Skip to main content
Log in

Moroccan specimens of Microctonus aethiopoides spice our understanding of genetic variation in this internationally important braconid parasitoid of adult weevils

BioControl Aims and scope Submit manuscript

Cite this article


Microctonus aethiopoides Loan (Hymenoptera: Braconidae) was introduced from Morocco to Australia and New Zealand for biological control of the lucerne pest, Sitona discoideus. Previous research has indicated that M. aethiopoides intraspecific genetic variation is more strongly associated with weevil host species than geographic origin. Cytochrome c oxidase subunit 1 (COI) sequences from parasitoids dissected from weevils collected during a survey of lucerne-growing areas in Morocco allowed us to further test this hypothesis. As found previously, there were two strong clades in M. aethiopoides with no geographical basis to this structure. Earlier research suggested that intraspecific variability within M. aethiopoides was related to weevil host genus (Sitona vs. Hypera), and the analysis confirmed that one of the clades corresponded strongly with the host Sitona discoideus. The other clade, however, previously characterised by parasitoids from Hypera postica also included parasitoids dissected from Charagmus spp., which is a sister genus to Sitona. It is suggested that food plant associations of the host weevils might have had an influence on the evolutionary history of the parasitoid.

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


  • Aeschlimann J-P (1983) Sources of importation, establishment and spread in Australia of Microctonus aethiopoides Loan (Hymenoptera: Braconidae), a parasitoid of Sitona discoideus Gyllenhal (Coleoptera: Curculionidae). J Aust Entomol Soc 22:325–331

    Article  Google Scholar 

  • Aeschlimann J-P (1995) Lessons from post-release investigations in classical biological control: the case of Microctonus aethiopoides Loan (Hym., Braconidae) introduced into Australia and New Zealand for the biological control of Sitona discoideus Gyllenhal (Col., Curculionidae). In: Lynch JM (ed) Biological control: benefits and risks. Cambridge University, New York, USA, pp 75–83

  • Avise JC (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, UK

  • Barlow ND, Goldson SL (1993) A modelling analysis of the successful biological control of Sitona discoideus (Coleoptera: Curculionidae) by Microctonus aethiopoides (Hymenoptera: Braconidae) in New Zealand. J Appl Ecol 30:165–179

    Article  Google Scholar 

  • Barratt BIP (2004) Microctonus parasitoids and New Zealand weevils: comparing laboratory estimates of host ranges to realized host ranges. In: van Driesche RG, Reardon R (eds) Assessing Host Ranges for Parasitoids and Predators Used for Classical Biological Control: A Guide to Best Practice. USDA Forest Service, Morgantown, USA, pp 103–120

  • Barratt BIP, Evans AA, Ferguson CM, Barker G, McNeill MR, Phillips CB (1997) Laboratory nontarget host range of the introduced parasitoids Microctonus aethiopoides and M. hyperodae (Hymenoptera: Braconidae) compared with field parasitism in New Zealand. Environ Entomol 26:694–702

    Google Scholar 

  • Barratt BIP, Blossey B, Hokkanen HMT (2006) Post-release evaluation of non-target effects of biological control agents. In: Kuhlmann U, Bigler F, Babendreier D (eds) Environmental Impact of Arthropod Biological Control: Methods and Risk Assessment. CABI Bioscience, Wallingford, UK, pp 166–186

    Chapter  Google Scholar 

  • Barratt BIP, Ferguson CM, Bixley AS, Crook KE, Barton DM, Johnstone PD (2007) Field parasitism of nontarget weevil species (Coleoptera: Curculionidae) by the introduced biological control agent Microctonus aethiopoides Loan (Hymenoptera: Braconidae) over an altitude gradient. Environ Entomol 36:826–839

    Article  PubMed  CAS  Google Scholar 

  • Barratt BIP, Oberprieler RG, Barton DM, Mouna M, Stevens M, Alonzo-Zarazaga M, Vink CJ, Ferguson CM (2012) Could native range research, and non-target host range in Australia have helped predict host range of Microctonus aethiopoides Loan (Hymenoptera: Braconidae), a biological control agent for Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) in New Zealand? BioControl (in press)

  • Brandley MC, Schmitz A, Reeder TW (2005) Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Syst Biol 54:373–390

    Article  PubMed  Google Scholar 

  • Brower AVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA 91:6491–6495

    Article  PubMed  CAS  Google Scholar 

  • Cullen JM, Hopkins DC (1982) Rearing, release and recovery of Microctonus aethiopoides Loan (Hymenoptera: Braconidae) imported for the control of Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) in south eastern Australia. J Aust Entomol Soc 21:279–284

    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 Biotech 3:294–299

    CAS  Google Scholar 

  • Gerard PJ, Eden TM, Hardwick S, Mercer CF, Slay MWA, Wilson DJ (2007) Initial establishment of the Irish strain of Microctonus aethiopoides in New Zealand. N Z Plant Prot 60:203–208

    Google Scholar 

  • Gerard PJ, Wilson DJ, Eden TM (2011) Field release, establishment and initial dispersal of Irish Microctonus aethiopoides in Sitona lepidus populations in northern New Zealand pastures. BioControl 56:861–870

    Article  Google Scholar 

  • Hasegawa M, Kishino K, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Hufbauer RA, Roderick GK (2005) Microevolution in biological control: Mechanisms, patterns, and processes. Biol Control 35:227–239

    Article  Google Scholar 

  • Hundsdoerfer AK, Rheinheimer J, Wink M (2009) Towards the phylogeny of the Curculionoidea (Coleoptera): Reconstructions from mitochondrial and nuclear ribosomal DNA sequences. Zool Anz 248:9–31

    Article  Google Scholar 

  • Kean JM, Barlow ND (2001) A spatial model for the successful biological control of Sitona discoideus by Microctonus aethiopoides. J Appl Ecol 38:162–169

    Article  Google Scholar 

  • Lanave C, Preparata G, Sacone C, Serio G (1984) A new method for calculating evolutionary substitution rates. J Mol Evol 20:86–93

    Article  PubMed  CAS  Google Scholar 

  • Loan CC (1975) A review of Haliday species of Microctonus, a neotype designation for M. aethiops, and a description of M. aethiopoides n. sp. (Hymenoptera: Braconidae, Euphorinae). Entomophaga 20:31–41

    Article  Google Scholar 

  • Loan C, Holdaway FG (1961) Microctonus aethiops (Nees) auctt. and Perilitus rutilus (Nees) (Hymenoptera: Braconidae), European parasites of Sitona weevils (Coleoptera: Curculionidae). Can Entomol 93:1057–1078

    Article  Google Scholar 

  • Lozier JD, Roderick GK, Mills NJ (2008) Evolutionarily significant units in natural enemies: Identifying regional populations of Aphidius transcaspicus (Hymenoptera: Braconidae) for use in biological control of mealy plum aphid. Biol Control 46:532–541

    Article  Google Scholar 

  • Lozier JD, Roderick GK, Mills NJ (2009) Molecular markers reveal strong geographic, but not host associated, genetic differentiation in Aphidius transcaspicus, a parasitoid of the aphid genus Hyalopterus. Bull Entomol Res 99:83–96

    Article  PubMed  CAS  Google Scholar 

  • McKenna DD, Sequeira AS, Marvaldi AE, Farrell BD (2009) Temporal lags and overlap in the diversification of weevils and flowering plants. Proc Natl Acad Sci USA 106:7083–7088

    Article  PubMed  CAS  Google Scholar 

  • Morris MG (2002) True Weevils (Part I) Coleoptera: Curculionidae (Subfamilies Raymondionyminae to Smicronychinae). Royal Entomological Society and the Field Studies Council, Dorchester, UK, 149 pp

  • Nylander JAA (2008) MrModeltest 2.3. Department of Systematic Zoology, Uppsala University, Uppsala, Sweden

  • Page RDM (1996) TREEVIEW: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Phillips CB, Iline II, Vink CJ, Winder LM, McNeill MR (2006) Methods to distinguish between the Microctonus aethiopoides strains that parasitise Sitona lepidus and Sitona discoideus. N Z Plant Prot 59:297–303

    Google Scholar 

  • Phillips CB, McNeill MR, Hardwick S, Vink CJ, Kean JM, Bewsell D, Ferguson CM, Winder LM, Iline II, Barron MC, Stuart B (2007) Clover root weevil in the South Island: detection, response and current distribution. N Z Plant Prot 60:209–216

    Google Scholar 

  • Phillips CB, Baird DB, Iline II, McNeill MR, Proffitt JR, Goldson SL, Kean JM (2008a) East meets West: Adaptive evolution of an insect introduced for biological control. J Appl Ecol 45:948–956

    Article  Google Scholar 

  • Phillips CB, Vink CJ, Blanchet A, Hoelmer KA (2008b) Hosts are more important than destinations: What genetic variation in Microctonus aethiopoides (Hymenoptera: Braconidae) means for foreign exploration for natural enemies. Mol Phylogenet Evol 49:467–476

    Article  PubMed  Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike Information Criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Shaw SR (1988) Euphorine phylogeny: the evolution of diversity in host-utilization by parasitoid wasps (Hymenoptera: Braconidae). Ecol Entomol 13:323–335

    Article  Google Scholar 

  • Stufkens MAW, Farrell JA, Goldson SL (1987) Establishment of Microctonus aethiopoides, a parasitoid of the Sitona weevil in New Zealand. In: Popay AJ (ed) Proceedings of the 40th New Zealand Weed Pest Control Conference, Nelson, New Zealand, pp 31–32

  • Sundaralingam S, Hower AA, Kim KC (2001) Host selection and reproductive success of French and Moroccan populations of the parasitoid, Microctonus aethiopoides (Hymenoptera: Braconidae). BioControl 46:25–41

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates, Sunderland, UK

  • Tavaré S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. Lect Math Life Sci 17:57–86

    Google Scholar 

  • Velázquez de Castro AJ, Alonso-Zarazaga MÁ, Outerelo R (2007) Systematics of Sitonini (Coleoptera: Curculionidae: Entiminae), with a hypothesis on the evolution of feeding habits. Syst Ent 32:312–331

    Article  Google Scholar 

  • Vink CJ, Phillips CB, Mitchell AD, Winder LM, Cane RP (2003) Genetic variation in Microctonus aethiopoides (Hymenoptera: Braconidae). Biol Control 28:251–264

    Article  CAS  Google Scholar 

  • Winder LM, Phillips CB, Lenney-Williams C, Cane RP, Paterson K, Vink CJ, Goldson SL (2005) Microsatellites and 16S sequences corroborate phenotypic evidence of trans-Andean variation in the parasitoid Microctonus hyperodae (Hymenoptera: Braconidae). Bull Entomol Res 95:289–298

    PubMed  CAS  Google Scholar 

  • Wojciechowski MF, Sanderson MJ, Steele KP, Liston A (2000) Molecular phylogeny of the “temperate herbaceous tribes” of papilionoid legumes: a supertree approach. In: Herendeen PS, Bruneau A (eds) Adv Legume Syst. Royal Botanic Gardens, Kew, UK, pp 277–298

  • Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39:306–314

    Article  PubMed  CAS  Google Scholar 

Download references


We thank Prof. Mohammed Mouna and Mataame Abderrahmane (Institute Scientifique, Rabat, Morocco) for coordinating the Moroccan weevil collections, and carrying out the collections, respectively. CJV and CBP were funded by New Zealand’s Foundation for Research, Science and Technology through contract LINX0304, Ecosystems Bioprotection. BIPB and DMB were funded by New Zealand’s Foundation for Research, Science and Technology through contract CO2X0501, Better Border Biosecurity (

Author information

Authors and Affiliations


Corresponding author

Correspondence to Cor J. Vink.

Additional information

Handling Editor: Torsten Meiners

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Vink, C.J., Barratt, B.I.P., Phillips, C.B. et al. Moroccan specimens of Microctonus aethiopoides spice our understanding of genetic variation in this internationally important braconid parasitoid of adult weevils. BioControl 57, 751–758 (2012).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: