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OBLIGATE THELYTOKY IN ORIBATID MITES: NO EVIDENCE FOR WOLBACHIA INDUCEMENT

Published online by Cambridge University Press:  31 May 2012

Marie-Jeanne Perrot-Minnot*
Affiliation:
Department of Biology, University of Rochester, Rochester, New York, USA 14627
Roy A. Norton
Affiliation:
College of Environmental Science and Forestry, State University of New York, Syracuse, New York, USA 13210
*
1Author to whom all correspondence should be sent at the following address: Laboratoire de Zoologie, École Nationale Supérieure Agronomique de Montpellier, INRA, 2 place Viala, F-34060 Montpellier Cedex 1 France.

Abstract

The wide distribution of obligate thelytoky in oribatid mites (Acari: Oribatida) raises the question of the mechanisms that allowed genetic diversity to be maintained or even promoted in these taxa. We tested whether or not endosymbiotic bacteria Wolbachia are associated with thelytoky in eight species of oribatid mites (as it is for most thelytokous parasitic Hymenoptera studied so far) by using a polymerase chain reaction assay. Our negative results in the selective amplification of Wolbachia DNA suggest that these bacteria are not responsible for the thelytokous mode of reproduction of oribatid mites. On the basis of known or suspected cytogenetic mechanisms in oribatid mites (automictic thelytoky, inverted meiosis), we discuss an alternative hypothesis for the inducement of thelytoky, and its relevance to the observed diversification of thelytokous oribatid mites over evolutionary time.

Résumé

L’étendue du phénomène de thélytoquie obligatoire chez les oribates (Acari : Oribatida) met en question les mécanismes qui ont permis le maintien et même la progression de la diversité chez ces taxons. Nous avons tenté de découvrir si les bactéries endosymbiotiques Wolbachia sont reliées au phénomène de la thélytoquie chez huit espèces d’oribates (comme c’est le cas chez la plupart des hyménoptères parasites thélytoques étudiés à ce jour), en procédant à des tests de réaction en chaîne par la polymérase. Les résultats négatifs des tentatives d’amplification sélective de l’ADN de Wolbachia indiquent que ces bactéries ne sont pas responsables du mode thélytoque de reproduction des oribates. D’après les mécanismes cytogénétiques connus ou présumés exister chez les oribates (thélytoquie automictique, méiose inversée), nous envisageons une hypothèse alternative sur les causes de la thélytoquie et sur son influence sur la diversification observée chez les oribates thélytoques au cours de l’évolution.

[Traduit par la Rédaction]

Type
Articles
Copyright
Copyright © Entomological Society of Canada 1997

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References

Breeuwer, J.A.J., and Jacobs, G.. 1996. Wolbachia: intracellular manipulators of mite reproduction. Experimental and Applied Acarology 20: 421434.CrossRefGoogle ScholarPubMed
Diehl, P.A., Aeschlimann, A., and Obenchain, F.D.. 1982. Tick reproduction: oogenesis and oviposition, Current Themes in Tropical Science 1: 277350.Google Scholar
Evans, G.O. 1992. Principles of Acarology. CAB International, Wallingford, UK. 563 pp.CrossRefGoogle Scholar
Hewitt, G.M. 1975. A new hypothesis for the origin of the parthenogenetic grasshopper Moraba virgo. Heredity 34: 117136.CrossRefGoogle Scholar
Hughes-Schrader, S. 1948. Cytology of coccids (Coccoidea-Homoptera). Advances in Genetics 2: 127203.CrossRefGoogle Scholar
Johanowicz, D.L., and Hoy, M.A.. 1995. Molecular evidence for a Wolbachia endocytobiont in the predatory mite Metaseiulus occidentalis. Journal of Cellular Biochemistry 21A: 198.Google Scholar
Johanowicz, D.L., and Hoy, M.A.. 1996. Wolbachia in a predator–prey system: 16S ribosomal DNA analysis of two phytoseiids (Acari: Phytoseiidae) and their prey (Acari: Tetranychidae). Annals of the Entomological Society of America 89: 435–431.CrossRefGoogle Scholar
Johnson, S.G. 1992. Spontaneous and hybrid origins of thelytoky in Campeloma decisum (freshwater prosobranch snail). Heredity 68: 253261.CrossRefGoogle Scholar
Judson, O.P., and Normark, B.B.. 1996. Ancient asexual scandals. Trends in Ecology and Evolution 11: 4146.CrossRefGoogle ScholarPubMed
Legner, E.F. 1985. Effects of scheduled high temperature on male production in thelytokous Muscidifurax uniraptor (Hymenoptera: Pteromalidae). The Canadian Entomologist 117: 383389.CrossRefGoogle Scholar
Maynard-Smith, J. 1986. Contemplating life without sex. Nature (London) 324: 300301.CrossRefGoogle Scholar
Norton, R.A. 1994. Evolutionary aspects of oribatid mite life histories and consequences for the origin of the Astigmata. pp. 99135in Houck, M.A. (Ed.), Mites. Ecological and evolutionary analyses of life history patterns. Chapman and Hall, New York.Google Scholar
Norton, R.A., and Kethley, J.B.. 1990. Berlese's North American oribatid mites: historical notes, recombinations, synonymies and type designations. Redia 62: 421499.Google Scholar
Norton, R.A., Kethley, J.B., Johnston, D.E., and Oconnor, B.M.. 1993. Phylogenetic perspectives on genetic systems and reproductive modes of mites. pp. 899in Wrensch, D.L., and Ebbert, M.A. (Eds.), Evolution and Diversity of Sex Ratio in Insects and Mites. Chapman and Hall, New York.CrossRefGoogle Scholar
Norton, R.A., and Palmer, S.C.. 1991. The distribution, mechanisms and evolutionary significance of thelytoky in oribatid mites. pp. 108136in Schuster, R., and Murphy, P.W. (Eds.), The Acari—Reproduction, Development and Life History Strategies. Chapman and Hall, London.Google Scholar
Nur, U. 1980. Evolution of unusual chromosome systems in scale insects (Coccoidea: Homoptera). pp. 97117in Blackman, R.L., Hewitt, G.M., and Ashburner, M. (Eds.), Insect Cytogenetics. Symposia of the Royal Entomological Society of London 10.Google Scholar
Palmer, S.C., and Norton, R.A.. 1990. Further experimental proof of thelytokous thelytoky in oribatid mites (Acari: Oribatida: Desmonomata). Experimental and Applied Acarology 8: 149159.CrossRefGoogle Scholar
Palmer, S.C., and Norton, R.A.. 1992. Genetic diversity in thelytokous oribatid mites (Acari: Acariformes: Desmonomata). Biochemical Systematics and Ecology 20: 219231.CrossRefGoogle Scholar
Pintureau, B., and Babault, M.. 1981. Caractérisation enzymatique de Trichogramma evanescens et de T. maidis (Hym.: Trichogrammatidae): étude des hybrides. Entomophaga 26: 1122.CrossRefGoogle Scholar
Rousset, F., Bouchon, D., Pintureau, B., Juchault, P., and Solignac, M.. 1992. Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proceedings of the Royal Society of London Series B Biological Sciences 250: 9198.Google ScholarPubMed
Schilthuizen, M., and Stouthamer, R.. 1997. Horizontal transmission of parthenogenesis-inducing microbes in Trichogramma wasps. Proceedings of the Royal Society of London Series B Biological Sciences 264: 361366.CrossRefGoogle ScholarPubMed
Stouthamer, R., Breeuwer, J.A.J., Luck, R.F., and Werren, J.H.. 1993. Molecular identification of microorganisms associated with thelytoky. Nature (London) 361: 6668.CrossRefGoogle Scholar
Stouthamer, R., and Kazmer, D.J.. 1994. Cytogenetics of microbe-associated thelytoky and its consequences for gene flow in Trichogramma wasps. Heredity 73: 317327.CrossRefGoogle Scholar
Stouthamer, R., Luck, R.F., and Hamilton, W.D.. 1990 a. Antibiotics cause thelytokous Trichogramma to revert to sex. Proceedings of the National Academy of Sciences of the United States of America 87: 24242427.CrossRefGoogle Scholar
Stouthamer, R., Pinto, J.D., Platner, G.R., and Luck, R.F.. 1990 b. Taxonomic status of thelytokous forms of Trichogramma (Hymenoptera: Trichogrammatidae). Annals of the Entomology Society of America 83: 475481.CrossRefGoogle Scholar
Stouthamer, R., and Werren, J.H.. 1993. Microbes associated with thelytoky in wasps of the genus Trichogramma. Journal of Invertebrate Pathology 61: 69.CrossRefGoogle Scholar
Taberly, G. 1987 a. Recherches sur la parthénogenèse thélytoque de deux espèces d'Acariens Oribates: Trhypochthonius testotum (Berlese) et Platynothrus peltifer (Koch). I. Acarologia 28: 187198.Google Scholar
Taberly, G. 1987 b. Recherches sur la parthénogenèse thélytoque de deux espèces d'Acariens Oribates: Trhypochthonius testotum (Berlese) et Platynothrus peltifer (Koch). II. Étude anatomique, histologique et cytologique des femelles parthénogénétiques. lère partie. Acarologia 28: 285293.Google Scholar
Taberly, G. 1987 c. Recherches sur la parthénogenèse thélytoque de deux espèces d'Acariens Oribates: Trhypochthonius testotum (Berlese) et Platynothrus peltifer (Koch). II. Étude anatomique, histologique et cytologique des femelles parthénogénétiques. 2ème partie. Acarologia 28: 389403.Google Scholar
Tsagkarakou, A., Guillemaud, T., Rousset, F., and Navajas, M.. 1996. Molecular identification of a Wolbachia endosymbiont in a Tetranychus urticae strain (Acari: Tetranychidae). Insect Molecular Biology 5: 217221.CrossRefGoogle Scholar
Walsh, P.S., Metzger, D.A., and Higuchi, R.. 1991. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10: 506513.Google ScholarPubMed
Werren, J.H., Windsor, D., and Guo, L.R.. 1995 b. Distribution of Wolbachia among neotropical arthropods. Proceedings of the Royal Society of London Series B Biological Sciences 262: 197204.Google Scholar
Werren, J.H., Zhang, W., and Guo, L.R.. 1995 a. Evolution and phylogeny of Wolbachia bacteria: reproductive parasites of arthropods. Proceedings of the Royal Society of London Series B Biological Sciences 261: 5571.Google ScholarPubMed
White, M.J.D., 1973. Animal Cytology and Evolution. 3rd ed. Cambridge University Press, Cambridge, England.Google Scholar
Wrensch, D.L., Kethley, J.B., and Norton, R.A.. 1994. Cytogenetics of holokinetic chromosomes and inverted meiosis: keys to the evolutionary success of mites, with generalizations on eukaryotes. pp. 282343in Houck, M.A. (Ed.), Mites: Ecological and Evolutionary Analyses of Life History Patterns. Chapman and Hall, New York.CrossRefGoogle Scholar
Zchori-Fein, E., Rosen, D., and Roush, R.T.. 1994. Microorganisms associated with thelytoky in Aphytis lingnansensis Compere (Hymenoptera: Aphelinidae). International Journal of Insect Morphology and Embryology 23: 169172.CrossRefGoogle Scholar
Zchori-Fein, E., Roush, R.T., and Hunter, M.S.. 1992. Male production induced by antibiotic treatment in Encarsia Formosa (Hymenoptera: Aphelinidae), an asexual species. Experientia 48: 102105.CrossRefGoogle Scholar