the feminizing effect is lost (Rigaud et al., 1991a). At high ... female-biased sex ratios: Armadillidium album and Ligia oceanica (Juchault et al., 1974),. A. nasatum .... organisms probably turn off a genetic switch during the early stages of sexual.
Biodiversity a n d Conservation 5, 999-1013 (1996)
What generates the diversity of arthropod interactions?
Wolbachia
-
THIERRY RIGAUD* Universit~ de Poitiers, Laboratoire de Biologie Animale, URA CNRS 1975, 40 avenue du Recteur Pineau, F-86022 Poitiers Cedex, France
FRANCOIS ROUSSET Universit~ de Montpellier 2, LS.E.M., URA CNRS 327 'G~ndtique et Environnement', CC 065, Place Eugene Bataillon, F-34095 Montpellier Cedex 05, France
Received 28 November 1994; revised and accepted 5 April 1995
Wolbachia are strictly endocellular, vertically transmitted bacteria associated with insects and crustaceans. This group of parasites modify their hosts' reproduction so as to increase their own fitness. This paper reviews the variability of these parasitic alterations and their consequences for host biology and populations. Wolbachia induce cytoplasmic incompatibility (a characteristic apparently specific to Wolbachia) in several insects and one isopod crustacean; parthenogenesis (thelytoky) in haplo-diploid insects; feminization in various isopods. The consequences of these phenomena on speciation, population dynamics and genetic polymorphism are discussed. The variability of the mechanisms of host sex determination is one important factor responsible for the diversity of Wolbachia-host interactions. However, parasite characteristics, such as the capacity to disturb host mitosis, and the ability to be horizontally transferred between hosts, also appear to play a role in this diversity. Keywords: cytoplasmic incompatibility; parthenogenesis; feminization; parasitic interactions;
genetic variability.
Introduction Host-parasite interactions are generally considered in terms of the development of parasite virulence and host response, generating genetic changes in both partners. These changes could lead to major evolutionary patterns (as proposed for the evolution and maintenance of sexual reproduction (Howard and Lively, 1994)). However, recent research shows the need for a better understanding of host-parasite interactions in order to assess the parasiteinduced variation at genetic and population levels (Minchella and Scott, 1991). This need is due in part to the difficulty of demonstrating the existence of co-evolutionary processes in the wild. This paper reviews a peculiar host-parasite association involving a group of endocellular microorganisms of the genus Wolbachia which pervert reproduction in their hosts. The variations in the types of interaction are first described. The basic characteristics underlying the multiple interactions are then analysed to provide a better understanding of this variability. *To whom correspondence should be addressed. 0960-3115 © 1996 Chapman & Hall
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Wolbachia microorganisms and the range of their effects Phylogenetic position and diversification of Wolbachia Wolbachia are strictly endocellular bacteria (endocytobiotes) associated with arthropods. In females, they infect most oocytes and they are maternally transmitted to offspring. These microorganisms were first described in the mosquito Culex pipiens (Hertig, 1936), and have been characterized by their ultrastructure, their sensitivity to high temperatures and antibiotics. They were named Wolbachia pipientis, belonging to the Rickettsiales bacteria. Many more Wolbachia-like bacteria have subsequently been found in various arthropods (Martin et al., 1973: Wright and Barr, 1981; Kellen et al., 1981; Binnington and Hoffmann, 1989: O'Neill, 1989: Breeuwer and Werren, 1990; Kambhampati et al., 1993: Juchault et al., 1994: Solignac et al., 1994). The taxonomic status of these microorganisms has recently been defined by sequencing parts of their 16S rDNA (Breeuwer et al., 1992: O'Neill et al., 1992; Rousset et al., 1992a, b). WoIbachia belong to the c~ subdivision of purple bacteria (Proteobacteria), and the most closely related genera are also endocytobiotic bacteria such as Rickettsia, Ehrlichia or Anaplasma. Wolbachia form a monophyletic group, and sequence data suggest that those described to date may have diverged about 50 million years ago (Rousset et al., 1992b). Effects of Wolbachia on their hosts One of the basic characteristics of Wolbachia described by Weiss (1974) is that they 'may interfere with their host reproduction'. In fact, the variety of such interactions is well summarized by Cioran's (1973) aphorism 'avoir commis tousles crimes, hormis celui d'etre pbre' (to have committed all crimes, save that of being a father). Initial interest in Wolbachia arose when they were shown to be associated with cytoplasmic incompatibility in the mosquito Culex pipiens, a phenomenon first described by Ghelelovitch (1952). The presence of bacteria is associated with sterility between certain strains: crosses between uninfected females and infected males result in non-viable progeny, whereas the reciprocal crosses are compatible and produce normal progeny (Yen and Barr, 1971) (Fig l a). This cytoplasmic incompatibility (CI) disappeared when infected males were treated with antibiotics, and all types of crosses produced normal progenies (Yen and Barr, 1971). These features have been found in several insects and in one isopod crustacean (Porcellio dilatatus) (Table 1). Other cases of Wolbachia-induced CI have been reported, but have not (or not yet) been correctly characterized as CI, or shown to be due to Wolbachia. In some hosts, CI occurs between infected individuals (Barr, 1982: Breeuwer and Werren, 1990; O'Neill and Karr, 1990) assumed to harbour different bacterial strains. These strains are seen as representing different "incompatibility types'. C1 does not lead to offspring death in Nasonia but rather to the production of all male haploid progeny (Breeuwer and Werren, 1990). Thelytokous parthenogenesis, the production of diploid females by unfertilized females (Fig. lb), occurs frequently in many species of haplodiploid parasitoid wasps (Luck et al., 1993), and is due to symbiont in several cases. In parthenogenetic lineages, antibiotic treatment or high temperatures cure the hosts of their symbionts, so that males appear in the progeny and sexuality is restored (Legner, 1985; Stouthamer et al., 1990; Zchori-Fein et al., 1992, 1994). The symbionts of several Trichogramma species and another parasitoid
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Diversity of Wolbachia-arthropod interactions
wasp, Muscidifurax uniraptor, are Wolbachia symbionts (Rousset et al., 1992b; Stouthamer et al., 1993), as may also be the case for Aphytis lingnanesis (Zchori-Fein et al., 1994). The third way in which Wolbachia alter the sexuality of their hosts has been shown only in crustacea. Some females of the woodlouse Armadillidium vulgare regularly produce highly female-biased broods (Vandel, 1941; Juchault et al., 1993). Wolbachia bacteria are responsible for this strong sex ratio deviation; they reverse genetic males (homogametic
(a)
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(b)
0,, x 9 ~ n chr.
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.
~
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.
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Figure 1. Diagram of the variability of Wolbachia effects on their hosts. (a) Cytoplasmic incompatibility; (b) parthenogenesis (thelytoky); (c) feminization. Black symbols = Wolbachia-infected individuals; white symbols = uninfected individuals; chr. = chromosomes; ZZ/WZ = homo-heterogametic status of individuals. To simplify, Wolbachia transmission to offspring was assumed to be total: all offspring from a single mother were
Wolbachia-infected.
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Table 1. Arthropod species in which Wolbachia-induced cytoplasmic incompatibility has been recorded Species Insects Culex pipiens (Diptera) Aedes scutellaris (Diptera) Aedes albopictus (Diptera) Drosophila simulans (Diptera) Drosophila melanogaster (Diptera) Ephestia cautella (Lepidoptera) Tribolium confusum (Coleoptera) Hypera postica (Coleoptera) Nasonia sp (Hymenoptera) Laodelphax striatellus (Homoptera) Crustacea PorceUio dilatatus (Isopoda)
Reference Yen and Barr (1973) Trpis et al. (1981) Kambhampati et al. (1993) Hoffmann et al. (1986) Hoffmann et al. (1988) Kellen et al. ( 1981 ) Wade and Stevens (1985) Hsiao and Hsiao (1985) Breeuwer and Werren (1990) Noda (1984)
Legrand et al. (1985)
ZZ) into functional neo-females (Martin et al., 1973). Because of the maternal transmission of Wolbachia, daughters from infected mothers also produce all-female or highly female-biased progeny (Fig. l c). All individuals in wild infected lineages are chromosomic males (see Evolution of sex-determining mechanisms, below); the female phenotype is determined only by the presence of feminizing Wolbachia, and males come from uninfected oocytes (Juchault et al., 1993). This is a typical case of cytoplasmic sex determination (Bull, 1983). Here again, heat or antibiotic treatment kills Wolbachia, and the feminizing effect is lost (Rigaud et al., 1991a). At high temperatures, offspring develop without any cytoplasmic influence on their sex determination. They therefore recover a phenotype consistent with their nuclear genotype, and, as a consequence, most broods are all-male (Rigaud et al., 1991b). Wolbachia have been found in other terrestrial isopods with female-biased sex ratios: Armadillidium album and Ligia oceanica (Juchault et al., 1974), A. nasatum, (Juchault and Legrand, 1989), Porcellionides pruinosus, Chaetophiloscia elongata (Juchault et al., 1994), and in one intertidal isopod Sphaeroma rugicauda (Martin et al., 1994). However, except for the bacteria harboured by A. nasatum (Rousset et al.. 1992b), it is not yet known whether these Wolbachia are closely related to those of A. vulgare.
Consequences of Wolbachia-arthropod associations Evolution of sex-determining mechanisms
The appearance of cytoplasmic sex determination in ArmadiUidium vulgate had major consequences for the evolution of sex determination. For example, in a population with ZW-ZZ sex determination, Z and W are maintained because they are required male and
Diversity of Wolbachia-arthropod interactions
1003
female determinants, but in the presence of Wolbachia, W is no longer a required female determinant. The high transovarial transmission rate of Wolbachia plus their feminizing effect lead to the gradual loss of the W chromosome from infected lineages (Taylor, 1990). Cytoplasmic sex determination (ZZ males and ZZ + Wolbachia females) thus rapidly develops, as observed in various infected populations (Juchault et al., 1993). A second feminizing factor has been found in this species (Legrand and Juchault, 1984). This non-bacterial factor (labelled f) also converts genetic males into functional females (ZZ + f females), which generally produce female-biased broods. However, the percentage of males often increases in successive broods of a given mother, and the inheritance of female-biased sex ratios is unstable. Although f transmission is mainly maternal, some male transmission occasionally occurs, suggesting that this factor lies in the nucleus rather than in the cytoplasm. Legrand and Juchault (1984) emphasized the analogy between f transmission and expression and that of transposable elements. In one laboratory strain of A. vulgare, Legrand and Juchault (1984) observed the transformation of an experimental Wolbachia-infected lineage into what was symptomatically an fharbouring lineage: bacteria were gradually lost, and f appeared spontaneously. The precise nature of the f factor remains uncertain, but it has been suggested that it is a segment of bacterial DNA carrying the feminizing information which might be unstably integrated into the host nuclear genome (Legrand and Juchault, 1984). Thus, under this hypothesis, symbiosis between Wolbachia and Armadillidium would give rise to a new sex-determining mechanism. This mechanism is selected for in wild populations (Juchault et al., 1992, 1993) and maintains a proportion of males high enough to ensure reproduction of the hosts. Recent genetic data also show that the f factor can acquire (under unknown conditions) a Mendelian inheritance, by a stable integration into a Z chromosome of the host (Juchault and Mocquard, 1993). This integration of a feminizing element creates a new female sex chromosome (W-like chromosome) from a male chromosome. The evolution of sex determining mechanisms in Armadillidium vulgare can thus be described as in Fig 2. This evolution might have begun with the appearance of parasitic sex determination from genetic sex determination, but it could also reflect the appearance of sexual chromosomes from cytoplasmic sex determination, as discussed in Juchault and Mocquard (1993). The high level of Wolbachia infection in terrestrial isopods indicates that parasitic sex determination undoubtedly plays a major role in the evolution of sex determining mechanisms in this group.
Polymorphism of cytoplasmic genomes It is generally assumed that altering their host's reproduction favours the spread of intracytoplasmic symbionts into uninfected populations (Hurst, 1993). Wolbachia-infected cytoplasms tend to replace uninfected ones (Stouthamer et al., 1990; Taylor, 1990; Rousset and Raymond, 1991; Turelli and Hoffmann, 1992). One of the most intriguing aspects of several Wolbachia symbioses is, however, the existence of striking cytoplasmic polymorphisms, at both the molecular and phenotypic (incompatibility types) levels. In the case of cytoplasmic incompatibility, simple population genetics models (Fine, 1978; Turelli et al., 1992) can explain the long-term persistence of low frequencies of uninfected individuals at equilibrium. In Tribolium confusum, curing may be frequent in natural populations, which might explain in part the observed polymorphism (Stevens and
Rigaud and Rousset
1004 Genetic sex determination
Wo~Ibachia (F)
Creation of a W-like ch romosome
(~) 77+F1 Cytoplasmic sex determination
Stable integration of f into the host genome
Unstable integration of a segment of the bacterial DNA (f factor) into the host genome f = transposon, plasmid?
Qzz÷, Parasitic sex determination
Figure 2. The evolution of sex-determining mechanisms in the woodtouse Armadillidium
vulgare (from Juchault and Mocquard, 1993). The origin of this evolution can be seen in two points of the circle: (i) the chromosomal sex determination is ancestral and is then altered by the Wolbachia,or (ii) the gonochorism could have evolved after the appearance of feminizing Wotbachia in ancestral hermaphrodites. Wicklow, 1992; but see section How often do new injections occur, and how successful are they? below). In the case of feminization or parthenogenesis, a polymorphism of infected and uninfected individuals can also be due to incomplete transmission, or if fecundity is affected by some interaction between infection and environmental factors (Stouthamer and Luck, 1993). A direct consequence of CI might be dramatic changes in mitochondrial DNA frequency in populations and a loss of mtDNA variability, as in Drosophila simulans (Turelli et al., 1992). A loss of cytoplasmic variability may also occur after invasion of feminizing factors. In A. vulgare, the elimination of Wolbachia-infected lineages by the f factor (Juchault et al., 1992) also decreases mitochondrial polymorphism. However, there is always mitochondrial polymorphism in wild populations, and one explanation for this is the insertion of f into the host genome, preventing the disappearance of some mitochondrial types (Souty-Grosset et al., 1992, Grandjean et al., 1993).
Gene .flow and speciation Like almost all biological phenomena, cytoplasmic incompatibility may be a mode of speciation. However, there is no clear mechanism by which Wolbachia could be the only agent of reproductive isolation (Rousset and Raymond, 1991 ), because polymorphism of
Diversity of Wolbachia--arthropod interactions
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incompatible cytoplasms cannot be stable in a panmictic population (Rousset et al., 1991). Wolbachia-infected and uninfected strains of the isopod Porcellio dilatatus can be distinguished by their phenotypes, genotypes and geographic distribution, allowing the identification of two sub-species (Legrand and Juchault, 1986). However, it is not known whether the unidirectional cytoplasmic incompatibility occurred before allopatry, and thus we cannot be sure that cytoplasmic incompatibility is the cause of this sub-species differentiation. However, if there is pre-mating isolation, independent bacterial clones may evolve in mutually incompatible types which have the potential to cause isolation at the level of cytoplasmic genes, and at the level of nuclear genes if incompatibility is complete. This may have occurred in several Nasonia species (Breeuwer and Werren, 1990, 1993a). Allopatric populations of Drosophila simulans also possess distinct bacteria responsible for bidirectional incompatibility (Montchamp-Moreau et al., 1991; Rousset et al., 1992a; Rousset and de Stordeur, 1994). The occurrence of multiple infections in the same species or the rate at which two descendant clones of an ancestral symbiont can become reciprocally incompatible would be important parameters. The latter is suspected to be high in the mosquito Culex pipiens (Barr, 1982), but the occurrence of many incompatibility types has not caused reproductive isolation, as shown by the rapid worldwide spread of some insecticide-resistance alleles in this species (Raymond et al., 1991).
Population dynamics There is no known model in which incompatibility would drive a population to extinction, but this is possible in the short term for feminization, if no males are available for reproduction (Taylor, 1990). The absence of A. vulgare populations containing only Wolbachia-infected females may be due to population extinctions induced by such a phenomenon (Juchault et al., 1993). In cases where extinction has not occurred (those we see), evolution of repressor systems can explain this persistence (Rigaud and Juchault, 1992, 1993), along with the co-existence of two feminizing sex ratio distorters in populations (Juchault et al., 1992, 1993). The various reasons which could lead parthenogenetic lineages to extinction have been much discussed (Maynard-Smith, 1988), but are not relevant when there is gene flow between sexual and thelytokous forms. Such gene flow occurs in Trichogramma, where infected females often reproduce sexually (Stouthamer and Kazmer, 1994). Selfish genetic elements which could affect population dynamics would be of great use for biological control and there is much interest in Wolbachia because of this. They could be used as vectors of genes neutral to the host, but favourable to man (Hastings, 1994) in natural host populations. These experiments would provide considerable information on the factors implicated in the evolution of Wolbachia symbioses.
What is responsible for the diversity of Wolbachia-host interactions? Wolbachia is a relatively homogeneous group of bacteria with a wide range of effects on their host. Could these effects be due to the bacteria themselves or to their host?
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Wolbachia characteristics Wolbachia are the only known agents of cytoplasmic incompatibility (CI), probably because of an adaptation which evolved once in a common ancestor. Little is known of how exactly Wolbachia act, but the patterns differ according to the hosts. In Culex, CI is due to the spermatozoon being stopped in the egg cytoplasm before it reaches the female nucleus (Jost, 1971). However, the sperm also stop temporarily in compatible eggs (Laven, 1967). So the significance of these observations is not clear. In all other species, incompatibility is associated with an abnormal first mitotic division: abnormal condensation of chromosomes derived from the sperm in Nasonia (Breuwer and Werren, 1990), abnormal eviction of chromosomes in Porcellio, in which the number of chromosomes varies during development and from one egg to another (Legrand and Juchault, 1986) and where 90% of mitoses are abnormal after 96 hours of development (Artault, 1977), and finally, non-segregation of nuclei in Drosophila. Mitosis is altered in all cases, chromosomal DNA 'lost' in the cytoplasm is degraded, which probably involves cellular mechanisms which are not specific to Wolbachia action. The induction of parthenogenesis also appears to be due to manipulation of mitosis (Stouthamer and Kazmer, 1994): Wolbachia prevent the segregation of chromosomes in the first mitotic division, which restores diploidy, leading to the development of parthenogenetic females. The only manipulation of reproduction where mitotic changes are not suspected is the feminization in isopods. The chromosome number, shape and division are identical in Wolbachia-infected and uninfected individuals (Artault, 1977). The precise mechanism of this feminization is not known, but Wolbachia appears to specifically inhibit the male genes (Legrand et al., 1987). This prevents the differentiation of androgenic glands and hence the release of androgenic hormone. In the absence of this hormone, the undifferentiated gonads develop into ovaries, inducing development of the female phenotype and physiology. Therefore, it appears that Wolbachia do not have a single mode of action to pervert sexuality in arthropods. However, the wide distribution of CI indicates that there is little doubt that these bacteria have acquired a specific means of disturbing a common mechanism of arthropod mitosis, although it is not efficient in every host species. Host characteristics There are certainly a number of characteristics which make symbiosis in general, or specific alterations of sexuality, more likely in some taxa. Host characteristics may explain why cytoplasmic sex determination is so much more common in crustacea (Legrand et al., 1987) than in insects. Two factors, the hormonal control of sex differentiation, and the fact that each individual possesses genetic programmes for male and female differentiation facilitate this phenomenon in crustacea (Charniaux-Cotton and Payen, 1985). Microorganisms probably turn off a genetic switch during the early stages of sexual differentiation, inhibiting the androgenic gland differentiation (Legrand et al., 1987). The inhibition of male genes is not specific to Wolbachia: several protists (Microsporida and Paramyxida) induce the same phenomenon in amphipod crustacea (Gammarus duebeni and Orchestia gamarellus respectively), inducing comparable distortions of the sex ratio (Bulnheim and Vavra, 1968, Ginsburger-Vogel and Desportes, 1979). The cytoplasmic control of sex determination thus appears to be more a characteristic of crustacea because
Diversity of Wolbachia-arthropod interactions
1007
of the ease with which sex reversal is induced, rather than a speciality of a given group of microorganisms. The fact that Wolbachia are present in all isopod tissues, while very rarely found outside gonads in insects, may also facilitate sex manipulation in crustaceans. These characteristics may explain why good examples of feminization are not known in insects, unlike other modes of cytoplasmic sex ratio distortion (cf. Hurst, 1993, for review). In Drosophila, no single genetic change that converts an XY individual into a functional female is known, because of the non-hormonal sex differentiation, the distinct differentiation of somatic and germinal tissues, and constraints of dosage compensation (e.g. Gilbert, 1991; Wilkins, 1993). Wolbachia-induced parthenogenesis occurs in Hymenoptera by gamete duplication (Stouthamer and Kazmer, 1994). This mechanism may restrict this form of parthenogenesis to taxa which do not have complementary sex determination (CSD, in which females are diploid individuals heterozygous at sex determining locus) (Cook, 1993), such as Chalcidoidea, because gamete duplication produces completely homozygous genotypes which determine male differentiation under CSD. Thelytoky is more common in these taxa (Cook, 1993; Luck et al., 1993.) How often do new infections occur, and how successful are they? The non-congruence between the phylogenetic tree of Wolbachia and that of their hosts is clearly due to horizontal transfers (O'Neill et al., 1992; Rousset et al., 1992a, b). The most recent common ancestor of currently known agents of CI is roughly 50 million years old (Rousset et al., 1992a; time scale from Ochman and Wilson, 1987), which is much more recent that the divergence of their hosts. There have been several infections in Drosophila simulans (Rousset et al., 1992a; Rousset and Solignac, 1995). Wolbachia transfers have also been shown to occur in terrestrial isopods by a simple hemolymph contact, a route likely to be used in natural populations (Rigaud and Juchault, 1995). However, even if such a transfer does occur, the infected cytoplasmic lineage does not always replace the uninfected cytoplasm. This is particularly relevant for CI, which is an example of positive frequency-dependent selection: the fitness of uninfected females will decrease proportionally to the frequency of infected males, so selection is weak when infection is rare. In a panmictic population of N females, the standard diffusion equations for the Wright-Fisher model give an estimate of the probability that a bacterial clone initially present in only one female will succeed in newly infecting an uninfected species. If s is the fraction of lethal embryos in incompatible crosses and 1 - d is the fecundity of infected females relative to uninfected females, this probability is:
u =
_Nd2 .e s
This probability decreases with an increasing population size, and equals: 2
when d = 0
u is also the probability of the spread of the infection if a mother transmits parasites to 1 - d of her offspring. Population subdivision may increase this probability. The
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probability of infection rapidly decreases when there are deleterious effects (d), which may be a powerful force against invasion by initially deleterious symbionts (or initially incompletely transmitted). Large negative effects on fecundity have been described (Hoffmann et al., 1988; Stevens and Wade, 1990). Possibilities for failures of infection spreading have also been investigated in the case of small populations newly infected by feminizing symbionts (Rigaud et al., 1992). It is also likely that the potential hosts will differ genetically in their sensitivity to Wolbachia infection and the associated alterations of reproduction. It is first necessary to understand how such differences evolve within a given species. No immediate nuclear effects have been detected in Nasonia (Breeuwer and Werren, 1993a). However, host resistance can appear in the long term, as observed in wild infected populations of Armadillidium, where resistance to the transmission of feminizing factors or their expression have been selected (Rigaud and Juchault, 1992, 1993). Populations of woodlice may nevertheless become extinct before the appearance of the resistance (see Population dynamics, above). Differences in sensitivity can also be demonstrated by interspecific transfers (Juchault et al., 1993; Boyle et al., 1993). For example, the success of the new infection depends on the fair transmission of the bacteria to their offspring by individual females. In woodlice, trans-specific transfers of feminizing Wolbachia between phylogenetically distant hosts could lead to failure of vertical transmission in the generation following the transfer (Rigaud and Juchault, 1995). Success also depends on the stability of the expression of the trait: incompatibility will depend upon bacterial density within individuals (Boyle et al., 1993; Breeuwer and Werren, 1993b: Rousset and de Stordeur, 1994; Solignac et al., 1994). The low probability of success of any infection implies that the rate of horizontal transfers is much higher than the rate of successful infections. Finally, a non-incompatible Wolbachia mutant could invade an infected population. It may be that the capacity to cause incompatibility in some hosts degenerates with time, and is maintained among all Wolbachia only through its advantage in infecting new hosts. An alternative possibility is the evolution of multiple incompatibilities within a host, as in Culex, but this situation is not well understood. Host factors that reduce the effects of infection could also be selected (Rousset et al., 1991). It thus appears that, even if horizontal transfers occur, several factors could lead to the loss of symbionts during the evolution of host-Wolbachia interactions. So what is responsible .f?~r the diversiO, of Wolbachia-arthropod interactions? Wolbachia have been very successful in a number of arthropod groups because of several properties. Because of their ability to disturb mitosis and/or by using specific host sexdetermining features, Wolbachia successfully distort their hosts' reproduction, a characteristic favouring their spread (see Consequences of Wolbachia-arthropod associations, above). They also must be available for many opportunities of horizontal transfer, so that the fraction of bacteria which is successful at the individual and population level still forms a large number of observable events. This supposes that these bacteria are able to adapt to the genetic and cellular environment of different hosts, such as insects and isopods. Wolbaehia are not exceptional in this respect, since many other microorganisms, such as Rickettsiales, are transmitted by several arthropods and infect vertebrates. The variability of effects produced by Wolbachia-arthropod interactions is probably a consequence of all
Diversity o f Wolbachia-arthropod interactions
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these factors, and the scattered distribution of symbionts could be due to total or partial losses of one of these characteristics.
Acknowledgements We are grateful to Pierre Juchault and Michel Raymond for their critical reading and comments.
References Artault, J.C. (1977) Contribution ~ l'~tude des garnitures chromosomiques chez quelques Crustac~s Isopodes. Thbse de Troisieme Cycle, Universit~ de Poitiers. Barr, A.R. (1982) Symbiont control of reproduction in Culex pipiens. In Recent Developments in the Genetics of Insect Disease Vectors (W.W.M. Steiner, W.J. Tabachnick, K.S. Rai and S. Narang, eds) pp. 153-8. Champaign, IL: Stipes Publishing Company. Binnington, K. and Hoffmann, A.A. (1989) Wolbachia-like organisms and cytoplasmic incompatibility in Drosophila simulans. J. Invertebr. Pathol. 54, 344-52. Boyle, L., O'Neill, S.L., Robertson, H. and Karr, T.L. (1993) Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260, 1796-9. Breeuwer, J.A.J. and Werren, J.H. (1990) Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature, 346, 558-60. Breeuwer, J.A.J. and Werren, J.H. (1993a) Effect of genotype on cytoplasmic incompatibility between two species of Nasonia. Heredity 70, 428-36. Breeuwer, J.A.J. and Werren, J.H. (1993b) Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics 135, 565-74. Breeuwer, J.A.J., Stouthamer, R., Barns, S.M., Pelletier, D A., Weisburg, W.G. and Werren, J.H. (1992) Phylogeny of cytoplasmic incompatibility microoganisms in the parasitoid wasp genus Nasonia (Hymenoptera, Pteromalidae) based on 16S ribosomal DNA sequences. Insect MoL Biol. 1, 25-36. Bull, J.J. (1983) Evolution of Sex Determining Mechanisms. Menlo Park, Benjamin/Cummings Publ. Co. Bulnheim, H.P. and Vavra, J. (1968) Infection by the microsporidian Octosporea effeminans and its sex determining influence in the amphipod Gammarus duebeni. J. Parasitol. 545, 241-8. Charniaux-Cotton, H. and Payen, G. (1985) Sexual Differentiation. In The Biology of Crustacea, Vol 9 (D.E. Bliss, ed.) pp. 217-99. Orlando: Academic press. Cioran, E.M. (1973) De l'inconvdnient d'Otre nd. Paris: Gallimard. Cook, J.M. (1993) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71, 421-35. Fine, P.E.M. (1978) On the dynamics of symbiote-dependent cytoplasmic incompatibility in culicine mosquitoes. J. Invertebr Pathol. 30, 10-18. Ghelelovitch, S. (1952) Sur le d6terminisme g6n6tique de la st6rilit6 dans les croisements entre diff6rentes souches de Culex autogenicus Roubaud. C. R. Acad. Sci. 234, 2386-8. Gilbert, S.F. (1991) Developmental Biology, 3rd edn. Sunderland, MA: Sinauer. Ginsburger-Vogel, T. and Desportes, I. (1979) Structure and biology of Marteilia sp in the amphipod Orchestia gammarellus. Mar. Fish. Rev. 41, 3-7. Grandjean, F., Rigaud, T., Raimond, R., Juchault, P. and Souty-Grosset, C. (1993) Mitochondrial DNA polymorphism and feminizing sex factors dynamics in a natural population of Armadillidium vulgare (Crustacea, Isopoda). Genetica 92, 55~60. Hastings, I.M. (1994) Selfish DNA as a method of pest control. Philos. Trans. R. Soc. Lond. B 344, 31-24.
1010
Rigaud and Rousset
Hertig, M. (1936) The rickettsia, Wolbachia pipientis. (gen. et sp. n.) and associated inclusions of the mosquito, Culex pipiens. Parasitology 28, 453-86. Hoffmann, A.A. (1988) Partial cytoplasmic incompatibility between two Australian populations of Drosophila melanogaster. Entomol Exp. Appl. 48, 61-7. Hoffmann, A.A, Turelli, M. and Simmons, G.M. (1986) Unidirectional incompatibility between populations of Drosophila simulans. Evolution 40, 692-701. Hoffmann, A.A., Turelli, M. and Harshman, L.H. (1988) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetic~s 126, 933-48. Howard, R.S. and Lively, C.M. (1994) Parasitism, mutation accumulation and the maintenance of sex. Nature 367, 554-7. Hsiao, C. and Hsiao, T.H. (1985) Rickettsia as the cause of cytoplasmic incompatibility in the alfalfa weevil, Hypera positica. J. Invertebr. Pathol. 45, 244-6. Hurst L.D. (1993) The incidences, mechanisms and evolution of cytoplasmic sex ratio distorters in animals. Biol. Rev. 68, 121-93. Jost, E. (1971) Meiosis in the male of Culex pipiens and Aedes albopictus and fertilization in the Culex-pipiens complex. Can. J. Genet. Cytol. 13, 237-50. Juchault, P. and Legrand, J.J. (1989) Sex determination and monogeny in terrestrial Isopods Armadillidium vulgate (Latreille, 1804) and Armadillidium nasatum (Budde-Lund, 1885L Monitore Zool. Ital. (N.S.) Monogr. 4, 359-75. Juchault, P. and Mocquard, J.P. (1993) Transfer of a parasitic sex factor to the nuclear genome of the host: a hyopothesis on the evolution of sex determining mechanisms in the terrestrial Isopod Armadillidium vulgare Latr. J. Evol. Biol. 6, 511-28. Juchault, P., Legrand J.J. and Martin, G. (1974) Action intersl~cifique du facteur 6pig6n6tique f6minisant responsable de la th61yg6nie et de l'intersexualit6 du Cmstac6 Armadillidium vulgate (Isopode Oniscoide). Ann. Embryo. Morphogen. 7, 265-76. Juchault, P., Rigaud, T. Mocquard, J.P. (1992) Evolution of sex determining mechanisms in a wild population of Armadillidium vulgare Latr. (Crustacea, Isopoda). competition between two feminizing parasitic factors. Heredity 69, 382-90. Juchault, P., Rigaud, T. and Mocquard, J.P. (1993) Evolution of sex determination and sex ratio variability in wild populations of ArmadiUidium vulgare Latr. (Crustacea, Isopoda): Acta Oecologica 14, 547-62. Juchault, P., Frelon, M., Bouchon, D. and Rigaud, T.(1994) New evidence for feminizing bacteria in terrestrial isopods: evolutionary implications. C. R. Acad. Sci. Paris Life Sciences, 317, 225-30. Kambhampati, S., Rai, K.S. and Burgun, S.J. (1993) Unidirectional cytoplasmic incompatibility in the mosquito, Aedes albopictus. Evolution 47 673-7. Kellen, W., Hoffmann, D. and Kwock, R. (1981) Wolbachia sp. (Rickettsiales: Rickettsiaceae) a symbiont of the almond moth, Ephestia cautella: ultrastructure and influence on host fertility. J. lnvertebr PathoI. 37, 273-83. Laven, H. (1967) Speciation and evolution in Culex pipiens. In Genetics of Insect Vectors of Disease (J. Wright and R. Pal, eds) pp. 251-75. Elsevier. Legner, E.F. (1985) Effects of scheduled high temperature on male production in thelytokous Muscidifurax uniraptor (Hymenoptera. Pteromalidae). Can. Entomol. 117, 383-9. Legrand, J.J. and Juchault, P. (1984) Nouvelles donn6es sur le d&erminisme g6n6tique et 6pig6n6tique de la monog6nie chez le crustac6 isopode terrestre Armadillidium vulgare Latr. G~ndt. S~l. Evol. 16, 57-84. Legrand, J.J. and Juchault, P. (1986) R61e des bact6des symbiotiques clans l'intersexualit6, la monog6nie et la sp6ciation chez des Crustac6s Oniscoides. Boll. Zool. 53, 161-72. Legrand, J.J., Juchault, P. and Martin, G. (1985) Inoculation chez la femelle du Crustac60niscoide Porcellio dilatatus Brandt d'une bact6rie symbiote caract6ristique de la sous esp~ce P.d. petiti,
Diversity o f Wolbachia-arthropod interactions
1011
et ses constquences sur l'issue du croisement des deux sous esI~ces. C.R. Acad. Sci. Paris 300, 147-50. Legrand J.J., Legrand-Hamelin, E. and Juchault, P. (1987) Sex determination in Crustacea. Biol. Rev. 62, 439-70. Luck, R.F., Stouthamer, R. Nunney, L.P. (1993) Sex determination and sex ratio patterns in parasitic Hymenoptera. In Evolution and Diversity of Sex Ratio in Insects and Mites (D.L. Wrensch and M.A. Ebbert, eds) pp. 442-76. New York: Chapman & Hall. Martin, G., Juchault, P. and Legrand, J.J. (1973) Mise en 6vidence d'un micro-organisme intracytoplasmique symbiote de l'Onisctide Armadillidium vulgare L., dont la prtsence accompagne l'intersexualit6 ou la ftminisation totale des turtles gtnttiques de la lignte thtlyg~ne. C. R. Acad. Sci. Paris 276, 2213-6. Martin, G., Gruppe, S.G., Laulier, M., Bouchon, D., Rigaud, T. and Juchault, P. (1994) Evidence for Wolbachia spp. in the estuarine isopod Sphaeroma rugicauda (Crustacea): a likely cytoplasmic sex ratio distorter. Endocytobiosis Cell Res. 10, 215-25. Maynard-Smith, J. (1988) The evolution of recombination. In The Evolution of Sex (R.E. Michod and B,R. Levin, eds) pp. 106-25. Sunderland, MA: Sinauer. Minchella, D.J. and Scott, M.E. (1991) Parasitism: a criptic determinant of animal community structure. Trends Ecol. Evol. 6, 250-4. Montchamp-Moreau, C., Ferveur, J.F. and Jacques, M. (1991) Geographic disibution and inheritance of three cytoplasmic types in Drosophila simulans. Genetics 129, 399--407. Noda, H. (1984) Cytoplasmic incompatibility in a rice planthoper. J Hered. 75, 345-8. Ochman, H. and Wilson, A.C. (1987) Evolution in bacteria, evidence for a universal substitution rate in cellular genomes. J. molec Evol. 26, 74-86. O'Neill, S.L. (1989) Cytoplasmic symbionts in Tribolium confusum. J. Invertebr. Pathol. 53, 132-4. O Neill S.L. and Karr, T.M. (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348, 178-80. O'Neill, S.L., Giordano, R., Colbert, A.M.E., Karr, T.L. and Robertson, H.M. (1992) Phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl Acad. Sci. USA 89, 2699-702. Raymond, M., Callaghan, A., Fort, P. and Pasteur, N. (1991) Worldwide migration of amplified insecticide resistance genes in mosquitoes. Nature 350, 151-3. Rigaud, T. and Juchault, P. (1992) Genetic control of the vertical transmission of a cytoplasmic sex factor in Armadillidium vulgare Latr. (Crustacea, Oniscidea). Heredity 68, 47-52. Rigaud, T. and Juchault, P. (1993) Conflict between feminizing sex ratio distorters and an autosomal masculinizing gene in the terrestrial isopod Armadillidium vulgare Latr. Genetics 133, 247-52. Rigaud, T. and Juchault, P. (1995) Success and failure of horizontal transfers of feminizing Wolbachia endosymbionts in woodlice. J. Evol. Biol. 8, 249-55. Rigaud, T., Souty-Grosset, C., Raimond, R., Mocquard, J.P. and Juchault, P. (1991a) Feminizing endocytobiosis in the terrestrial crustacean Armadillidium vulgare Latr. (Isopoda). recent acquisitions. Endocytobiosis Cell Res. 7, 259-73. Rigaud, T., Juchault, P. and Mocquard, J.P. (1991b) Experimental study of temperature effects on the sex ratio of broods in terrestrial Crustacea Armadillidium vulgare Latr. Possible implications in natural populations. J. Evol. Biol. 4, 603-17. Rigaud, T. Mocquard, .P. and Juchault, P. (1992) The spread of parasitic sex factors in populations of Armadillidium vulgare Latr (crustacea, Oniscidea): effects on sex ratio. Gen. Sel. Evol. 24, 3-18. Rousset, F. and de Stordeur, E. (1994) Properties of Drosophila simulans strains experimentally infected by different clones of the bacterium Wolbachia. Heredity 72, 325-31.
1012
Rigaud and Rousset
Rousset, F. ~,nd Raymond, M. (1991) Cytoplasmic incompatibility in Insects: why sterilize females'? Trends Ecol. Evol. 6, 54-7. Rousset, F. and Solignac, M. (1995) Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc. Natl. Acad. Sci. USA 92, 6389-93. Rousset, F., Raymond, M. and Kjellberg, F (1991) Cytoplasmic incompatibility in the mosquito Culex pipiens: how to explain a cytotype polymorphism? J. EvoI. Biol. 4, 69-82. Rousset, F., Vautrin, D. and Solignac, M. (1992a) Molecular identification of Wolbachia. the agent of cytoplasmic incompatibility in Drosophila simulans, and variation in relation to host mitochondrial types. Proc. Roy. Soc. Lond. B 247, 163-8. Rousset, F., Bouchon, D., Pintureau, B., Juchault, P. and Solignac, M. ¢1992b) Wolbaehia endosymbionts responsible for various alterations of sexuality in Arthropods. Proc. Roy. Soc. Lond. B 250, 91-8. Solignac, M., Vautrin, D. and Rousset, F. (1994) Widespread occurrence of Wolbachia and partial cytoplasmic incompatibility in Drosophila melanogaster. C.R. Acad. Sci, Paris Life Scieneex 317, 461-70. Souty-Grosset, C., Raimond, R. and Tourte, M. (1992) D6terminisme 6pig6n6tique du sexe et divergence g6n6tique de I'ADN mitochondrial chez Armadillidium vulgare Latr. (Crustac6, Oniscoide): variabilit6 inter et intrapopulation. C.R. Acad. Sci. Paris 314, 119-25. Stevens. L. and Wade, M.J. (1990) Cytoplasmically inherited reproductive incompatibility in Tribolium flour beetles: the rate of spread and effect on population size. Genetics 124. 367-72. Stevens, L. and Wicldow, D.T. (1992) Multispecies interactions affect cytoplasmic incompatibilities, in Tribolium flour beetles. Am. Nat. 140, 642-53. Stouthamer, R. and Kazmer, D.J. (1994) Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 73. 317--27. Stouthamer, R. and Luck, R.F, (1993) Influence of microbe-associated parthenogenesis on the fecundity of Trichogramma deion and Triehogramma pretiosum. Ent. Exp. Appl. 67, 183-92. Stouthamer, R., Luck, R.F. and Hamilton, W.D. (1990) Antibiotics cause parthenogenetic Trichogramma (Hymenoptera/Trichogrammatidae) to revert to sex. Proc. Natl Acad. Sci. USA 87, 2424-7. Stouthamer, R., Breeuwer, J.A.J., Luck, R.F. and Werren, J.H. (1993) Molecular identification of microorganisms associated with parthenogenesis. Nature, 361 66-8. Taylor, D.R. (1990) Evolutionary consequences of cytoplasmic sex ratio distorters. Evol. Ecol. 4, 235--48. Trpis, M., Perrone, J.B., Reissig, M. and Parker, K.L. (1981) Control of cytoplasmic incompatibility in the Aedes scutellaris complex. J. Hered. 72, 313-7. Turelli M., Hoffmann A.A. (1992) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353, 440-2, Turelli, M., Hoffmann, A.A. and McKechnie, S.W. (1992) Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics 132, 713-23 Vandel, A. (1941) Recherches sur la g6n6tique et la sexualit6 des Isopodes terrestres. VI. Les ph6nom~nes de monog6nie chez les Onisco'ides. Bull. Biol. Fr. Bel. 75, 316-63. Wade, M.J. and Stevens, L. (1985) Microorganism mediated reproductive isolation in flour beetle (genus Tribolium). Science 227, 527-8. Weiss, E. (1974) Wolbachia. In Bergey's Manual of Determinative Bacteriology (R.E. Buchaman and N.E. Gobbons, eds), pp. 898-900, Baltimore: Williams and Wilkins. Wilkins, A.S. (1993) Genetic' Analysis of Animal Development, 2nd edn. New York: Wiley-Liss. Wright J. and Barr, A.R. (1981) Wolbachia and the normal and incompatible eggs of Aede~ polynesiensis (Diptera: Culicidae). J. lnvertebr. Pathol. 38, 409-18. Yen, J.H. and Barr, A.R. (1971) New hypothesis on the cause of cytoplasmic incompatibility in Culex pipiens L. Nature 232, 657-8.
Diversi~ of Wolbachia-arthropod interactions
1013
Zchori-Dein, E., Roush, R.T. and Hunter, M.S. (1992) Male production induced by antibiotic treatment in Encarsiaformosa (Hymenoptera: Aphelinidae), an asexual species. Experientia 48, 102-5. Zchori-Fein, E., Rosen, D. and Roush, R.T. (1994) Microorganisms associated with thelytoky in Aphytis lignanensis Compere (Hymenoptera: Aphelinidae). Int. J. Insect Morphol. Embryol. 23, 169-72.
