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Wolbachia are a common type of intracellular bacteria. They are a type of Selfish Genetic Element which are prevalent in forming symbiotic relationships with arthropods and nematodes (1). By infecting the host eggs they are transmitted vertically through the population. In order to do this effectively they use a range of reproductive manipulations such as; feminization, parthenogenesis, male killing and sperm-egg incompatibility or cytoplasmic incompatibility. All of which increase the frequency of infected females. The most common Wolbachia - induced phenotype is cytoplasmic incompatibility (2) and it has been described in arachnids, isopods and insect orders(1). Here the focus is on the proposed mechanisms by which cytoplasmic incompatibility (Ci) is achieved, the costs and benefits associated with infection, the evolutionary implications and the use of Wolbachia as an aid to biocontrol.
Cytoplasmic Incompatibility occurs when sperm from Wolbachia - infected males is incompatible with eggs which either do not contain the same Wolbachia strain (Bidirectional) or are not infected at all (Unidirectional)(3). Incompatible crosses which form haploids in normally diploid organisms, observed in flies, wasps and mosquitoes, result in embryonic lethality. Whereas in haplodiploids, haploidy can result in normal male development (1).
When the infected egg and sperm are compatible all offspring produced contain the Wolbachia infection. Compatible pairings can either be an infected female and uninfected male or infected female and infected male. As cytoplasm is inherited from the female infected females always produce infected offspring (3). Infected eggs are always compatible with uninfected sperm, no exception has been found to date (4). As male cytoplasm is lost during spermatogenesis an infected male cannot pass on the infection and is therefore a 'dead-end' to the Wolbachia (Figure 1).
The sperm is used to indirectly disrupt the ability of uninfected females to reproduce as sperm is conditionally sterile (2). When an infected sperm fertilises an uninfected egg no offspring are produced. Uninfected females are then only able to produce offspring with uninfected males, therefore the infection is spread through the population as effectively double the amount of infected offspring are produced in comparison to uninfected offspring (Figure 1).
How does Cytoplasmic Incompatibility occur?
Cytoplasmic Incompatibility works through the interaction of two components; Sperm chromosome modification by Wolbachia (Selfish Genetic Element) during spermatogenesis (possibly through chromatin binding proteins (3)) and rescue of this modification in the embryos infected with the same strain. Without this 'rescue' modification the sperm and egg remain incompatible and no offspring would be produced (3). This process occurs during the early stages of mitosis. The chromosomes of the infected modified sperm remain condensed, are unable to line up at the first metaphase plate and are unable to separate correctly (Figure 2). Consequentially a lethal haploid is produced. When a rescue occurs the sperm's modified chromosomes are able to uncondense, the actual molecular mechanisms for this are unknown, despite considerable work on the effect and various proposed mechanisms (4).
There are three proposed mechanisms for the actions of modification and rescue; the 'Lock and Key' Hypothesis, the 'Titration-restitution' or 'Sink' hypothesis and the 'Slow Motion' Hypothesis.
The 'Lock and Key' Hypothesis
The 'Lock and Key' Hypothesis involves the Wolbachia producing a substance which 'Locks' the sperm chromosomal material in place. Once fertilisation occurs the Wolbachia-infected egg produces the 'Key' which removes the 'Lock' thus enabling fertilisation to occur and embryogenesis to continue. However, there has been no molecular evidence for this (4).
The 'Lock and Key' Model. A) The cell is infected with the bacteria (White). The bacteria produces a substance (Red) which binds to the paternal chromosomal structures (Black) locking it in place. B) During spermatogenesis the bacteria are lost in the waste-bag (w.b). C) The sperm fertilizes the uninfected egg. D) An incompatible cross is formed and the paternal chromosomal material is unable to uncondense. E) In the infected egg the bacteria produces the 'Key' substance (Green) which removes the 'Lock'. F) Normal mitosis resumes in the compatible cross (4).
The 'Titration-restitution' hypothesis
It is suggested that the Wolbachia removes some proteins from the paternal chromosome important for supercoiling. When the sperm fertilises an infected egg the proteins are returned by the resident Wolbachia infection (4). Without the returning of these proteins the paternal chromosome is unable to complete normal mitosis. This was hypothesised as a result of experiments with anti-Wolbachia antibodies where by anti-Wolbachia antibodies associated strongly with the Wolbachia- infected egg but not with the paternal chromosomal material (4). This association antibody association is also faintly present in uninfected male chromosomes. Interestingly, these antibodies also associated strongly with Histone-like proteins (5).
The 'Titration-restitution' hypothesis. A) In the bacteria (White) infected cell, proteins (Green) are removed from the condensed chromosomal structure (Black). B) During spermatogenesis the proteins and bacteria are lost in the 'waste- bag' (w.b). C) The sperm fertilises an uninfected egg. D) The chromosome cannot be 'rescued' and mitosis cannot function correctly. E) The sperm fertilises an infected egg and the bacteria are able to 'rescue' the chromosome through producing the correct protein. F) The chromosomes split through mitosis correctly (4).
The 'Slow-motion' Model
In this model the infected paternal chromosome is not prevented from condensing but is slightly delayed from doing so. Therefore, the synchronisation of the uninfected maternal to infected paternal mitosis is not correct thus making them incompatible (4). Experiments performed by Callaini et al and Tram and Sullivan propose this delay as Callaini et al showed a paternal anaphase-like phase after the maternal anaphase (6) and Tram and Sullivan showed a delay in the nuclear envelope breakdown which occurs at the beginning of mitosis (7).
It is speculated that this mechanism is rescued not by the manipulation of the paternal chromosomal material but the maternal. It is therefore proposed that this 'slowing down' factor is produced in the egg after fertilisation. With both zygotes containing the factor they then become synchronised and normal mitosis can occur (4).
The 'Slow-motion' Model A) During spermatogenesis an infected male Wolbachia (White) produce the slowing down factor (Red) and attach it to the chromatid (Black). B) The bacteria are lost in the 'waste-bag' (w.b). C) The modified sperm fertilises an uninfected egg. D) As the slowing down factor is not present in the uninfected egg mitosis is unsynchronised and they are incompatible. E) The sperm fertilises an infected egg which is also producing the slowing down factor. F) Mitosis is synchronised and so effective mitosis can take place (4).
The 'Modification' and 'Rescue' functions
These 'Modification' (Mod) and 'Rescue' (Resc) functions can be present within wildtype Wolbachia strains independently. This creates four distinct phenotypes which are possible; Mod+ Resc+ ('Invasive'), Mod+ Resc- ('Suicide'), Mod- Resc+ ('Defensive') and Mod- Resc- ('Helpless'). All but the Mod+ Resc - 'suicide' phenotype have been described within wildtype strains, although the theory cannot discount it (4). Alternative strains of Wolbachia can contain different modification-rescue mechanisms as indicated by crossing data (1).
It is suggested that this is possible that the modification and rescue functions are present in different genes, making the 'Lock and Key' hypothesis the most likely as with the addition of this suggestion (as well as others) this hypothesis the most parsimonious (4).
However, extensive study into the mechanism of cytoplasmic incompatibility has not yet revealed to true mechanism by which it works (1).
Bidirectional Cytoplasmic Incompatibility
An infected female which contains one type of bacterial strain is incompatible with an infected male which contains another. This is termed bidirectional incompatibility as two different stains of bacteria work to control the reproductive success of the population (Figure - 6) (4).
However, recently Zabalou, S. et al. (2008) showed that when different strains of Wolbachia from different Drosophilia species were used to infect a common genotype (Drosophilia simulans) these different strains were able to either fully partically rescue one another using complex interactions. However, some pairings were not able to rescue one another at all. Therefore, it was suggested that alternative Wolbachia strains can have more than one modificaition-rescue type (1,8).
Strengthening this conclusion is work performed by Poinsot, D. et al (1998) where D.simulans females were artificially infected with the Wolbachia wMel strain which is normally found in D.melanogaster. These females partially rescued (only 25%-30% die) males infected with the normal D.simulans Wolbachia strain, wRi. In addition to this wRi infected females were capably of fully rescuing wMel males (9).
Bidirectional incomptatibility, however, is suggested to be less common in nature (1).
Bidirectional Cytoplasmic Incompatibility. Crosses between strain one Wolbachia infected (Red) hosts and strain two Wolbachia infected (Blue) Hosts (20).
Other factors which influence expression of Cytoplasmic Incompatibility
Other factors such as; bacterial strain, host genotype and bacterial density have been put forward as influencers to the strength and direction of cytoplasmic incompatibility (10).
Evidence for the influence of host genotype was found by Zabalou, S. et al. (2008) as one Wolbachia variant was found which was unable to fully rescue the modification that it induced after transfer into an alternative host species. This phenotype therefore was converted to a 'suicide' phenotype as a result of this transinfection (1,8).
This work by Zabalou, s. et al suggests complicated mechanisms by which host and parasite genotypes work in order to produce an effective relationship. It seems as though the genotype of the Wolbachia strain as well as the genotype of the host strain work in a complex relationship to achieve a range of out comes.
Costs and Benefits to the Selfish Genetic Element and to the Host
As previously discussed Wolbachia infection manipulates their female host reproductively by preventing uninfected females from producing offspring from infected males thus indirectly enabling infected female hosts to produce more offspring in comparison with their uninfected counter-parts (11, 12).
Montenegro.H, et al (2006) established the fitness effects of Wolbachia on the female Drosophilia melanogaster host by comparing larval competitiveness and adult fecundity of infected and uninfected hosts. There were no benefits or cost found using these measures for the infection of the host. Montenegro. H, et al, therefore, proposed that the bacteria probably have alternative fitness effects in order for them to be so common within host populations (11).
Due to their vertical transmission Wolbachia have previously been found to form mutualistic relationships with Nematodes whereby a concordance of phylogeny is found as host and symbiont are so closely linked they have evolved to provide benefits for one another (1). However, Arthropod hosts do not show the same concordance (1). Although it would be prudent for the bacteria not to harm the host, as their fitness is strongly correlated, a 'trade-off' can occur between bacterial titre and strength of reproductive manipulation and vertical transmission efficiency (11). This 'trade - off' enables the bacteria to produce an optimal phenotype where it is unnecessary to match the hosts optimal phenotype (11). Therefore a range of interactions can occur from directly deleterious (found in D.bifasciata and D. willistoni) to neutral (D. melanogaster) to beneficial (D. melanogaster and Aeddes aldopictus) to the host.
Although fitness benefits were not found by Montenegro.H, et al, Hoffmann, Hercus and Dagher (1998) believe that Wolbachia is so prevalent in Austrailian populations of D.melanogaster due to direct fitness effects. This is because of the weak, absent and imperfect transmission of cytoplasmic incompatibility within their field experiments (11). And benefits such as increased life span, resistance to RNA viral infections, fecundity and egg-to-adult viability have been found in some laboratory Drosophila host strains (21) suggesting that these benefits could exist in the wild.
Benefits to wild hosts have yet to be found conclusively and the continuation of no or deletious effects are continuously being described. The explanation of this is that although Wolbachia is maternally inherited some horizontal transmission must occur between hosts (12). Conclusive evidence for this where the Adm Wolbachia strain has been found in 3 orders of insects, the hymenopterans, the dipterans and lipidopterans with virtually no differences in sequence between the genomes of the strains (22). Such movement has been also documented in the laboratory. This horizontal transmission would enable this bacteria to take advantage of the host without completely relying on it for its transmission. Horizontal transmission is necessary to maintain the Ci phenotype within the bacteria as without it the phenotype would be lost through competition with non-expressing Wolbachia strains (1, 10, 11, 12).
Wolbachia are capable of promoting speciation in their host species (13) by decreasing gene flow between different populations therefore causing isolation through limiting the combination of sperm-egg compatibility and enabling speciation to occur by permitting genetic divergence (1, 14).
Bidirectional cytoplasmic incompatibility is of particular interest within this subject as theory indicates that it creates opportunities for divergence without substantial gene flow. However, as earlier stated bidirectional Ci is less common in nature and so less likely to contribute to large changes within species (1). Theoretically unidirectional Ci is also suggested to be an unlikely contributor to speciation as isolation caused by this method would be easily disrupted by migration (1).
This view, however, has been disputed by D. Subquinari genetic evidence which shows that a decrease in Wolbachia fertility cost and the development of imperfect transmission can enable the maintenance of genetic divergence (1). As well as this
In connection with this Telschow, Hammerstein and Werren (2005) show through comparison between bidirectional Ci, single locus nuclear genetic incompatibilities (Ni) and eipstatic Ni, bidirectional Ci induces premating isolation faster than epistatic Ni and that bidirectional Ci and single locus Ni are much more stable, enabling stronger migration rates than in epistatic Ni. This, therefore, supports the idea that bidirectional Ci has the capability to induce speciation (13).
As a consequence of the unfair advantage given to infected females and the increase in non-viable fertilization events caused by incompatible crosses genetic divergence is reduced in connection with a decrease in population size. If the population continues to reduce and becomes too extreme a local extinction event can occur (15).
How the Ci-inducing phenotype evolved and new strains arise within Wolbachia is not yet completely understood. This is most likely due to the unresolved understanding of the mechanism of how it is controlled.
The complete genome of the Ci-inducing wMel strain of Wolbachia as recently become available and other Ci-inducing strains are currently in process or assembled. By comparing these genomes it important information will no doubt come to light regarding the evolution of this function within these bacteria (1).
The Use of Wolbachia in Biocontrol
As Cytoplasmic Incompatibility has the capability to decrease population size when introduced to a population of pests, it can therefore be used as pest control in order to drive down the population (1, 14, 16). The release of hosts infected with Ci-inducing Wolbachia will either, reduce the population, maintain it at low levels or eliminate it (17).
When released into the population the infection status of the native population must be known. The population must either contain no alternative infection so that unidirectional incompatibility can occur or the alternative infection which reside in the pest population must be know in order for bidirectional incompatibility to occur (18).
In the 1960's this method of pest control was used to successful eradicate Culex pipiens, the nematode worm, in two villages in Burma. Although the researchers did not know that this was through the action of Wolbachia incompatibility reached 100% (19).
Recently work done in the laboratory by Zabalou et al. (2004b) has shown that populations of Ceratitis capitata can be controlled through Ci-inducing Wolbachia (19).
Wolbachia is a reproductive parasite which manipulates its host through a variety of functions including cytoplasmic incompatibility. Through cytoplasmic incompatibility Wolbachia has the ability to control the numbers of infected offspring within populations thus causing its spread throughout the host population (1).
The mechanism by which this process is undertaken is not yet completely understood, however, various models have been proposed in order to best explain findings involved in the transmission and manipulation of Ci (4). Unfortunately without the complete understanding of the mechanisms involved understanding of how this mechanism could have evolved within Wolbachia remains indefinable (14).
Perhaps work involving understanding the histone-like proteins found in the Titration-restitution model. As they seem to suggest that it is the way in which the chromosomal material condenses which effect the modification model.
Wolbachia, through bidirectional incompatibility, is able to drive speciation within host populations. This is achieved by creating genetic isolation and stabilising divergence (13).
No doubt work will continue in order to resolve the mysteries surrounding cytoplasmic incompatibility as its applications in biocontrol could be lucrative.
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