Cardinium symbionts induce haploid thelytoky in most clones of three closely related Brevipalpus species
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Bacterial symbionts that manipulate the reproduction of their host to increase their own transmission are widespread. Most of these bacteria are Wolbachia, but recently a new bacterium, named Cardinium, was discovered that is capable of the same manipulations. In the host species Brevipalpus phoenicis (Acari: Tenuipalpidae) this bacterium induces thelytoky by feminizing unfertilized haploid eggs. The related species B. obovatus and B. californicus are thelytokous too, suggesting that they reproduce in the same remarkable way as B. phoenicis. Here we investigated the mode of thelytokous reproduction in these three species. Isofemale lines were created of all three species and 19 lines were selected based on variation in mitochondrial COI sequences. All B. phoenicis and B. californicus lines (10 and 4 lines, respectively) produced males under laboratory conditions up to 6.7%. In contrast, males were absent from all B. obovatus lines (5 lines). Additional experiments with two B. phoenicis isofemale lines showed that males can be produced by very young females only, while older females produce daughters exclusively. For most lines it was shown that they are indeed feminized by a bacterium as treatment with antibiotics resulted in increased numbers of males up to 13.5%. Amplification and identification of specific gyrB sequences confirmed that those lines were infected with Cardinium. Three out of the five B. obovatus lines did not produce males after treatments with antibiotics, nor did they contain Cardinium or any other bacterium that might induce thelytoky. In these lines thelytoky is probably a genetic property of the mite itself. Despite the different causes of thelytoky, flow cytometry revealed that all 19 lines were haploid. Finally, the taxonomic inferences based on the mitochondrial COI sequences were incongruent with the classical taxonomy based on morphology, suggesting that a taxonomic revision of this group is necessary.
KeywordsBrevipalpus phoenicis Brevipalpus obovatus Brevipalpus californicus Acari Tenuipalpidae Cardinium Thelytoky Spanandric males
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We thank Dr. G. de Moraes and N.C. Mesa for morphologically identifying the mite species. We also thank the people at the Burger’s Bush tropical greenhouse for allowing us to collect mites and their help in doing so. The advise by M. Stift and R. Bregman on the flow cytometry analysis was much appreciated. We thank Prof. S. Menken for his remarks on an earlier draft in this manuscript. This study was supported by the Netherlands Foundation for the Advancement of Tropical Research (WOTRO), grant number W89–141.
- Dedeine F, Bandi C, Bouletreau M and Kramer LH (2003) Insights into Wolbachia obligatory symbiosis. In: Bourtzis K, Miller TA (eds) Insect Symbiosis. CRC Press, Florida, pp 267–282Google Scholar
- Doyle JJ (1991) DNA protocols for plants. In: Hewitt G, Johnson AWB, Young JPW (eds) Molecular techniques in taxonomy, vol 57, pp. 283–293Google Scholar
- Haramoto FH (1969) Biology and control of Brevipalpus phoenicis (Geijskes) (Acarina: Tenuipalpidae). Tech Bull Hawaii Agricul Exp Stat 68:1–63Google Scholar
- Hurst GDD, Jiggins FM, Majerus MEN (2003) Inherited microorganisms that selectively kill male hosts: the hidden players of insect evolution? In: Bourtzis K, Miller DJ (eds) Insect symbiosis. CRC Press, Florida, pp 177–198Google Scholar
- Kennedy JS (1995) Functional ecology of the false spider mite, Brevipalpus phoenicis (Geijskes). Dissertation, Université Catholique de Louvain, Louvain-la-NeuveGoogle Scholar
- Nagesha Chandra BK, Channabasavanna GP (1974) Biology of guave scarlet mite, Brevipalpus phoenicis (Geijskes) (Acarina: Tenuipalpidae). Proc. 4th Int Cong Acarol pp 167–176Google Scholar
- Oomen PA (1982) Studies on population dynamics of the scarlet mites, Brevipalpus phoenicis, a pest of tea in Indonesia. Mededelingen Landbouwhogeschool Wageningen 82:1–82Google Scholar
- Pijnacker LP, Ferwerda MA, Helle W (1981) Cytological investigations on the female and male reproductive system of the parthenogenetic privet mite Brevipalpus obovatus Donnadieu (Phytoptipalpidae, Acari). Acarologia 22:157–163Google Scholar
- Razoux Schultz L (1961) Enkele notities over de oranje mijt, Brevipalpus phoenicis Geijskes, op thee in Indonesie. Mededelingen landbouwhogeschool Gent 26:1694–1702Google Scholar
- Sambrook J, Frisch EF, Maniatis T (1989) Molecular cloning. Cold Spring Harbor Press, Cold Spring Harbor, New YorkGoogle Scholar
- Siegel S, Castellan NJ Jr (1988) Nonparametric statistics for the behavioral sciences, McCraw-Hill, New YorkGoogle Scholar
- Swofford DL (1998) PAUP*, phylogenetic analysis using parsimony (*and other methods). Sinauer Assoc., SunderlandGoogle Scholar
- Werren JH, O’Neill SL (1997) The evolution of heritable symbionts. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers; inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford, pp 1–41Google Scholar