Skip to main content
Log in

Molecular characterization and phylogenetic comparisons of three Mayetiola species (Diptera: Cecidomyiidae) infesting cereals in Tunisia

Applied Entomology and Zoology Aims and scope Submit manuscript

Abstract

Species from the genus Mayetiola are observed in the main cereal cultures of Tunisia. Some researchers have studied M. destructor that attacks wheat and M. hordei that attacks barley. However, a third important species observed in oat, M. avenae, has not been studied and is not well documented in Tunisia. A method to easily separate the species is needed to clarify the occurrences of these gall midge species. This study aimed to first distinguish between the three species of gall midges by molecular characterization and second to reveal the phylogenetic relationships within and between the three species of Mayetiola collected from 5 different regions of northern Tunisia. To achieve these purposes, two regions of the mitochondrial DNA, cytochrome oxidase subunit I gene, and the 16S rRNA gene were amplified by polymerase chain reaction and sequenced. For each marker, a set of 75 individuals were used for DNA analysis. Phylogenetic trees were created using the DNA sequences of all samples from the 3 species. Results showed significant separation of the three different species into dissimilar clades. Each clade contained only specimens from the same species. Differences were observed between DNA sequences of the same species. The differences within the same species were not representative of geographical variations but coexisted within a population Therefore, using the COI and 16S rRNA genes as markers can clearly separate M. avenae, M. destructor and M. hordei.

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

Access this article

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

References

  • Augot D, Sauvage F, Jouet D, Simphal E, Veuille M, Couloux A, Kaltenbach ML, Depaquit J (2010) Discrimination of Culicoidesobsoletus and Culicoidesscoticus, potential bluetongue vectors, by morphometrical and mitochondrial cytochrome oxidase subunit I analysis. Infect Genet Evol 10:629–637

    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 

  • Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271

    Article  CAS  PubMed  Google Scholar 

  • Cywinska A, Hannan MA, Kevan PG, Roughley RE, Iranpour M, Hunter FF (2010) Evaluation of DNA barcoding and identification of new haplomorphs in Canadian deerflies and horseflies. Med Vet Entomol 24:382–410

    Article  CAS  PubMed  Google Scholar 

  • Dorchin N, Scott ER, Clarkin CE, Luongo MP, Jordan S, Abrahamson WG (2009) Behavioural, ecological and genetic evidence confirm the occurrence of host-associated differentiation in goldenrod gall-midges. J Evol Biol 22:729–739

    Article  CAS  PubMed  Google Scholar 

  • Efron B (1982) The jackknife, the bootstrap, and other resampling plans. In: CBMS-NSF regional conference series in applied mathematics, SIAM J Appl Math, pp 92

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Funk DJ, Futuyama DJ, Orti G, Meyer A (1995) Mitochondrial DNA sequences and multiple data sets: a phylogenetic study of phytophagous beetles (Chrysomelidae:Opharaella). Mol Biol Evol 12:627–640

    CAS  PubMed  Google Scholar 

  • Gagné RJ, Jaschhof M (2014) A catalog of the Cecidomyiidae (Diptera) of the world, 3rd edn. Digital version 2. https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_2014_World_Cecidomyiidae_Catalog_3rd_Edition.pdf

  • Gagné RJ, Hatchett JH, Lhaloui S, El Bouhssini M (1991) Hessian fly and barley gall midge, two different species of Mayetiola (Diptera: Cecidomyiidae) in Morocco. Ann Entomol Soc Am 84:436–443

    Article  Google Scholar 

  • Harris KM (1994) Gall midges (Cecidomyiidae): classification and biology. In: Williams MAJ (ed) Plant galls. Oxford University Press, New York, pp 201–211

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004a) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004b) Identification of birds through DNA barcodes. PLoS Biol 2:e312

    Article  PubMed  PubMed Central  Google Scholar 

  • Hebert PD, Ratnasingham S, Zakharov EV, Telfer AC, Levesque-Beaudin V, Milton MA, Pedersen S, Jannetta P, deWaard JR (2016) Counting animal species with DNA barcodes: Canadian insects. Philos Trans R Soc Lond B Biol Sci 371:20150333. doi:10.1098/rstb.2015.0333

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson AJ, Schemerhorn BJ, Shukle RH, Weintraub PGH (2012) Biological and molecular characterization of Hessian fly (Diptera: Cecidomyiidae) from Israel. Bull Entomol Res 102:632–643

    Article  CAS  PubMed  Google Scholar 

  • Kessing B, Croom H, Martin A, McIntosh C, McMillan WO, Palumbi SP (1989) The simple fool’s guide to PCR. Version 1.0. Special publication. Honolulu, Department of Zoology, University of Hawaii

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Lhaloui S, El Bouhssini M, Naserlhaq N, Amri A, Nachit M, El Haddoury J, Jlibène M (2006) Les cécidomyies des céréales au Maroc: Biologie, dégâts et moyens de lutte. INRA, Marocco, pp 51

  • Makni H, Marrakchi M, Pasteur N (2000) Biochemical characterization of sibling species of Tunisian Mayetiola (Diptera: Cecidomyiidae). Biochem Syst Ecol 28:101–109

    Article  CAS  Google Scholar 

  • Marchal P (1897) Les cécidomyies des céréales et leurs parasites. Ann Soc Entomol Fr 66:1–105

    Google Scholar 

  • Mezghani M (2003) Etude de la phylogénie et de la variabilité génétique des populations de cécidomyies par les marqueurs moléculaires, mitochondriaux et nucléaires. Ph. D. Thesis. Université de Tunis II. Faculté des Sciences de Tunis

  • Mezghani KM, Makni H, Marrakchi M (2001) Distinction of two species of cecidomydies (Diptera: Cecidomyiidae) revealed by mitochondrial DNA genes variation. Entomol Corat 5:65–75

    Google Scholar 

  • Mezghani KM, Makni H, Pasteur N, Navajas M, Marrakchi M (2002) Species distinction and population structure in Mayetiola species (Diptera: Cecidomyiidae) based on nuclear and mitochondrial sequences. Int J Dipterol Res 13:93–107

    Google Scholar 

  • Mezghani-Khemakhem M, Markakchi M, Makni H (2005) Genetic diversity of Mayetiola destructor and Mayetiola hordei (Diptera: Cecidomyiidae) by inter-simple sequence repeats (ISSRs). Afr J Biotechnol 4:601–606

    Article  CAS  Google Scholar 

  • Miller RH, Kamel A, Lhaloui S, Elbouhssini M (1989) Survey of Hessian fly in northern Tunisia. Rachis 8:27–28

    Google Scholar 

  • Ozdil F, Ayetekin I, Ilhan F, Boztepe S (2012) Genetic variation in Turkish honeybees Apis mellifera anatoliaca, A. m. caucasica, A. m. meda (Hymenoptera: Apidae) inferred from RFLP analysis of three mtDNA regions (16S rDNA-COI-ND5). Eur J Entomol 109:161–167

    Article  CAS  Google Scholar 

  • Rach J, Desalle R, Sarkar IN, Schierwater B, Hadrys H (2008) Character-based DNA barcoding allows discrimination of genera, species and populations in Odonata. Proc Biol Sci 275:237–247

    Article  CAS  PubMed  Google Scholar 

  • Shirota Y, Iituka K, Asano J, Abe J, Yukawa J (1999) Intraspecific variations of mitochondrial cytochrome oxidase I sequence in an aphidophagous species, Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Entomol Sci 2:209–215

    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 87:651–701

    Article  CAS  Google Scholar 

  • Skuhravá M, Skuhravý V (2010) Species richness of gall midges (Diptera: Cecidomyiidae) in Europe (West Palaearctic): biogeography and coevolution with host plants. Acta Soc Zool Bohem 73:87–156

    Google Scholar 

  • Smith MA, Woodley NE, Janzen DH, Hallwachs W, Hebert PD (2006) DNA barcodes reveal cryptic host specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proc Natl Acad Sci USA 103:3657–3662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Telfer AC, Young MR, Quinn J, Perez K, Sobel CN, Sones JE, Levesque-Beaudin V, Derbyshire R, Fernandez-Triana J, Rougerie R, Thevanayagam A, Boskovic A, Borisenko AV, Cadel A, Brown A, Pages A, Castillo AH, Nicolai A, Glenn Mockford BM, Bukowski B, Wilson B, Trojahn B, Lacroix CA, Brimblecombe C, Hay C, Ho C, Steinke C, Warne CP, Garrido Cortes C, Engelking D, Wright D, Lijtmaer DA, Gascoigne D, Hernandez Martich D, Morningstar D, Neumann D, Steinke D, Marco DeBruin DD, Dobias D, Sears E, Richard E, Damstra E, Zakharov EV, Laberge F, Collins GE, Blagoev GA, Grainge G, Ansell G, Meredith G, Hogg I, McKeown J, Topan J, Bracey J, Guenther J, Sills-Gilligan J, Addesi J, Persi J, Layton KK, D’Souza K, Dorji K, Grundy K, Nghidinwa K, Ronnenberg K, Lee KM, Xie L, Lu L, Penev L, Gonzalez M, Rosati ME, Kekkonen M, Kuzmina M, Iskandar M, Mutanen M, Fatahi M, Pentinsaari M, Bauman M, Nikolova N, Ivanova NV, Jones N, Weerasuriya N, Monkhouse N, Lavinia PD, Jannetta P, Hanisch PE, McMullin RT, Ojeda Flores R, Mouttet R, Vender R, Labbee RN, Forsyth R, Lauder R, Dickson R, Kroft R, Miller SE, MacDonald S, Panthi S, Pedersen S, Sobek-Swant S, Naik S, Lipinskaya T, Eagalle T, Decaens T, Kosuth T, Braukmann T, Woodcock T, Roslin T, Zammit T, Campbell V, Dinca V, Peneva V, Hebert PD, deWaard JR (2015) Biodiversity inventories in high gear: DNA barcoding facilitates a rapid biotic survey of a temperate nature reserve. Biodivers Data J 3:E6313

    Article  Google Scholar 

  • Tian Z, Liu G, Xie J, Yin H, Luo J, Zhang L, Zhang P, Luo J (2011) Discrimination between Haemaphysalis longicornis and H. qinghaiensis based on the partial 16S rDNA and the second internal transcribed spacer (ITS-2). Exp Appl Acarol 54:165–172

    Article  PubMed  Google Scholar 

  • Tokuda M, Tabuchi K, Yukawa J, Amano H (2004) Inter- and intraspecific comparisons between Asteralobia gall midges (Diptera: Cecidomyiidae) causing axillary bud galls on Ilex species (Aquifoliaceae): Species identification, host range, and mode of speciation. Ann Entomol Soc Am 97:957–970

    Article  CAS  Google Scholar 

  • Tokuda M, Yang M, Yukawa J (2008) Taxonomy and molecular phylogeny of Daphnephila gall midges (Diptera: Cecidomyiidae) inducing complex leaf galls on Lauraceae, with descriptions of five new species associated with Machilus thunbergii in Taiwan. Zool Sci 25:533–545

    Article  CAS  PubMed  Google Scholar 

  • Yang SY, Chen MY, Yang JT (2002) Application of cecidomyiid galls to the systematic of the genus Machillus (Lauraceae) in Taiwan. Bot Bull Acad Sin 43:31–35

    CAS  Google Scholar 

  • Yang Q, Zhao S, Kučerová Z, Stejskal V, Opit G, Qin M, Cao Y, Li F, Li Z (2013) Validation of the 16S rDNA and COI DNA barcoding technique for rapid molecular identification of stored product psocids (Insecta: Psocodea: Liposcelididae). J Econ Entomol 106:419–425

    Article  CAS  PubMed  Google Scholar 

  • Yukawa J, Uechi N, Horikiri M, Tuda M (2003) Description of the soybean pod gall midge, Asphondylia yushimai sp. n. (Diptera: Cecidomyiidae), a major pest of soybean, and findings of host alternation. Bull Entomol Res 93:73–86

    Article  CAS  PubMed  Google Scholar 

  • Yukawa J, Sato S, Harris KM, Tokuda M, Sasaki M, Arkawa A, Nakada K, Sawamura N (2009) A new species of Resseliella (Diptera: Cecidomyiidae) infesting Japanese pear, Pyrus pyrifolia (Rosaceae). Appl Entomol Zool 44:655–666

    Article  CAS  Google Scholar 

  • Yukawa J, Sato S, Xu H, Tokuda M (2011) Description of a new species of the genus Resseliella (Diptera: Cecidomyiidae), a pollinator of Kadsura longipedunculata (Schisandraceae) in China, with comments on its flower-visiting habit. Entomol Sci 14:297–303

    Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Associate Professor Makoto Tokuda of the Faculty of Agriculture, Saga University, Japan for advice on primers, enzymes and methods for isolation, identification and analysis of the COI genes. We are also grateful to Wataru Ishiguro Master’s student of the Graduate School of Life and Environmental Sciences, University of Tsukuba, Japan for help with the laboratory experiments, and Professor Yooichi Kainoh and Associate Professor Seiichi Furukawa of the Faculty of Life and Environmental Sciences, University of Tsukuba, Japan, for their advice and support. This research was supported with funds for the faculty from the University of Tsukuba, Tsukuba, Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to DeMar Taylor.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cherif, A., Kinoshita, N., Taylor, D. et al. Molecular characterization and phylogenetic comparisons of three Mayetiola species (Diptera: Cecidomyiidae) infesting cereals in Tunisia. Appl Entomol Zool 52, 543–551 (2017). https://doi.org/10.1007/s13355-017-0507-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13355-017-0507-y

Keywords

Navigation