Case Notes 10

We tend to imagine the genome as a relatively discrete entity -- large, complicated, variously mutable and recombined through sex, yes, but at least something for which we can draw boundaries to say what is part of it and what isn't. A bacterial infection, for example, is clearly not part of it, just a parasite coming along for the ride. Except that, in various interesting cases, things are not that clear cut at all.

Inherited bacteria are found quite widely in invertebrates, and their behaviour is interesting both in its own right and for the light it casts on the now widely-accepted theory that eukaryotic cellular organelles, like mitochondria and chloroplasts, were once separate organisms that were adopted as symbionts and subsequently evolved to become inextricable parts of their hosts.

The bacteria under consideration here are still identifiably separate entities, which live inside the cells of their insect companions and seldom travel beyond. Horizontal transmission -- that is, between mature organisms -- is rare. Rather, they are passed from a mother to her offspring in the gametes: her eggs are infected before they are even fertilized. And not by accident.

Two classes of heritable bacteria are distinguished: primary symbionts are obligate, which is to say the host cannot survive without them, while secondary symbionts are conditionally beneficial -- there are hosts without them, but infection confers some potential advantage. In evolutionary terms, primary symbionts must once have been secondary, until the host discovered it could dispense with its own facilities for doing those things that its guests did better, and live more efficiently by living in harmony.

The bacteria retain their own lifecycle and can be killed off by antibiotics. In the case of primary symbionts, such treatment leads to death or, at best, sterility in the host. Often the symbionts' role is anabolic, manufacturing chemicals such as amino acids that the host needs but cannot create on its own. This is particularly common in insects whose diets are very restricted -- those that feed on wood, for example, which is markedly lacking in interesting nutritional content. Some dependent hosts actually have special organs in which the bacteria are stored and maintained and their products used.

Since the offspring of these creatures cannot survive uninfected, the mothers must guarantee transmission. To this end, bacteria are transported from the bacteriome organs into the ovum. Such intricate relationships are evolutionarily long-standing, the hosts and their necessary diseases bound together for hundreds of millions of years. Even though their genes remain in separate units, the bacteria must be considered quasi-genomic now.

Secondary symbiosis is less cut and dried, and uninfected hosts may prosper. The advantages of infection will often be environmentally determined, so in some contexts it is better to be infected whereas in others it is not. Typical benefits include resistance to fungal infections or parasitoid wasp larvæ, or the ability to make use of different diet plants. Infected and uninfected hosts may then not be competing for exactly the same resources and the species as a whole -- if we can still regard it as just one -- can occupy a larger niche.

For the symbiont, its environmental niche is the host. Since transmission typically occurs only maternally, male hosts are a reproductive dead end -- and many inherited bacteria have evolved to cause sex-ratio distortion in their hosts, leading to a disproportionate number of female children.

One common mechanism for this is male killing: the mother still lays approximately equal numbers of male and female eggs, but the males do not hatch. With offspring battling for the same resources, removing the sons improves the prospects for the daughters, and hence also for their bacterial passengers. The process may provide a more immediate and concrete gain: ladybirds, for example, exhibit dead larval cannibalism: eggs that do not hatch are eaten by the larvæ, so the nutritional resources that went into the boys are transferred directly to the girls.

Another way to shift the balance is feminization: the bacteria cause genetically male offspring to develop as females. In woodlice, for example, which are female heterogametic -- meaning that females have two different sex chromosomes (ZW) while males have a duplication (ZZ), in contrast to humans where it is the males that are heterogametic (XY) -- the phenotypic difference between the sexes is caused by an androgenic gland in the males; the inherited bacteria inhibit the function of this gland, changing the males into phenotypic females.

Yet a third approach is induced parthenogenesis, whereby the females wind up producing daughters asexually. Parthenogenesis is common in social insects such as ants and bees, which are haplodiploids: males have half as many chromosomes as females and are developed from unfertilized eggs. Fertilization provides the second set of chromosomes and leads to females. The inherited bacterial infection disrupts this process, causing duplication of the maternal chromosomes in the offspring so that the would-be haploid males instead become homozygous diploid females. This can lead to the loss of sex altogether: the entire population becomes female (and treatment with antibiotics leads to an entirely male population that cannot reproduce at all).

There are also strategies that act through the males as well as the females to increase the chances of infected offspring. In this case, both sexes are produced, but infected males are modified so that their sperm is incompatible with the eggs of uninfected females. Infected females can thus be fertilized by all males, while uninfected females are limited to uninfected males. As the prevalence of infection increases, the uninfected females find it more difficult to locate a compatible mate.

This strategy is interesting because it can lead to essentially disjoint populations, infected by two different kinds of bacteria each of which induces incompatibility to mates hosting the other. Even though the populations are still notionally the same species, they can no longer exchange genetic material and may subsequently diverge. In this case, since it is important for individuals to be able to recognise compatible mates, one obvious way they might diverge is in appearance, which is often quite variable between isolated populations of the same species even when they remain genetically compatible.

Male killing and other sex ratio distorting behaviour is not, in general, particularly advantageous to the host, since male offspring are good at spreading the host genes. Consequently, there is an ongoing evolutionary tension between behaviour modification by the bacteria and host adaptation, which can lead to rapid changes in particular populations. Observations of Pacific island butterflies over the last century or so have found drastic swings one way or the other over remarkably short time periods. In Samoa, for example, male killing was observed with very high prevalence for the whole of the 20th century, but since the end of 2001 sex ratios have returned to 1:1. Males and females are now all infected, but the MK behaviour is suppressed.
Posted by matt at February 26, 2007 12:50 PM