'Hopeful Monsters': Nothing in Evolution Makes Sense Except in the Light of E. coli (and Shigella)

When I read Olivia Judson's post about hopeful monsters, I didn't think she used the term correctly (here are some good explanations why), but I was surprised by Jerry Coyne's response.

First, the personal attack on Judson is unwarranted: when we reach the point where the serious challenge to evolutionary biology is the misuse of a discredited decades-old idea, as opposed to the politically powerful anti-science creationist movement, we're in a pretty good place. She made a mistake--I don't think her motives were self-aggrandizing. Second, if you're going to launch an ad homeniem attack, make it a good one. Third, there's definitely some ax-grinding going on that has nothing to do with Judson's misuse of "hopeful monsters", as revealed by a commentary that Coyne co-authored and counter-argued by ScienceBlogling Razib (italics mine):

Coyne is a traditionalist who doesn't suffer fools; his recent critiques of evo-devo make this sort of sally understandable. The ideas resurrected by Judson are fundamentally more radical than anything Sean Carroll has proposed. But, I do want to offer that I remember listening to a young zebrafish researcher explaining how shocked he was a lot of the extant variation they saw was controlled by only a few genes. There is a real story to be told about the exposure via genomics that many quantitative traits are controlled by a few loci of large effect as opposed to architectures hypothesized by the infinitesimal models....

But onto the title of post. As someone who has spent most of his career* studying bacterial evolution, many evolutionary debates focus on those organisms, which are at most, ten percent of the earth's biomass (eukaryotes). When one considers bacteria, there are single events that radically change an organism's ecology--whether one wants to call these hopeful monsters or not, I leave to the reader.

I've posted before about the evolution of Shigella, which is nothing more than several pathogenic lineages of E. coli, so I won't revisit that topic in detail. For a commensal E. coli to become Shigella, a critical step is the acquisition of a virulence plasmid. This plasmid (a mini-chromosome roughly ~3% the size of the E. coli genome) confers various traits on the bacterium, including the ability to stick to certain tissue types, and to produce an enterotoxin that causes bloody diarrhea.

These plasmid-bearing bacteria are not Shigella. They are facultative pathogens--they can cause disease, but don't always do so--known as enteroinvasive E. coli, or EIEC. Typically, EIEC aren't as virulent as the obligate pathogen Shigella. In fact, a genomic comparison of EIEC and Shigella suggests that Shigella has lost several hundred genes (5-10% of its original gene compliment) when compared to EIEC. Many of these lost genes result from a reduction in purifying selection--that is, mutations that eliminate these genes don't appear to hurt Shigella strains. On the other hand, there are gene losses that appear to favored by selection, such as the loss of cadaverine production, since cadaverine reduces the effectiveness of the enterotoxin.

While EIEC isn't Shigella, although there are EIEC which due to gene loss are well on their way to becoming Shigella, and irreversibly so, EIEC is ecologically distinct from commensal E. coli. It causes a lot of disease, and unlike its commensal relatives, is not frequently observed in commensal habitats (i.e., healthy mammals). Certainly, EIEC is more ecologically distinct than some of the slight species differences that people who study eukaryotes get all hot and bothered about.

So is the evolution of EIEC from commensal E. coli a "hopeful monster?" Personally, I don't care, since it's just an imprecise phrase. What I do care about is that there is good evidence in bacteria that single genetic changes can radically alter ecology, and lead to irreversible ecological divergence.

*My early training was as a marine evolutionary ecologist.

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Evolutionary biologists who focus on animals, I've noticed, rarely acknowledge that their debates over evolutionary mechanisms often concern processes that are limited to animals. Instead, you get the impression you're watching a debate over mechanisms that are important for all living things. Perhaps some day, microbes will be recognized as the overwhelming majority, and animals as the oddballs... ; )

Thanks for posting this, Mike. Like I said towards the tail-end of my own post, I think you're right in that the focus is so much an animals that the majority of life is overlooked in this area. Likewise, the term "hopeful monster" is so vague that it is a little use (nearly every paper I was able to find featuring the term defined it differently). Anyway, well done.

There are several terms I would see eliminated from biology and geology: "sudden", "abrupt", "saltation", "large" and other comparatives and their antonyms. They add nothing to the debate and confuse many.

Carl: And what about plants? At least bacteria figure big in textbooks (for genetic systems, cell process, etc). Plants are mere background for much of the discussion.

I say this as an offender. My interests, experience, training, etc. is mainly concerning mammals and closely related forms (like birds). I do have to actively remind myself that plants are people too.

John: Those terms would be useful if they had meaning and could be compared.

I say this as an offender. My interests, experience, training, etc. is mainly concerning mammals and closely related forms (like birds). I do have to actively remind myself that plants are people too

Thanks for posting this, Mike. Like I said towards the tail-end of my own post, I think you're right in that the focus is so much an animals that the majority of life is overlooked in this area. Likewise, the term "hopeful monster