5.10.4. Reproductive effects of endosymbionts
Wolbachia, an intracellular bacterium discovered first infecting the ovaries of Culex pipiens mosquitoes, causes some inter-populational (intraspecific) matings to produce inviable embryos. Such crosses, in which embryos abort before hatching, could be returned to viability after treatment of the parents with antibiotic — thus implicating the microorganism with the sterility. This phenomenon, termed cytoplasmic or reproductive incompatibility, now has been demonstrated in a very wide range of invertebrates that host many “strains” of Wolbachia. Surveys have suggested that up to 76% of insect species may be infected. Wolbachia is transferred vertically (inherited by offspring from the mother via the egg), and causes several different but related effects. Specific effects include the following:
- Cytoplasmic (reproductive) incompatibility, with directionality varying according to whether one, the other, or both sexes of partners are infected, and with which strain. Unidirectional incompatibility typically involves an infected male and uninfected female, with the reciprocal cross (uninfected male with infected female) being compatible (producing viable offspring). Bidirectional incompatibility usually involves both partners being infected with different strains of Wolbachia and no viable offspring are produced from any mating.
- Parthenogenesis, or sex ratio bias to the diploid sex (usually female) in insects with haplodiploid genetic systems (sections 5.6, 12.2, & 12.4.1). In the parasitic wasps (Trichogramma) studied this involves infected females that produce only fertile female offspring. The mechanism is usually gamete duplication, involving disruption of meiotic chromosomal segregation such that the nucleus of an unfertilized, Wolbachia-infected egg contains two sets of identical chromosomes (diploidy), producing a female. Normal sex ratios are restored by treatment of parents with antibiotics, or by development at elevated temperature, to which Wolbachia is sensitive.
- Feminization, the conversion of genetic males into functional females, perhaps caused by specific inhibitions of male-determiner genes, thus far only observed in terrestrial isopods and two Lepidoptera species, but perhaps yet to be discovered in other arthropods.
The strategy of Wolbachia can be viewed as reproductive parasitism (section 3.6.5), in which the bacterium manipulates its host into producing an imbalance of female offspring (this being the sex responsible for the vertical transmission of the infection), compared with uninfected hosts. Only in a very few cases have infections been shown to benefit the insect host, primarily via enhanced fecundity. Certainly, with evidence derived from phylogenies of Wolbachia and their host, Wolbachia often has been transferred horizontally between unrelated hosts, and no coevolution is apparent.
Although Wolbachia is now the best studied system of a sex-ratio modifying organism, there are other somewhat similar cytoplasm-dwelling organisms, with the most extreme sex-ratio distorters known as male-killers. This phenomenon of male lethality is known across at least five orders of insects, associated with a range of maternally inherited, symbiotic—infectious causative organisms, from bacteria to viruses, and microsporidia. Each acquisition seems to be independent, and others are suspected to exist. Certainly, if parthenogenesis often involves such associations, many such interactions remain to be discovered. Furthermore, much remains to be learned about the effects of insect age, remating frequency, and temperature on the expression and transmission of this bacterium. There is also an intriguing case involving the parasitic wasp Asobara tabida (Braconidae) in which the elimination of Wolbachia by antibiotics causes the inhibition of egg production rendering the wasps infertile. Such obligatory infection with Wolbachia also occurs in filarial nematodes (section 15.5.5).