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Apomictic parthenogenesis in a parasitoid wasp Meteorus pulchricornis, uncommon in the haplodiploid order Hymenoptera

Published online by Cambridge University Press:  13 February 2014

Y. Tsutsui
Affiliation:
Graduate School of Agricultural Science, Kobe University, Kobe, Hyogo 657-8501, Japan
K. Maeto*
Affiliation:
Graduate School of Agricultural Science, Kobe University, Kobe, Hyogo 657-8501, Japan
K. Hamaguchi
Affiliation:
Kansai Research Center, Forestry and Forest Products Research Institute, Kyoto, Kyoto 612-0855, Japan
Y. Isaki
Affiliation:
Graduate School of Agricultural Science, Kobe University, Kobe, Hyogo 657-8501, Japan
Y. Takami
Affiliation:
Graduate School of Human Development and Environment, Kobe University, Kobe, Hyogo 657-8501, Japan
T. Naito
Affiliation:
Graduate School of Agricultural Science, Kobe University, Kobe, Hyogo 657-8501, Japan
K. Miura
Affiliation:
Graduate School of Biosphere Sciences, Hiroshima University, Higashi-Hiroshima, Hiroshima 739-8511, Japan National Agricultural Research Center for Western Region, Fukuyama, Hiroshima 721-8514, Japan
*
*Author for correspondence Phone: +81-78-803-5871 Fax: +81-78-803-5871 E-mail: maeto@kobe-u.ac.jp

Abstract

Although apomixis is the most common form of parthenogenesis in diplodiploid arthropods, it is uncommon in the haplodiploid insect order Hymenoptera. We found a new type of spontaneous apomixis in the Hymenoptera, completely lacking meiosis and the expulsion of polar bodies in egg maturation division, on the thelytokous strain of a parasitoid wasp Meteorus pulchricornis (Wesmael) (Braconidae, Euphorinae) on pest lepidopteran larvae Spodoptera litura (Fabricius) (Noctuidae). The absence of the meiotic process was consistent with a non-segregation pattern in the offspring of heterozygous females, and no positive evidence was obtained for the induction of thelytoky by any bacterial symbionts. We discuss the conditions that enable the occurrence of such rare cases of apomictic thelytoky in the Hymenoptera, suggesting the significance of fixed heterosis caused by hybridization or polyploidization, symbiosis with bacterial agents, and occasional sex. Our finding will encourage further genetic studies on parasitoid wasps to use asexual lines more wisely for biological control.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2014 

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References

Abe, Y., Nishimura, T. & Maeto, K. (2013) Causes of polymorphic melanism and its thermoregulatory function in a parasitoid wasp Meteorus pulchricornis (Hymenoptera: Braconidae). European Journal of Entomology 110, 627632.Google Scholar
Adachi-Hagimori, T., Miura, K. & Stouthamer, R. (2008) A new cytogenetic mechanism for bacterial endosymbiont-induced parthenogenesis in Hymenoptera. Proceedings of the Royal Society B 275, 26672673.CrossRefGoogle ScholarPubMed
Agresti, A. & Coull, B. (1998) Approximate is better than ‘exact’ for interval estimation of binomial proportions. American Statistician 52, 119126.Google Scholar
Ardeh, M.J., de Jong, P.W. & van Lenteren, J.C. (2005) Selection of Bemisia nymphal stages for oviposition or feeding, and host-handling times of arrhenotokous and thelytokous Eretmocerus mundus and arrhenotokous E. eremicus . BioControl 50, 449463.Google Scholar
Berry, J.A. & Walker, G.P. (2004) Meteorus pulchricornis (Wesmael) (Hymenoptera: Braconidae: Euphorinae): an exotic polyphagous parasitoid in New Zealand. New Zealand Journal of Zoology 31, 3344.Google Scholar
Beukeboom, L.W. & Zwaan, B.J. (2007) Genetics. pp. 167218 in Jervis, M.A. (Ed.) Insects as Natural Enemies: A Practical Perspective. Dordrecht, Springer.Google Scholar
Bürgi, L.P. & Mills, N.J. (2013) Developmental strategy and life history traits of Meteorus ictericus, a successful resident parasitoid of the exotic Light Brown Apple Moth in California. Biological Control 66, 173182.CrossRefGoogle Scholar
Dodds, K.S. (1939) Oogenesis in Neuroterus baccarum L. Genetica 21, 177190.Google Scholar
Doncaster, L. (1916) Gametogenesis and sex-determination in the gall-fly, Neuroterus lenticularis (Spathegaster baccarum) III. Proceedings of the Royal Society B 89, 183200.Google Scholar
D'Souza, T.G. & Michiels, N.K. (2010) The costs and benefits of occasional sex: theoretical predictions and a case study. Journal of Heredity 101 (Suppl. 1), S3441.Google Scholar
Dunning Hotopp, J.C. (2011) Horizontal gene transfer between bacteria and animals. Trends in Genetics 27, 157163.Google Scholar
Fischer, D. & Bachmann, K. (1998) Microsatellite enrichment in organisms with large genomes (Allium cepa L.). Bio Techniques 24, 796802.Google Scholar
Fuester, R.W., Taylor, P.B., Peng, H. & Swan, K. (1993) Laboratory biology of a uniparental strain of Meteorus pulchricornis (Hymenoptera: Braconidae), an exotic larval parasite of the gypsy moth (Lepidoptera: Lymantriidae). Annals of the Entomological Society of America 86, 298304.Google Scholar
Haccou, P. & Schneider, M.V. (2004) Modes of reproduction and the accumulation of deleterious mutations with multiplicative fitness effects. Genetics 166, 10931104.Google Scholar
Hagimori, T., Abe, Y., Date, S. & Miura, K. (2006) The first finding of a Rickettsia bacterium associated with parthenogenesis induction among insects. Current Microbiology 52, 97101.Google Scholar
Hale, M.L., Bevan, R. & Wolff, K. (2001) New polymorphic microsatellite markers for the red squirrel (Sciurus vulgaris) and their applicability to the grey squirrel (S. carolinensis). Molecular Ecology Notes 1, 4749.Google Scholar
Hamaguchi, K., Matsumoto, T., Maruyama, M., Hashimoto, Y., Yamane, S. & Itioka, T. (2007) Isolation and characterization of eight microsatellite loci in two morphotypes of the Southeast Asian army ant, Aenictus laeviceps . Molecular Ecology Notes 7, 984986.Google Scholar
Hamaguchi, K., Kato, K., Esaki, K. & Kamata, N. (2011) Isolation and characterization of 10 new microsatellite loci in the ambrosia beetle Platypus quercivorus . Journal of Forest Research 16, 518521.Google Scholar
Hoshizaki, S. & Shimada, T. (1995) PCR-based detection of Wolbachia, cytoplasmic incompatibility microorganisms, infected in natural populations of Laodelphax striatellus (Homoptera: Delphacidae) in central Japan: has the distribution of Wolbachia spread recently? Insect Molecular Biology 4, 237243.Google Scholar
Huddleston, T. (1980) A revision of the western Palaearctic species of the genus Meteorus (Hymenoptera: Braconidae). Bulletin of the British Museum (Natural History) Entomology 41, 158.Google Scholar
Imai, H.T., Crozier, R.H. & Taylor, R.W. (1977) Karyotype evolution in Australian ants. Chromosoma 59, 341393.Google Scholar
Kremer, N., Charif, D., Henri, H., Bataille, M., Pre´vost, G., Kraaijeveld, K. & Vavre, F. (2009) A new case of Wolbachia dependence in the genus Asobara: evidence for parthenogenesis induction in Asobara japonica . Heredity 103, 248256.Google Scholar
Liu, Y. & Li, B. (2006) Developmental interactions between Spodoptera exigua (Noctotuidae: Lepidoptera) and its unparental endoparasitoid, Meteorus pulchricornis (Braconidae: Hymenoptera). Biological Control 38, 264269.Google Scholar
Maeto, K. (1989) Systematic studies on the tribe Meteorini (Hymenoptera, Braconidae) from Japan: V. The pulchricornis group of the genus Meteorus (1). Japanese Journal of Entomology 57, 581595.Google Scholar
Marsh, P.M. (1979) The braconid (Hymenoptera) parasites of the gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae). Annals of the Entomological Society of America 72, 794810.CrossRefGoogle Scholar
Mateo Leach, I., Pannebakker, B.A., Schneider, M.V., Driessen, G.D., Van de Zande, L. & Beukeboom, L.W. (2009) Thelytoky in Hymenoptera with Venutria canescens and Leptopilina clavipes as case studies. pp. 347375 in Schön, I., Martens, K. & Van Dijk, P. (Eds) Lost Sex: The Evolutionary Biology of Parthenogenesis. Dordrecht, Springer.CrossRefGoogle Scholar
Naito, T. & Inomata, R. (2006) A new triploid thelytokous species of the genus Pachyprotasis Hartig, 1837 (Hymenoptera: Tenthredinidae) from Japan and Korea. pp. 279283, + plate 10 in Blank, S.M., Schmidt, S. & Taeger, A. (Eds) Recent Sawfly Research: Synthesis and Prospects. Keltern, Goecke & Evers.Google Scholar
Pannebakker, B.A., Pijnacker, L.P., Zwaan, B.J. & Beukeboom, L.W. (2004) Cytology of Wolbachia-induced parthenogenesis in Leptopilina clavipes (Hymenoptera: Figitidae). Genome 47, 299303.CrossRefGoogle ScholarPubMed
Peacock, A.D. & Sanderson, A.R. (1939) The cytology of the thelytokously parthenogenetic saw-fly Thrinax macula Kl. Transactions of the Royal Society of Edinburgh 59, 647660.CrossRefGoogle Scholar
Pearcy, M., Hardy, O. & Aron, S. (2006) Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity 96, 377382.Google Scholar
Pearcy, M., Hardy, O. & Aron, S. (2011) Automictic parthenogenesis and rate of transition to homozygosity. Heredity 107, 187188.Google Scholar
Quicke, D.L.J. (1997) Parasitic Wasps. London, Chapman & Hall.Google Scholar
Rabeling, C. & Kronauer, D.J.C. (2013) Thelytokous parthenogenesis in eusocial Hymenoptera. Annual Review of Entomology 58, 273292.Google Scholar
Ramirez-Romero, R., Sivinski, J., Copeland, C.S. & Aluja, M. (2012) Are individuals from thelytokous and arrhenotokous populations equally adept as biocontrol agents? Orientation and host searching behavior of a fruit fly parasitoid. BioControl 57, 427440.CrossRefGoogle Scholar
Rey, O., Loiseau, A., Facon, B., Foucaud, J., Orivel, J., Cornuet, J.M., Robert, S., Dobigny, G., Delabie, J.H.C., Mariano, C.D.S.F. & Estoup, A. (2011) Meiotic recombination dramatically decreased in thelytokous queens of the little fire ant and their sexually produced workers. Molecular Biology and Evolution 28, 2591–601.Google Scholar
Schuelke, M. (2000) An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18, 233234.CrossRefGoogle ScholarPubMed
Sharkey, M.J. (2007) Phylogeny and classification of Hymenoptera. Zootaxa 1668, 521548.Google Scholar
Sharkey, M.J., Carpenter, J.M., Vilhelmsen, L., Heraty, J., Liljeblad, J., Dowling, A.P.G., Schulmeister, S., Murray, D., Deans, A.R., Ronquist, F., Krogmann, L. & Wheeler, W.C. (2012) Phylogenetic relationships among superfamilies of Hymenoptera. Cladistics 28, 80112.Google Scholar
Stigenberg, J. & Ronquist, F. (2011) Revision of the Western Palearctic Meteorini (Hymenoptera, Braconidae), with a molecular characterization of hidden Fennoscandian species diversity. Zootaxa 3084, 195.Google Scholar
Stouthamer, R. & Kazmer, D.J. (1994) Cytogenetics of microbe-associated parthenogenesis and its consequence for gene-flow in Trichogramma wasps. Heredity 73, 317327.Google Scholar
Suomalainen, E., Saura, A. & Lokki, J. (1987) Cytology and Evolution in Parthenogenesis. Boca Raton, CRC Press.Google Scholar
Tagami, Y. & Miura, K. (2007) Sex determination and mass production of parasitic Hymenoptera. Japanese Journal of Applied Entomology 51, 120 (in Japanese.).Google Scholar
Takashino, K., Kobayashi, H. & Okada, T. (1998) Research for parasitic natural enemies to larvae of two Helicoverpa species in Shikoku. Proceedings of the Association for Plant Protection of Shikoku 33, 4955 (in Japanese.).Google Scholar
Van Wilgenburg, E., Driessen, G. & Beukeboom, L.W. (2006) Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Frontiers in Zoology 3, 115.Google Scholar
Vavre, F., de Jong, J.H. & Stouthamer, R. (2004) Cytogenetic mechanism and genetic consequences of thelytoky in the wasp Trichogramma cacoeciae . Heredity 93, 592596.Google Scholar
Weisburg, W.G., Barns, S.M., Pelletier, D.A. & Lane, D.J. (1991) 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173, 697703.Google Scholar
White, M.J.D. (1984) Chromosomal mechanisms in animal reproduction. Bolletino di zoologia 51, 123.Google Scholar
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