Inherited microorganisms and sex determination of arthropod hosts
Different animal species have various mechanisms for controlling differentiation between males and females, commonly involving 'sex factors' coded for by genes on sex chromosomes. An interesting variation on this is seen in certain crustaceans, in which sex determination is influenced not only by sex chromosomes but also by the presence or absence of intracellular symbionts such as the bacterium Wolbachia.
For example, in the woodlouse Armadillidium vulgare (an isopod crustacean), females infected with Wolbachia symbionts produce a disproportionately high number of female offspring, whereas uninfected individuals produce offspring with the normal 1:1 sex ratio that would be expected from Mendelian genetics. (Gender in these woodlice is dictated by the presence of Z and W sex chromosomes: ZZ in males and ZW in females.) It has been shown that this is because the Wolbachia symbionts exert a feminising effect upon male A. vulgare, turning individuals that are genetically male into phenotypic females. This sex-ratio bias disappears if the woodlice are reared at high temperatures of around 30°C, since Wolbachia are eliminated from host tissues at this temperature. In a small proportion of genotypically-male, Wolbachia-infected individuals, feminisation is incomplete and results in the development of sterile, intersexual animals possessing features of both sexes.
Intracellular symbionts such as Wolbachia gain an obvious genetic advantage by converting males into females, because the symbionts are transmitted primarily down the maternal line (from mother to offspring). From Wolbachia's perspective, a male host represents an evolutionary 'dead end', and the ability to convert male hosts into female ones confers a strong selective advantage.
This kind of 'cytoplasmic sex determination' involving intracellular symbionts is found in various other crustacean families. Some amphipods, for example, are feminised by the presence of certain protists (microsporidia or paramixydia) in their cells. However, cytoplasmic sex determination is not known in any other animal group (with the possible exception of certain insects and aphids), and it has therefore been suggested that the sex-determining machinery of isopod and amphipod crustaceans is uniquely vulnerable to being hijacked by symbionts.
In A. vulgare, 'maleness' is conferred by male gene(s) on the Z chromosome, which direct the development of an androgenic gland synthesising male hormone. In the absence of these, an individual will develop as a female. The W chromosome in normal females carries a 'female gene' that inhibits the expression of the male gene(s). (The Z and W chromosomes of A. vulgare are believed to be identical except for the presence of the female gene on the W chromosome.) Under this system, it is relatively easy for a symbiont to bring about feminisation of a male individual, either genetically by mimicking the action of the female gene and suppressing the male gene(s), or physiologically by causing degradation of the androgenic gland. Wolbachia is capable of acting through both these mechanisms.
In natural populations of A. vulgare, Wolbachia is relatively rare. This is perhaps because the symbiont imposes a fitness cost upon its host, either by decreasing the host's fecundity (there is evidence for this in some situations) or by causing the production of a certain number of sterile intersexual offspring. We might also speculate that in some isolated populations, Wolbachia has been the victim of its own success, driving its host population (and consequently itself) to extinction by completely eliminating the males necessary for reproduction.
An intriguing twist to the story is the discovery of female-biased sex ratios, similar to those conferred by Wolbachia, in strains of A. vulgare that do not carry such symbionts. This has been ascribed to the presence of a feminising 'f factor' (possibly a self-replicating transposable genetic element), exhibiting non-Mendelian inheritance, in affected lineages. The spontaneous appearance of an f factor has been observed in an A. vulgare lineage previously infected with Wolbachia, suggesting that the f factor might be a chunk of bacterial DNA that became incorporated into the nuclear genome of the woodlouse, although there are other possible explanations for its origin.
Feminising factors that distort the sex ratio lead to intragenomic conflict, since Fisherian selection acting on the autosomal genes of the host favours an overall sex ratio of 1:1. This can result in selection for a male-biased sex ratio in lineages uninfected by the symbiont (to compensate for the excess of females), or lead to the evolution of 'male restorer' genes that allow infected individuals to resist the feminising effect exerted by their symbionts.
In some lines of A. vulgare, the f factor has been observed becoming incorporated into the male (Z) chromosome, effectively creating a new female (W) chromosome. This raises the possibility that the evolution of sex determination in these crustaceans might proceed in a circular fashion. In the first instance, woodlice with normal chromosomal sex determination become infected with Wolbachia. In later generations, Wolbachia is lost but leaves behind an element of its DNA - the feminising f factor - in the host genome. This f factor is then integrated into one of the host's Z chromosomes, creating a new W-like chromosome, resulting once more in purely chromosomal sex determination and completing the cycle. This continuing renewal of the sex chromosomes might explain why the Z and W chromosomes in A. vulgare remain relatively alike and the evolution of chromosomal sex determination in these isopods has not proceeded to the same extreme as in organisms such as mammals, in which one sex chromosome has become highly reduced in contrast to the other.
The genetics of organisms such as A. vulgare, in which intracellular symbionts play a role in controlling sex differentiation, thus provide a fascinating insight into the ways in which different sex determination mechanisms can be evolved and maintained.
This essay is a summary of Rigaud, T. (1997), "Inherited microorganisms and sex determination of arthropod hosts", in Influential Passengers (ed. S. O'Neil, A.A. Hoffmann & J.W. Werren), pp. 81-101.
This was originally written as a university biology essay