Krishnaiah K (eds) New approach to gall midge resistance in rice. Proceedings of the International Workshop. 22–24 November, 1998. Hyderabad, India, pp 71–76

  • Jairin J, Sansen K, Teangdeerith S, Leelakud P, Kawichai R, Sriratanasak W, Chiengwattana N (2009) Genetic Diversity and Biotypes of the Rice Gall Midge in Thailand. Thai Rice Res J 3:39–47 (in Thai with English abstract)

    Google Scholar 

  • Jobb G, Haeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:1

    Article  Google Scholar 

  • Katiyar SK, Chandel G, Tan Y, Chandel G, Xu Y, Zhang Y, Xie Z, Bennett J (2000) Biodiversity of Asian rice gall midge (Orseolia oryzae Wood Mason) from five countries examined by AFLP analysis. Genome 43:322–332

    Article  CAS  PubMed  Google Scholar 

  • Katiyar SK, Tan Y, Huang B et al (2001) Molecular mapping of gene Gm-6 (t) which confers resistance against four biotypes of Asian rice gall midge in China. Theor Appl Genet 103:953–961

    Article  CAS  Google Scholar 

  • Lakshmi PV, Amudhan S, Bindu KH, Cheralu C, Bentur JS (2006) A new biotype of the Asian rice gall midge Orseolia oryzae (Diptera: Cecidomyiidae) characterized from the Warangal population in Andhra Pradesh, India. Int J Trop Insect Sci 26:207–211

    Google Scholar 

  • Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759

    Article  CAS  Google Scholar 

  • Lingaraj VK, Chakravarthy AK, Eregowda TN (2008) Detection of Asian rice gall midge (Orseolia oryzae) biotype 1 in the new locations of Karnataka, South India. B Insectol 61:277–281

    Google Scholar 

  • Mardi G, Pandey AC, Kumar SS (2009) Occurrence and management of rice gall midge in transplanted rice (Orseolia oryzae Wood Mason). Ecol Env Cons 15:361–365

    Google Scholar 

  • Masta SE, Boore JL (2004) The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Mol Biol Evol 21:893–902

    Article  CAS  PubMed  Google Scholar 

  • Masters G, Norgrove L (2010) Climate change and invasive alien species. UK: CABI Working Paper, 1

  • Meier R, Zhang G (2009) DNA barcoding and DNA taxonomy in Diptera: an assessment based on 4,261 COI sequences for 1001 species. In: Pape T, Bickel DJ, Meier R (eds) Diptera diversity: status, challenges and tools. Brill, Leiden, pp 347–380

    Chapter  Google Scholar 

  • Oupkaew P, Pusadee T, Sirabanchongkran A, Rerkasem K, Jamjod S, Rerkasem B (2011) Complexity and adaptability of a traditional agricultural system: case study of a gall midge resistant rice landrace from northern Thailand. Genet Resour Crop Evol 58:361–372

    Article  Google Scholar 

  • Pedgley DE, Reynolds DR, Tatchell GM (1995) Long range insect migration in relation to climate and weather: Africa and Europe. In: Drake VA, Gatehouse AG (eds) Insect migration: tracking resources through space and time. Cambridge University Press, Cambridge, pp 3–29

    Chapter  Google Scholar 

  • Pendleton BB, Teetes GL (1994) Sorghum midge dispersal from sorghum. Southwestern Entomol 19:1–9

    Google Scholar 

  • Perrault A, Bennett M, Burgiel S, Delach A, Muffett C (2003) Invasive species, agriculture and trade: Case studies from the NAFTA context. North American Commission for Environmental Cooperation Working Paper. Montreal

  • Rajamani S, Pasalu IC, Mathur KC, Sain M (2004) Biology and ecology of rice gall midge. In: Bennett J, Bentur JS, Pasalu IC, Krishnaiah K (eds) New approach to gall midge resistance in rice. Proceedings of the International Workshop. 22–24 November, 1998. Hyderabad, India, pp 7–16

  • Rerkasem B (2015) The Agroecosystem of Thai rice: a review. CMU J Nat Sci 14:1–21

    Google Scholar 

  • Roderick GK (1996) Geographic structure of insect populations: Gene flow, phylogeography, and their uses. Ann Rev Entomol 19:325–352

    Article  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosen D (1978) The importance of cryptic species and specific identifications as related to biological control. In: Beltsville symposia in agricultural research (2). Biosystematics in agriculture. Invited papers presented at a symposium held May 8–11, 1977. Beltsville Agricultural Research Center (BARC), Beltsville, Maryland, pp 23–35

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Sardesai N, Rajyashri KR, Behura SK, Nair S, Mohan M (2001) Genetic, physiological and molecular interactions of rice and its major dipteran pest, gall midge. Plant Cell Tiss Org 64:115–131

    Article  CAS  Google Scholar 

  • Scheffer SJ, Wiegmann BM (2000) Molecular phylogenetics of the holly leafminers (Diptera: Agromyzidae: Phytomyza): Species limits, speciation, and dietary specialization. Mol Phylogenet Evol 17:244–255

    Article  CAS  PubMed  Google Scholar 

  • Shao R, Campbell NJ, Barker SC (2001) Numerous gene rearrangements in the mitochondrial genome of the wallaby louse, Heterodoxus macropus (Phthiraptera). Mol Biol Evol 18:858–865

    Article  CAS  PubMed  Google Scholar 

  • Simms EL (1987) Ecological genetics and evolution in insect pests: Implications for lower input agriculture. Am J Alternative Agric 2:153–159

    Article  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–702

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanabe AS (2007) Kakusan: a computer program to automate the selection of a nucleotide substitution model and the configuration of a mixed model on multilocus data. Mol Ecol Notes 7:962–964

    Article  CAS  Google Scholar 

  • Tayathum C, Junseesommaei N, Srirattanasak V (1995) Biotypes of rice gall midge, Orseolia oryzae (Wood-Mason) in Thailand. In Conference of Entomology and Zoology group. Ministry of Agriculture and Cooperative. Bangkok, Thailand, pp 160–172 (in Thai with English abstract)

  • Tayathum C, Attathom T, Thongphak D, Sripongpankul K (2004) Biology and ecology of rice gall midge. In: Bennett J, Bentur JS, Pasalu IC, Krishnaiah K (eds) New approach to gall midge resistance in rice. Proceedings of the International Workshop. 22–24 November, 1998 Hyderabad, India, pp 89–98

  • Telfer AC, Young MR, Quinn J et al (2015) Biodiversity inventories in high gear: DNA barcoding facilitates a rapid biotic survey of a temperate nature reserve. Biodivers Data J. doi:10.3897/BDJ.3.e6313

    PubMed  PubMed Central  Google Scholar 

  • Tinpalanai N (2009) Coping with the rice gall midge, a new insect pest of highland paddies, in upland villages in Mae Win, Chiang Mai, Thailand. In: Workshop of the use of agrobiodiversity by indigenous peoples and rural communities in adapting to climate change: Experiences, knowledge gaps and opportunities for collaboration. 17–20 June 2009, Chiang Mai, Thailand (in Thai)

  • Withers TM, Harris MO, Madie C (1997) Dispersal of mated female Hessian Flies (Diptera: Cecidomyiidae) in field arrays of host and nonhost plants. Environ Entomol 26:1247–1257

    Article  Google Scholar 

  • Wolstenholme DR (1992) Animal mitochondrial DNA: Structure and evolution. Int Rev Cytol 141:173–216

    Article  CAS  PubMed  Google Scholar 

  • Yajai P, Siangyai P (2013) Reaction of PRE01017-10-1-1-1 rice promising line to gall midge in the upper north under greenhouse condition. In: Proceedings of the 30th rice and temperate cereal crops annual conference, 5–7 June 2013, Bangkok, Thailand, pp 171–182 (in Thai with English abstract)

  • Zhang DX, Hewitt GM (1997) Insect mitochondrial control region: A review of its structure, evolution and usefulness in evolutionary studies. Biochem Syst Ecol 25:99–120

    Article  Google Scholar 

  • Ziska LH, Blumenthal DM, Runion GB, Hunt ER Jr, Diaz-Soltero H (2011) Invasive species and climate change: An agronomic perspective. Clim Change 105:13–42

    Article  Google Scholar 

Download references

Acknowledgements

This research project was supported by Mahidol University under the Talent Management Program and Faculty of Science, Mahidol University to EJ. We also would like to give our regards to Dr. Sangvorn Kitthawee and Dr. Jenjit Khudamrongsawat for comments as well as Dr. James Rudge and Stephan Schreier for comments and grammar checking.

Author information

Authors and Affiliations

  1. Animal Systematics and Molecular Ecology Laboratory, Department of Biology, Faculty of Science, Mahidol University, Bangkok, 10400, Thailand

    Solene Janique & Ekgachai Jeratthitikul

  2. Bureau of Rice Research and Development, Rice Department, Chatuchak, Bangkok, 10900, Thailand

    Wantana Sriratanasak

  3. Phrae Rice Research Center, P.O. Box 54, Mueang, Phrae, 54000, Thailand

    Kulchana Ketsuwan

  4. Ubon Ratchathani Rice Research Center, P.O. Box 65, Mueang, Ubon Ratchathani, 34000, Thailand

    Jirapong Jairin

Authors
  1. Solene Janique
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wantana Sriratanasak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kulchana Ketsuwan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jirapong Jairin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ekgachai Jeratthitikul
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ekgachai Jeratthitikul.

Ethics declarations

Conflict of interest

The authors have no conflict of interest.

Ethics statement

Orseolia oryzae is a serious insect pest of rice, Oryza sativa. It is not endangered species or protected by law. Therefore, no permits are required to study this insect.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 30 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Janique, S., Sriratanasak, W., Ketsuwan, K. et al. Phylogeography of the Asian rice gall midge Orseolia oryzae (Wood Mason) (Diptera: Cecidomyiidae) in Thailand. Genetica 145, 37–49 (2017). https://doi.org/10.1007/s10709-016-9944-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-016-9944-8

Keywords

Search

Navigation