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Rapid evolution of beneficial infections

Given my location halfway between the Twin Cities of Minneapolis and St. Paul, and my childish love of clever acronyms, I sometimes wish I'd named this blog This Week In Natural Selection. But then I suppose I'd have to review a pair of closely related papers each week. I'm going to do that this week, anyway.

This week's twins were both published in PLoS Biology, so both are freely available on-line. Both have new data on bacteria that infect insects. Both help us understand the conditions under which infecting bacteria evolve to be beneficial, rather than harmful. Finally, both disprove, again, the popular idea that any evolutionary change big enough to matter (except antibiotic resistance, which a creationist commenter once claimed always involves "horizontal transfer" of genes among bacteria, even though resistance often evolves in bacteria in a closed container all descended from a single cell) always involves lots of genes and takes millions of years. Evolution is our present and future, not just our past.

The first paper is "From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila" by Andrew Weeks, my former colleague Michael Turelli, and three others (Universities of Melbourne, California at Davis, and Texas).

The popular idea that pathogens (microbes that cause disease) always evolve into mutualists (which help their hosts) "because otherwise both species will eventually go extinct" is wrong. Natural selection is never guided by future benefits, any more than a river will run uphill if that's the shortest route to the ocean.

On the other hand, there are some conditions that favor the evolution of mutualism. Bacteria or viruses that can easily spread from a very sick (or dead) host to a new host will often become more deadly over the course of evolution, as discussed in a previous post. But a microbe that only reproduces when its host does may evolve in a way that increases the host's chances of reproducing. (This may not be true if each host individual has several competing strains of the microbe. In this case "It may be better to keep alive the goose that lays the golden eggs than to kill it. But this argument depends on the assumption that, if you do not kill the golden goose, no one else will either: that is, it assumes that the host is infected by a single clone of symbionts." Maynard Smith 1989 Nature 341:284-285.)

Wolbachia are bacteria that infect various insects, including the fruit-fly Drosophila. Twenty years ago, female fruit-flies from California that were infected with Wolbachia laid more eggs if they were "cured" of their infection using antibiotics. So Wolbachia was harmful to fruit-flies, then. But because Wolbachia is transmitted mainly in eggs, the authors thought they might evolve to be helpful instead. So they collected fruit-flies from several locations and measured the effects of Wolbachia on egg production, using the same antibiotic method. Sure enough, curing the infection now reduces egg production.

Does this prove that the Wolbachia have evolved so that they are now beneficial rather than harmful? Not quite. Suppose Wolbachia have both beneficial and harmful effects, such as consuming energy inside the host but also making some vitamin. If the hosts (fruit-flies) evolved so that they lost the ability to make that vitamin themselves, then curing them of bacteria could reduce their egg production, but they might still be worse off than their uninfected ancestors (de Mazancourt et al. 2005 J. Ecol.). In this case, however, the authors showed that it was the Wolbachia that have evolved, not the fruit-flies.

Even the evolved Wolbachia can reduce egg production, however. When an infected male mates with an uninfected female fruit-fly, many of her eggs fail to hatch. This "you're either with us or against us" strategy helped Wolbachia spread rapidly in California.

This week's second paper is "Aphid thermal tolerance is governed by a point mutation in bacterial symbionts" by Helen Dunbar and colleagues at the University of Arizona.

Whether aphids infected with the bacterium Buchnera are better or worse off than their uninfected ancestors is not known, as far as I can tell. But now, at least, they depend on them for essential nutrients.

Dunbar et al. looked at a Buchnera mutation, seen both in lab and field, that reduces a biochemical response to high temperature. With high temperature exposure, the mutants apparently died, which greatly reduced the reproduction of their aphid host. Under cool temperatures, however, aphids containing the mutant Buchnera reproduced earlier and laid more eggs total. The mutant bacteria are fairly common in aphids in the field, probably reflecting back-and-forth evolution with varying temperature exposure in time and space.

With respect to the gene studied, the bacteria and the aphids have a shared interest in adapting to the temperatures to which they are exposed in the field. This contrasts with the more complex case of Wolbachia, where bacteria and host have both shared interests and conflicting interests. Are there other genes in Buchnera where a mutation could benefit bacteria while hurting their host? Or has this symbiosis evolved to the point where there are few such conflicts of interest? These aren't the first interesting papers I've seen on Wolbachia and Buchnera, and they probably won't be the last.

Comments

Have you checked out the new Cell Host and Microbe journal yet? It's my new favourite!

Gotta love those PLoS journals. BioMed Central also publishes some good open access journals. I got a paper into BMC Genomics before it had been assigned an impact factor and it's ended up being much more prestigious than we expected when we submitted!

Thanks! I hadn't seen it, but it might be right for some of our work.

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