Skip to main content Accessibility help
×
Home

Patterns and drivers of genetic diversity and structure in the biological control parasitoid Habrobracon hebetor in Niger

  • M. Garba (a1), A. Loiseau (a2), C. Tatard (a2), L. Benoit (a2) and N. Gauthier (a2)...

Abstract

When a promising natural enemy of a key pest exists locally, it is a common practice in biological control (BC) to rear and release it for supplementary control in the targeted agroecosystem even though significant knowledge gaps concerning pre/post release may still exist. Incorporating genetic information into BC research fills some of these gaps. Habrobracon hebetor, a parasitoid of many economically important moths that infest stored and field crops worldwide is commonly used, particularly against the millet head miner (MHM), a key pest of millet in Sahelian countries. To advance our knowledge on how H. hebetor that occurs naturally in open-field cropping systems and grain stores as well as being mass-produced and released for MHM control, performs in millet agroecosystems in Niger we evaluated its population genetics using two mitochondrial and 21 microsatellite markers. The field samples were genetically more diverse and displayed heterozygote excess. Very few field samples had faced significant recent demographic bottlenecks. The mating system (i.e. nonrandom mating with complementary sex determination) of this species may be the major driver of these findings rather than bottlenecks caused by the small number of individuals released and the scarcity of hosts during the longlasting dry season in Niger. H. hebetor population structure was represented by several small patches and genetically distinct individuals. Gene flow occurred at local and regional scales through human-mediated and natural short-distance dispersal. These findings highlight the importance of the mating system in the genetic diversity and structure of H. hebetor populations, and contribute to our understanding of its reported efficacy against MHM in pearl millet fields.

Copyright

Corresponding author

*Author for correspondence Phone: +33 (0)499623319 Fax: +33 (0)49996245 E-mail: Nathalie.Gauthier@ird.fr

References

Hide All
Adarkwah, C., Ulrichs, C., Schaarschmidt, S., Badii, B.K., Addai, I.K., Obeng-Ofori, D. & Schöller, M. (2014) Potential of Hymenopteran larval and egg parasitoids to control stored-product beetle and moth infestation in jute bags. Bulletin of Entomological Research 104, 534542.
Adashkevich, B.P., Saidova, E. & Takanaev, A.A. (1986) Migration of Habrobracon. Zashchita rastenii 7, 3636.
Antolin, M.F. & Strand, M.R. (1992) Mating system of Bracon hebetor (Hymenoptera: Braconidae). Ecological Entomology 17, 17.
Antolin, M.F., Ode, P.J., Heimpel, G.E., O'Hara, R.B. & Strand, M.R. (2003) Population structure, mating system, and sex-determining allele diversity of the paarsitoid wasp Habrobracon hebetor. Heredity 91, 373381.
Ba, M.N., Baoua, I.B., Kaboré, A., Laouali, A., Oumarou, N., Dabire-Binso, C. & Sanon, A. (2014) Augmentative on-farm delivery methods for the parasitoid Habrobracon hebetor Say (Hymenoptera: Braconidae) to control the millet head miner Heliocheilus albipunctella (de Joannis) (Lepidoptera: Noctuidae) in Burkina Faso and Niger. Biological Control 59, 689696.
Bal, A.B. (2002) Guide d’élevage et de lâchers de Habrobracon hebetor Say (Hymenoptèra Braconidae) parasitoïde de la chenille mineuse de l’épi de mil et de son hôte de substitution Corcyra cephalonica (Stainton) Lepidoptera pyralidae. 15p.
Baoua, I.B., Ba, M.N., Amadou, L., Kaboré, A. & Dabire-Binso, C.L. (2018) Field dispersal of the parasitic wasp Habrobracon hebetor (Hymenoptera: Braconidae) following augmentative release against the millet head miner Heliocheilus albipunctella (Lepidoptera; Noctuidae) in the Sahel. Biocontrol Science and Technology 28, 404415.
Behura, S.K. (2006) Molecular marker systems in insects: current trends and future avenues. Molecular Ecology 15, 30873113.
Calvo, F.J., Bolckmans, K. & Belda, J.E. (2012) Biological control based IPM in sweet pepper greenhouses using Amblyseius swirskii (Acari: Phytoseiidae). Biocontrol Science and Technology 22, 13981416.
Chapuis, M. & Estoup, A. (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology & Evolution 24, 621631.
Chen, H., Zhang, H., Zhu, K.Y. & Throne, J.E. (2012) Induction of reproductive diapause in Habrobracon hebetor (Hymenoptera: Braconidae) when reared at different photoperiods at low temperatures. Environmental Entomology 41, 697705.
Chomphukhiao, N., Takano, S., Takasu, K. & Uraichuen, S. (2018) Existence of two strains of Habrobracon hebetor (Hymenoptera: Braconidae): a complex in Thailand and Japan. Applied Entomology and Zoology 53, 373380.
Cock, M.J.W., van Lenteren, J.C., Brodeur, J., Barratt, B.I.P., Bigler, F., Bolckmans, K., Cônsoli, F.L., Haas, F., Mason, P.G. & Parra, J.R.P. (2010) Do new access and benefit sharing procedures under the convention on biological diversity threaten the future of biological control? Biological Control 55, 199218.
Cornuet, J.M. & Luikart, G. (1996) Description and Power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 20012014.
Cowan, D.P. & Stahlhut, J.K. (2004) Functionally reproductive diploid and haploid males in an inbreeding hymenopteran with complementary sex determination. Proceedings of the National Academy of Sciences of the United States of America 101, 1037410379.
Dowton, M., Austin, A.D. & Antolin, M.F. (1998) Evolutionary relationships among the Braconidae (Hymenoptera: Ichneumonoidea) inferred from partial 16S rDNA gene sequences. Insect Molecular Biology 7, 129150.
Earl, D.A. & vonHoldt, B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359361.
Elias, J., Mazzi, D. & Dorn, S. (2009) No need to discriminate? Reproductive diploid males in a parasitoid with complementary sex determination. PloS One 4, e6024.
Eliopoulos, P.A. & Stathas, G.J. (2008) Life tables of Habrobracon hebetor (Hymenoptera: Braconidae) parasitizing Anagasta kuehniella and Plodia interpunctella (Lepidoptera: Pyralidae): effect of host density. Journal of Economical Entomology 101, 982988.
Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of cluster of individuals using the software structure: a simulation study. Molecular Ecology 14, 26112620.
Follett, P.A., Calvert, F. & Golden, M. (2014) Genetic studies using the orange body color type of Nezara viridula (Hemiptera: Pentatomidae): inheritance, sperm precedence, and disassortative mating. Annals of the Entomological Society of America 100, 433438.
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. Molecular Marine Biology Biotechnology 3, 294299.
Gahukar, R.T., Guèvremont, H., Bhatnagar, V.S., Doumbia, Y.O., Ndoye, M. & Pierrard, G. (1986) A review of the pest status of the millet spike worm, Raghuva albipunctella De Joannis (Noctuidae: Lepidoptera) and its management in the Sahel. International Journal of Tropical Insect Science 7, 457463.
Garba, M., Loiseau, A., Benoit, L. & Gauthier, N. (2016) A new suite of twenty-two polymorphic microsatellite loci in the parasitic wasp, Habrobracon hebetor (Hymenoptera: Braconidae): promising molecular tools for studying the population genetics of several beneficial braconid species. European Journal of Entomology 113, 265269.
Gariepy, T.D., Kuhlmann, U., Gillott, C. & Erlandson, M. (2007) Parasitoids, predators and PCR: the use of diagnostic molecular markers in biological controls of Arthropods. Journal of Applied Entomology 131, 225240.
Gaskin, J.F., Bon, M.C., Cock, M.J., Cristofaro, M., De Biase, A., De Clerck-Floate, R., Ellison, C.A., Hinz, H.L., Hufbauer, R.A. & Julien, M.H. (2011) Applying molecular-based approaches to classical biological control of weeds. Biological Control 58, 121.
Ghimire, M.N. & Philipps, T.W. (2014) Oviposition and reproductive performance of Habrobracon hebetor (Hymenoptera: Braconidae) on six different pyralid host species. Annals of Entomological Society of America 107, 809817.
Greenspoon, P.B. & M'Gonigle, L.K. (2014) Host-parasite interactions and the evolution of nonrandom mating. Evolution 68, 35703580.
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.
Gurr, G.M. & Wratten, S.D. (2000) Measures of Success in Biological Control. Dordrecht, Kluwer Academic Publishers.
Hagler, J.R. & Jackson, C.G. (2001) Methods for marking insects: current techniques and future prospects. Annual Review of Entomology 46, 511543.
Heimpel, G.E. & Asplen, M.K. (2011) A « Goldilocks » hypothesis for dispersal of biological control agents. BioControl 56, 441450.
Heimpel, G.E. & de Boer, J.G. (2008) Sex determination in the Hymenoptera. Annual Review of Entomology 53, 209230.
Heimpel, G.E., Antolin, M.F., Franqui, R.A. & Strand, M.R. (1997) Reproductive isolation and genetic variation between two « strains » of Bracon hebetor (Hymenoptera: Braconidae). Biological Control 9, 149156.
Holman, L., van Zweden, J.S., Linksvayer, T.A. & d'Ettore, P. (2013) Crozier's paradox revisited: maintenance of genetic recognition systems by disassortative mating. BMC Evolutionary Biology 13, 211225.
Hubisz, M., Falush, D., Stephens, M. & Pritchard, J.K. (2009) Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9, 13221332.
Jiang, Y., Bolnick, D.I. & Kirkpatrick, M. (2013) Assortative mating in animals. The American Naturalist 191, E125E138.
Kaboré, A., Ba, N.M., Ba, , Dabire-Binso, C.I. & Sanon, A. (2017) Field persistence of Habrobracon hebetor (Say) (Hymenoptera: braconidae) following augmentative releases against the millet head miner, Heliocheilus albipunctella (de Joannis) (Lepidoptera: Noctuidae), in the Sahel. Biological Control 108, 6469.
Lavandero, B., Wratten, S., Hagler, J. & Jervis, M. (2004) The need for effective marking and tracking techniques for monitoring the movements of insect predators and parasitoids. International Journal of Pest Management 50, 147151.
Lefort, V., Longueville, J.E. & Gascuel, O. (2017) SMS: smart model selection in PhyML. Molecular Biology and Evolution 34, 24222424.
Li, W., Cowley, A., Uludag, M., Gur, T., McWilliam, H., Squizzato, S., Park, Y.M., Buso, N. & Lopez, R. (2015) The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Research 43, W580W584.
Magro, S.R. & Parra, J.R.P. (2001) Biology of the ectoparasitoid Bracon hebetor Say. 1857 (Hymenoptera: Braconidae) on seven Lepidopteran species. Scientia Agricola 58, 693698.
Manishkumar, D.R., Dhirubhai, K.M. & Piyushbhai, V.R. (2013) Reproductive parameters of Bracon hebetor Say on seven different hosts. African Journal of Agricultural Research 8, 32513254.
Mardulyn, P. & Whitfield, J.B. (1999) Phylogenetic signal in the COI, 16S, and 28S genes for inferring among genera of microgastrinae (Hymenoptera; Braconidae): evidence of a high diversification in this group of parasitoids. Molecular Phylogenetics and Evolution 12, 282294.
Moffat, C.E. & Smith, M.A. (2015) Pre-release detection of a biocontrol agent: combining independent and public DNA sequences to identify the first North American record of Aulacidea pilosellae (Hymenoptera: Cynipidae). The Canadian Entomologist 147, 390395.
Nwanze, K.F. & Harris, K.M. (1992) Insect pests of pearl millet in West Africa. Review of Agricultural Entomology 80, 11331155.
Nwanze, K.F. & Sivakumar, M.V.K. (1990) Insect pests of pearl millet in Sahelian West Africa _ II Rhaguva albipunctella De Joannis (Noctuidae, Lepidoptera): Distribution, population dynamics and assessment of crop damage. Tropical Pest Management 36, 5965.
Oleke, J.M., Manyong, V. & Mignouna, D. (2013) Ex-ante analysis of biological control of coconut mite in Benin. AgBioForum 16, 161169.
Papp, J. (2012) A revision of the Bracon fabricius species in Wesmael's collection deposited in Brussels (Hymenoptera: Braconidae: Braconinae). European Journal of Taxonomy 21, 1154.
Payne, W., Tapsoba, H., Baoua, I.B., Ba, N.M., N'Diaye, M. & Dabiré-Binso, C. (2011) On-farm biological control of the pearl millet head miner: realization of 35 years of unsteady progress in Mali, Burkina faso and Niger. International Journal of Agricultural Sustainability 9, 186193.
Peakall, R. & Smouse, P.E. (2012) Genalex 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics (Oxford, England) 28, 25372539.
Piry, S., Luikart, G. & Cornuet, J.M. (1999) BOTTLENECK: a program for detecting recent effective population size reductions from allele frequency data. Journal of Heredity 90, 502503.
Pomari-Fernandes, A., de Freitas Bueno, A., de Dortoli, S.A. & Favetti, B.M. (2018) Dispersal capacity of the egg parasitoid Telenomus remus Nixon (Hymenoptera: Platygastridae) in maize and soybean crops. Biological Control 126, 158168.
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945959.
Puttarudriah, M. & Channa Basavanna, G.P. (1956) A study on the identity of Bracon hebetor Say and Bracon brevicornis Wesmael (Hymenoptera: Braconidae). Bulletin of Entomological Research 47, 183191.
Rauth, S.J., Linz, H.L., Gerber, E. & Hufbauer, R.A. (2011) The benefits of pre-release population genetics: a case study using Ceutorhynchus scrobicollis, a candidate agent of garlic mustard, Alliaria petiolata. Biological Control 56, 6776.
Raymond, M. & Rousset, F. (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248249.
Rolán-Alvarez, E., Saura, M., Diz, A.P., Rivas, M.J., Alvarez, M., Cortés, B., de Coo, A., Estévez, D. & Iglesias, L. (2012) Can sexual selection and disassortative mating contribute to the maintenance of a shell color polymorphism in an intertidal marine snail? Current Zoology 58, 463474.
Rozas, J., Sanchez-Delbarrio, J.C., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics (Oxford, England) 19, 24962497.
Rukhsana, K. & Sebastian, C.D. (2015) Genetic structure and molecular phylogeny analysis of Bracon brevicornis Wesmael, a larval parasitoid of coconut black headed caterpillar, Opsinia arenosella Walker. Research in Biotechnology 6, 1723.
Sow, A., Brévault, T., Delvare, G., Haran, J., Benoit, L., Cœur d'Acier, A., Galan, M., Thiaw, C., Soti, V. & Sembène, M. (2018) DNA sequencing to help identify crop pests and their natural enemies in agro-ecosystems: the case of the millet head miner Heliocheilus albipunctella (Lepidoptera: Noctuidae) in sub-Saharan Africa. Biological Control 121, 199207.
Streito, J.C., Clouet, C., Hamdi, F. & Gauthier, N. (2017) Population genetic structure of Macrolophus pygmaeus in Mediterranean agroecosystems. Insect Science 24, 859876.
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595.
Tien, N.S.H., Massourakis, G., Sabelis, M.W. & Egas, M. (2011) Mate choice promotes inbreeding avoidance in the two-spotted spider mite. Experimental and Applied Acarology 54, 119124.
Van Lenteren, J.C., Bolckmans, K., Köhl, J., Ravensberg, W.J. & Urbaneja, A. (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. Biological Control 63, 3959.
Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. (2004) Microchecker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535538.
Van Wilgenburg, E., Driessen, G. & Beukeboom, L.W. (2006) Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Frontiers in Zoology 3, 1.
Vorsino, A., Wieczorek, A., Wright, M. & Messing, R. (2012) Using evolutionary tools to facilitate the prediction and prevention of host-based differentiation in biological control: a review and perspective. Annals of Applied Biology 160, 204216.
Wang, Z.Y., He, K.L., Zhang, F., Lu, X. & Babendreier, D. (2014) Mass rearing and release of Trichogramma for biological control of insect pests of corn in China. Biological Control 68, 136144.
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38, 13581370.

Keywords

Type Description Title
WORD
Supplementary materials

Garba et al. supplementary material
Tables S1-S6 and Figure S1

 Word (222 KB)
222 KB

Patterns and drivers of genetic diversity and structure in the biological control parasitoid Habrobracon hebetor in Niger

  • M. Garba (a1), A. Loiseau (a2), C. Tatard (a2), L. Benoit (a2) and N. Gauthier (a2)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed