Biological Journal of the Linnean Society, 2003, 79, 43–58. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 79, 43–58 43 Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2003? 2003 79? Original Article MICROORGANISMS and PARTHENOGENESISR. K. K. KOIVISTO and H. R. BRAIG *Corresponding author. E-mail: r.k.k.koivisto@bangor.ac.uk Intraclonal genetic variation: ecological and evolutionary aspects. Edited by H. D. Loxdale FLS, FRES and G. Lushai FRES Microorganisms and parthenogenesis R. K. KAROLIINA KOIVISTO* and HENK R. BRAIG School of Biological Sciences, University of Wales Bangor, Bangor LL57 2UW, UK Endosymbionts are being discovered in unprecedented numbers of invertebrate species. The bacterium Wolbachia pipientis alone is carried by some 20% of all insect species, in which it is responsible for such reproductive manip- ulations as cytoplasmic incompatibility, feminization of genetic males, male-killing and parthenogenesis. The dis- covery of Wolbachia-induced thelytoky in hymenopteran parasitoids has initiated the successful search in other groups of haplodiploid species. Haplodiploidy has arisen at least 17 times during animal evolution and intracellular bacteria that effect sexual development have been found in many of these haplodiploid groups, rekindling the ques- tion regarding the origin of haplodiploidy. The detection of Wolbachia in parthenogenetic thrips (Thysanoptera), booklice (Psocoptera), springtails (Collembola), mites (Acari) and Xiphinematobacter in dragger nematodes (Dory- laimida) raises the possibility of bacterial-induced parthenogenesis in diplodiploid species as well. Recent studies indicate that Wolbachia might be just one of a rapidly increasing list of intracellular bacteria capable of inducing par- thenogenesis in their host. The search for novel endosymbionts will rely heavily on previous taxonomic work, but the possibilities for discovery remain boundless. © 2003 The Linnean Society of London. Biological Journal of the Lin- nean Society 2003, 79, 43–58. ADDITIONAL KEYWORDS: bacteria – cytogenetics – endosymbionts – geographical parthenogenesis – haplodiploidy – sex ratio distortion – thelytoky – Wolbachia pipientis. INTRODUCTION Parthenogenesis is surprisingly common among both plants and animals, perhaps accounting for up to 1% of the total number of species (Suomalainen, Saura & Lokki, 1987; Short & Balaban, 1994). With the excep- tion of the most evolved taxa such as gymnosperms and mammals, in which it has not been reliably reported, parthenogenesis is practically universally distributed in the tree of life. This might reflect the ongoing battle between two basic forms of reproduc- tion. Only bdelloid rotifers constitute an order that consists entirely of parthenogens. Most parthenogens have close relatives that are sexual, and often sexual and asexual populations of one species have been found geographically separated. Local adaptation eas- ily explains these patterns. However, the sympatric occurrence of sexual and asexual populations defies mainstream evolutionary thinking. After all, cytoplas- mic genes and not nuclear ones might be the decisive evolutionary force behind some of the more interesting population structures of invertebrates. DISCOVERING ENDOSYMBIOTIC BACTERIA Many invertebrates are known to have intimate intra- cellular relationships with a diverse array of microor- ganisms. The taxonomic range of the invertebrate hosts to the microorganisms is equally wide. Microor- ganisms associated with parthenogenesis can be placed into three general categories. The Wolbachia pipientis assemblage is a widespread group of closely related a-Proteobacteria known to cause a variety of reproductive alterations, including cytoplasmic incom- patibility, thelytokous parthenogenesis, feminization of genetic males, and male-killing (O’Neill, Hoffmann & Werren, 1997; Bourtzis & Braig, 1999; Stouthamer, Breeuwer & Hurst, 1999; Stevens, Giordano & Fialho, 2001). Bacteria belonging to the Cytophaga–Flexi- bacter–Bacteroides (CFB) group are associated with parthenogenetic wasps and feminized mites (Zchori- Fein et al., 2001; Weeks, Marec & Breeuwer, 2001). Downloaded from https://academic.oup.com/biolinnean/article/79/1/43/2639914 by guest on 24 November 2023