How to celebrate Valentine’s Day: A note on the Red Queen and maintaining sexual reproduction

This year’s Valentine’s card of choice

HAPPY VALENTINE’S DAY! As a perpetually single girl this is my favorite holiday of the year. The first and second half of those statements may appear conflicted. However, every year on Valentine’s Day, I send out glorious amounts of Valentine’s to all my single friends (See below for this years!), eat chocolate and drink red wine while ordering myself sexy lingerie on the internet. Yeah, it’s a pretty awesome holiday. This year, one of my favorite evolutionary biologists has upped the excitement by publishing a paper on what conditions favor sex! Perfect for Valentine’s Day!

Why organisms reproduce sexually is one of the great mysteries in evolutionary biology (I’d like to note that here I’m talking about sex in terms of reproduction. It isn’t a mystery to me why organisms copulate, the differences being if that sex comes with offspring while copulation is just good old fashioned fun). There are a number of theoretical reasons that they shouldn’t! One of the strongest arguments was first laid out by John Maynard Smith (1978) who noted that an asexual female can produce twice as many offspring per individual than a sexual female, who wastes half of her effort producing males. This almost immediately results in sexuals being driven to extinction and is termed “the two-fold cost of males.”

There have been a number of different mechanisms of selection that have been proposed to explain sex: host-parasite interactions (Bell 1982), elimination of deleterious alleles (Mueller 1964), and various forms of selection (Charlesworth 1993; Otto and Barton 2001; Roze and Barton 2006). However, none of these alone are able to theoretically overcome the two-fold cost of producing males, so many biologists have started taking a pluralist approach (West et al. 1999; Howard and Lively 1994) and combing one or more of the advantages to being sexual in an effort to understand why the birds do it, the bees do it, and even educated fleas do it.

The theoretical problem with sex

Hodgson and Otto (that’s MacArthur “Genius Grant” recipient Sarah “Sally” Otto) recently published such a model, looking at how directional selection for advantageous alleles and host-parasite coevolutionary interactions could potentially combine to favor sexual reproduction. They specifically looked at host-parasite interactions that are mediated by one allele in the parasite matching or mismatching one allele in the host resulting in infection or no infection. This kind of interaction (referred to as the Matching Allele Model) at equilibrium results in negative frequency dependent selection causing oscillations in both populations, which are called “Red Queen” dynamics.

I mentioned the Red Queen in my last post, so I’ll just touch on it again here. Famed paleontologist Van Valen (1973) noted that organisms tend to continuously evolve to their environment, which is also constantly changing. He noted it was similar to a passage in Lewis Carrol’s Alice in Wonderland, and dubbed this hypothesis The Red Queen. Graham Bell (1982) used the Red Queen to talk about host-parasite interactions, noting that as hosts and parasites are both evolving in response to each other, then the Red Queen should be stronger than other, less changeable environmental factors. The Red Queen has since been used to evaluate conditions under which the negative frequency dependent selection can favor sexual selection in hosts when under strong selection by parasites, both empirically and theoretically.  Unfortunately, theory generally finds that sexual reproduction is only favored by the Red Queen under conditions where selection is unrealistically strong. However, there are a few conditions that, when coupled with the Red Queen, favor sex.

Hodgson and Otto simulated a model in which they considered three different loci in the host population, one that mediates host-parasite interactions, one that directional selection acts on and one that dictates how much recombination occurs (the sex allele). The frequency of this “sex allele” in the population is tracked through time and allows you to look at when sex is favored and when it is driven to extinction. The parasite population have only one locus of interest, which interacts with the host’s interaction locus.

In general the “sex allele” was favored, but it was more strongly favored in simulations where the beneficial allele was strongly beneficial. Moreover, the frequency of the modifier allele changed more slowly when selection on the host-parasite interaction allele was weaker. Finally when both loci were linked, the amount of sex in the population increased the most. The authors conclude that this interaction favors sex in the population because the genetic mixing uncouples the fate of beneficial alleles from those being selected against in host-parasite interactions*.

This result is contrary to previous work, and generates a scenario under which sex can be maintained. Moreover, it fits well with the empirical data. where many host-parasite interactions have been shown to be mediated at a single loci. It’s a very simple solution laid out in an excellent and easily accessible model. What an excellent way to spend your Valentine’s Day, reading about sex!

Now if you’ll excuse me, there are some dark chocolate covered strawberries with my name on them.

* I’d like to take a moment to note that I love Sally Otto’s models. I hope someday I can write models as well formulated and elegant as she does … in every paper she writes.

Literature Cited:

Charlesworth B (1993) Mutation-selection balance and the evolutionary advantage of sex and recombination. Genetic Research Cambridge 61: 205-224.

Hodgson EE and SP Otto (2012) The red queen coupled with directional selection favours the evolution of sex. Journal of Evolutionary Biology doi: 10.111/j.142-=9101.2012.02468.x

Jokela J, Dybdahl MF and CM Lively (2009) The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. American Naturalist 174: S43-S53.

Maynard Smith J (1978) The evolution of sex. Cambridge University Press, London.

Muller HJ (1964). The relation of recombination to mutational advance  Mutat Res 106: 2–9.

Otto SP and N Barton (2001) Selection for recombination in small populations. Evolution 55: 1921-1931.

Roze D and N Barton (2006) The Hill-Robertson effect and the evolution of recombination. Journal of Evolutionary Biology 12: 1003-1012.

Van Valen, L (1973) “A new evolutionary law” Evolutionary Theory 1: 1¬30.