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Efficacy of using DNA barcoding to identify parasitoid wasps of the melon-cotton aphid (Aphis gossypii) in watermelon cropping system

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Abstract

Parasitoid wasps have received a great deal of attention in the biological control of melon-cotton aphid (Aphis gossypii Glover). The species of parasitoids are often difficult to identify because of their small body size and profound diversity. DNA barcoding offers scientists who are not expert taxonomists a powerful tool to render their field studies more accurate. Using DNA barcodes to identify aphid parasitoid wasps in specific cropping systems may provide valuable information for biological control. Here, we report the use of DNA barcoding to confirm the morphological identification of 14 species (belonging to 13 genera of 7 families) of parasitoid wasps from two-year field samples in a watermelon cropping system. We generated DNA sequences from the mitochondrial COI gene and the nuclear D2 region of 28S rDNA to assess the genetic variation within and between parasitoid species. Automatic Barcode Gap Discovery (ABGD) supported the presence of 14 genetically distinct groups in the dataset. Among the COI sequences, we found no overlap between the maximum K2P distance within species (0.49%) and minimum distance between species (6.85%). The 28S sequences also showed greater interspecific distance than intraspecific distance. DNA barcoding confirmed the morphological identification. However, inconsistency and ambiguity of taxonomic information available in the online databases has limited the successful use of DNA barcoding. Only five species matched those in the BOLD and GenBank. Four species did not match the entries in GenBank and five species showed ambiguous results in BOLD due to confusing nomenclature. We suggested that species identification based on DNA barcodes should be performed using both COI and other genes. Nonetheless, we demonstrate the potential of the DNA barcoding approach to confirm field identifications and to provide a foundation for studies aimed at improving the understanding of the biocontrol services provided by parasitoids in the melon ecosystem.

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References

  • Andrews FG (1978) Taxonomy and host specificity of Nearctic Alloxystinae with a catalog of the world species (Hymenoptera: Cynipidae). State Calif Dep Food Agric Occas Pap Entomol 25:1–128

    Google Scholar 

  • Askew RR (1971) Parasitic insects. Heinemann Educational Bks, London

    Google Scholar 

  • Beijing Municipal Bureau of Statistics (2016) Beijing statistical yearbook. China Statistic Press, Beijing

    Google Scholar 

  • Bernardo U, Pedata PA, Viggiani G (2006) Life history of Pnigalio soemius (Walker) (Hymenoptera: Eulophidae) and its impact on a leafminer host through parasitization, destructive host-feeding and host-stinging behavior. Biol Control 37:98–107

    Article  Google Scholar 

  • Blackman RL, Eastop VF (2007) Taxonomic issues. In: van Emden H, Harringtons RV (eds) Aphids as crop pests. CAB International, London, pp 1–29

    Google Scholar 

  • Campbell B, Steffen-Campbell J, Werren J (1994) Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer (ITS2) and 28S rDNA sequences. Insect Mol Biol 2:225–237

    Article  Google Scholar 

  • Cerutti-Pereyra F, Meekan MG, Wei NWV, O’Shea O, Bradshaw CJA, Austin CM (2012) Identification of rays through DNA barcoding: an application for ecologists. PLoS ONE 7(6):e36479

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Derocles SAP, Le Ralec A, Plantegenest M, Chaubet B, Cruaud C, Cruaud A, Rasplus J-Y (2012) Identification of molecular markers for DNA barcoding in the Aphidiinae (Hym. Braconidae). Mol Ecol Resour 12:197–208

    Article  PubMed  CAS  Google Scholar 

  • Evans DM, Kitson JJN, Lunt DH, Straw NA, Pocock MJO (2016) Merging DNA metabarcoding and ecological network analysis to understand and build resilient terrestrial ecosystems. Funct Ecol 30:1904–1916

    Article  Google Scholar 

  • 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 Biotechnol 3:294–299

    PubMed  CAS  Google Scholar 

  • Frank SD (2010) Biological control of arthropod pests using banker plant systems: past progress and future directions. Biol Control 52:8–16

    Article  Google Scholar 

  • Frézal L, Leblois R (2008) Four years of DNA barcoding: current advances and prospects. Infect Genet Evol 8:727–736

    Article  PubMed  CAS  Google Scholar 

  • Fueloep D, Miko I, Seltmann K, Penzes Z, Melika G (2013) The description of Alloxysta chinensis, a new Charipinae species from China (Hymenoptera, Figitidae). Zootaxa 3637:394–400

    Article  Google Scholar 

  • Gariepy TD, Haye T, Zhang J (2014) A molecular diagnostic tool for the preliminary assessment of host-parasitoid associations in biological control programmes for a new invasive pest. Mol Ecol 23:3912–3924

    Article  PubMed  CAS  Google Scholar 

  • Gillespie JJ, Munro JB, Heraty JM, Yoder MJ, Owen AK, Carmichael AE (2005) A secondary structural model of the 28S rRNA expansion segments D2 and D3 for chalcidoid wasps (Hymenoptera: Chalcidoidea). Mol Biol Evol 22:1593–1608

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Marco F, Urbaneja A, Tena A (2016) A sown grass cover enriched with wild forb plants improves the biological control of aphids in citrus. Basic Appl Ecol 17:210–219

    Article  Google Scholar 

  • Hayat M, Fatima K (1992) Taxonomic studies on Aphelinus (Hymenoptera: Aphelinidae). 5. Description of a new species and further records from A. gossypii with a new synonymy. Entomon 17:103–107

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Heraty JM, Woolley JB, Hopper KR, Hawks DL, Kim JW, Buffington M (2007) Molecular phylogenetics and reproductive incompatibility in a complex of cryptic species of aphid parasitoids. Mol Phylogenet Evol 45:480–493

    Article  PubMed  CAS  Google Scholar 

  • Heraty J, Ronquist F, Carpenter JM, Hawks D, Schulmeister S, Dowling AP, Murray D, Munro J, Wheeler WC, Schiff N, Sharkey M (2011) Evolution of the hymenopteran megaradiation. Mol Phylogenet Evol 60:73–88

    Article  PubMed  Google Scholar 

  • Jacobson RJ, Croft P (1998) Strategies for the control of Aphis gossypii Glover (Hom.: Aphididae) with Aphidius colemani Viereck (Hym.: Braconidae) in protected cucumbers. Biocontrol Sci Techn 8:377–387

    Article  Google Scholar 

  • Jinbo U, Kato T, Ito M (2011) Current progress in DNA barcoding and future implications for entomology. Entomol Sci 14:107–124

    Article  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Kos K, Petrović A, Starý P, Kavallieratos NG, Ivanović A, Toševski I, Jakše J, Trdan S, Tomanović Ž (2011) On the identity of cereal aphid parasitoid wasps Aphidius uzbekistanicus, Aphidius rhopalosiphi, and Aphidius avenaphis (Hymenoptera: Braconidae: Aphidiinae) by examination of COI mitochondrial gene, geometric morphometrics, and morphology. Ann Entomol Soc Am 104:1221–1232

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Luo Z, Gan G (1986) Population dynamics of cotton aphids on cotton during square-boll stage and the relation between population age structure and parasitization. Acta Entomologica Sinica 29(1):56–61 (in Chinese)

    Google Scholar 

  • Luo A, Lan H, Ling C, Zhang A, Shi L, Ho SYW, Zhu C (2015) A simulation study of sample size for DNA barcoding. Ecol Evol 5:5869–5879

    Article  PubMed  PubMed Central  Google Scholar 

  • Neuville S, Le Ralec A, Outreman Y, Jaloux B (2016) The delay in arrival of the parasitoid Diaeretiella rapae influences the efficiency of cabbage aphid biological control. BioControl 61:115–126

    Article  Google Scholar 

  • Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol 21:1864–1877

    Article  PubMed  CAS  Google Scholar 

  • Ramsden M, Menendez R, Leather S, Wackers F (2017) Do natural enemies really make a difference? Field scale impacts of parasitoid wasps and hoverfly larvae on cereal aphid populations. Agr Forest Entomol 19:139–145

    Article  Google Scholar 

  • Sharkey MJ, Carpenter JM, Vilhelmsen L, Heraty J, Liljeblad J, Dowling AP, Schulmeister S, Murray D, Deans AR, Ronquist F (2012) Phylogenetic relationships among superfamilies of Hymenoptera. Cladistics 28:80–112

    Article  PubMed  Google Scholar 

  • Shaw M, Huddleston T (1991) Classification and biology of braconid wasps. In: Dolling WR, Askew RR (eds) Handbooks for the identification of British insects. British Museum, London 7(11):1–126

  • Stahlhut JK, Fernandez-Triana J, Adamowicz SJ, Buck M, Goulet H, Hebert PDN, Huber JT, Merilo MT, Sheffield CS, Woodcock T, Smith MA (2013) DNA barcoding reveals diversity of Hymenoptera and the dominance of parasitoids in a sub-arctic environment. BMC Ecol 13:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Starý P, Schlinger EI (1967) A revision of the Far East Asian Aphidiidae (Hymenoptera). Springer, New York

    Book  Google Scholar 

  • Tatsumi E, Takada H (2005) Evaluation of Aphelinus asychis and A. albipodus (Hymenoptera: Aphelinidae) as biological control agents against three pest aphids. Appl Entomol Zool 40:379–385

    Article  Google Scholar 

  • Tian L, Yang L, Gao S (1981) A preliminary study on aphid parasites in cotton fields (Hymenoptera: Aphidiidae). Insect Knowl 18:158–160 (in Chinese)

    Google Scholar 

  • Valentini A, Pompanon F, Taberlet P (2009) DNA barcoding for ecologists. Trends Ecol Evol 24:110–117

    Article  PubMed  Google Scholar 

  • Wu ZS, Hopper KR, O’Neil RJ, Voegtlin DJ, Prokrym DR, Heimpel GE (2004) Reproductive compatibility and genetic variation between two strains of Aphelinus albipodus (Hymenoptera: Aphelinidae), a parasitoid of the soybean aphid, Aphis glycines (Homoptera: Aphididae). Biol Control 31:311–319

    Article  CAS  Google Scholar 

  • Xi X, Zhu Z (1984) Preliminary studies on aphid parasites in Jiangsu Province. Nat Enem Insects 6:49–52 (in Chinese)

    Google Scholar 

  • Yang F, Wu YK, Xu L, Wang Q, Yao ZW, Zikic V, Tomanovic Z, Ferrer-Suay M, Selfa J, Pujade-Villar J, Lu YH, Guo YY (2017) Species composition and richness of aphid parasitoid wasps in cotton fields in northern China. Sci Rep 7:9799

    Article  PubMed  PubMed Central  Google Scholar 

  • Ye ZP, Vollhardt IMG, Tomanovic Z, Traugott M (2017) Evaluation of three molecular markers for identification of European primary parasitoids of cereal aphids and their hyperparasitoids. PLoS ONE 12(5):e0177376

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zamani AA, Talebi A, Fathipour Y, Baniameri V (2007) Effect of temperature on life history of Aphidius colemani and Aphidius matricariae (Hymenoptera: Braconidae), two parasitoids of Aphis gossypii and Myzus persicae (Homoptera: Aphididae). Environ Entomol 36:263–271

    Article  PubMed  Google Scholar 

  • Zhang Y-Z, S-l Si, Zheng J-T, Li H-L, Fang Y, Zhu C-D, Vogler AP (2011) DNA barcoding of endoparasitoid wasps in the genus Anicetus reveals high levels of host specificity (Hymenoptera: Encyrtidae). Biol Control 58:182–191

    Article  Google Scholar 

  • Zhou QS, Xi YQ, Yu F, Zhang X, Li XJ, Liu CL, Niu ZQ, Zhu CD, Qiao GX, Zhang YZ (2014) Application of DNA barcoding to the identification of Hymenoptera parasitoids from the soybean aphid (Aphis glycines) in China. Insect Sci 21:363–373

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We would like to thank Yifan Li, Yuansheng Li, and Baofeng Mu for providing assistance with sampling and DNA extraction and the farmers for allowing us to collect aphids from their fields. We also thank Dr. Xu Zhang (Institute of Zoology, Chinese Academy of Sciences) for assistance in parasitoid identification. This study was supported by National Key R&D Program of China (2017YFD0200300), National Natural Science Foundation of China (No. 31501646) and Scientific Research Project of Beijing Municipal Education Commission (KM201710020006).

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  1. Zhaoke Dong and Shuang Liu have contributed equally to this work.

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  1. Beijing Key Laboratory of New Technology in Agricultural Application, National Demonstration Center for Experimental Plant Production Education, Beijing University of Agriculture, Beijing, 102206, China

    Zhaoke Dong, Shuang Liu & Zhiyong Zhang

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  1. Zhaoke Dong
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Correspondence to Zhiyong Zhang.

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Dong, Z., Liu, S. & Zhang, Z. Efficacy of using DNA barcoding to identify parasitoid wasps of the melon-cotton aphid (Aphis gossypii) in watermelon cropping system. BioControl 63, 677–685 (2018). https://doi.org/10.1007/s10526-018-9894-4

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