A race to the bottom with a new card from the coevolutionary deck

I’m a sucker for a clever, amusing title, though I’ve recently read that amusing titles are cited less (see here). Alas, maybe a well placed metaphor can enliven a manuscript and also not get lost in a citation-less abyss?
In basic evolution courses, students are taught about the Red Queen Hypothesis or evolutionary “arms races.”

© Lewis Carroll Through the Looking Glass

© Lewis Carroll Through the Looking Glass

Taken from Lewis Carroll’s Through the Looking-Glass, the Red Queen says “it takes all the running you can do, to keep in the same place.” This has been used as a clever way to explain the interaction between hosts and pathogens. A parasite evolves a way to overcome a host’s defenses and the host evolves a new defense. In response, the parasite evolves a new mechanism to attack the host. And so on and so on.

A personal favorite of mine extends the Lewis Carroll theme with the Chesire Cat.
© Lewis Carroll Through the Looking-Glass

© Lewis Carroll Through the Looking-Glass

Frada et al. (2008) described these dynamics for the coccolithophore Emiliania huxleyi in which the haploid cells are invisible to the virus that results in the collapse of blooming diploid cells. This is analogous to the Cheshire Cat, who in response to the Red Queen’s execution order, makes himself invisible. Thus, the Red Queen can’t carry out the death threat. Haploid Ehux cells do the same thing and it turns out macroalgae do too (stay tuned for more on this when I find a spare afternoon to finally write it up!).
I stumbled across a new metaphor called the Black Queen (Morris et al. 2012). Like the Red Queen, the Black Queen is a playing card, but this time not a Lewis Carroll invention. Rather, the Black Queen is the queen of spades in the card game Hearts.
I’ll admit, I’ve never played Hearts, so there was some necessary time spent with Google before I read the original paper by Morris et al. (2012) and the paper that peaked my interest for this post Morris (2015). The queen of spades is worth as much as all the other cards combined, so you don’t want this card! In the context of coevolution, some biological processes are as costly as the queen of spades. So, if you can avoid them because another species performs them, all the better (Morris et al. 2012).
Evolution is sometimes misinterpreted as a pathway to increased complexity, but what about all the organisms that have become less biological complicated. Morris et al. (2012) use the example of a tape worm. Tape worms don’t digest their own food because they don’t have to. Tapeworms don’t loose anything by losing their digestive capabilities because they live inside your digestive track. You do the work for them!
This reductive evolution is something that is more common, but is it simply genetic drift as found with endosymbiotic bacteria?
Morris et al. (2012) use the bacterioplankton Prochlorococcus as an exemplar of the Black Queen Hypothesis and argue reduction is the product of natural selection. Genome reduction has occurred in this dominant planktonic organism by which Prochlorococcus is no longer able to break down hydrogen peroxide. It relies on other bacteria to do this necessary biological process.
If you’re a microorganism, it costs a lot to carry genes around and then make proteins, so you can jettison some costly molecular hardware if another microbe still retains the ability perform that function, such as breaking down hydrogen peroxide.
Morris (2015) takes his original ideas further in a paper from last August in Trends in Genetics. He describes the leakiness spectrum and when evolution can favor coexistence between helpers that provide the functions and beneficiaries that, you guessed it, benefit.
© Morris 2015 Trends in Genetics

© Morris 2015 Trends in Genetics

Biological functions yield products that can be entirely private to purely public. The cell that performs a leaky function still retains substantial access to the product, but beneficiaries can still benefit from those products that scoot by a cell wall, for example, and aren’t used by the producer.
At first blush, this may seem altruistic, but as Morris (2015) points out, reciprocity isn’t required for leaky functions to become evolutionarily stable. But, members of a microbial community are in a different type of race. Rather than acquiring novel weapons, they’re shedding functions left, right and center. The helpers are those microbes that have lost the race and have become mired in their role as providers.

Aren’t the beneficiaries, such as Prochlorococcus, cheating the system?

Cheaters are typically thought of as mutants within a single-species population that stop performing some function that is costly to the individual but beneficial to the group as a whole, thereby gaining a fitness advantage at the expense of their conspecifics (West et al. 2006).

But, in the context of the Black Queen Hypothesis, the fitness of the producer is not necessarily diminished. Rather,

When dependencies evolved in this manner persist, they have the potential to develop into intricate networks of mutual dependency. Through the simple mechanism of selfish evolution toward efficient marshaling of resources, an entire ‘tangled bank’ can evolve from a simple monoculture in a few mutational steps.

Frada et al. (2008) The “Cheshire Cat” escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. PNAS 105, 15944-15949.
Morris et al. (2012) The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss. mBio 3(2):e00036-12.
Morris (2015) Black Queen evolution: the role of leakiness in structuring microbial communities. Trends in Genetics 31, 475-482.
West et al. (2006) Social evolution theory for microorganisms. Nature Reviews Microbiology 4597-607.

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