The Red Queen hypothesis

” Now, here you see, it takes all the running you can do, to keep in the same place. If you want to get somewhere else, you must run at least twice as that!”

~ Lewis Carroll, Through the Looking Glass (1897), page 50

A two-fold fitness cost is a rather high price to pay for any trait (see discussion of the cost of sex). One could then reasonably predict that a survey of the natural world would reveal sex to be an unpopular strategy, with the vast majority of organisms reproducing asexually. The natural world, however, tells us precisely the opposite. The vast majority of eukaryotes reproduce sexually. Obligate asexuality is exceedingly rare (fewer than 0.1% of animal species), and few of those lineages (if any) have persisted through evolutionary time. How can we explain the ubiquity of sex, given its inherent costs? See Lively and Morran (2014 JEB) and Hartfield and Keightley (2012 Int Zool) for recent reviews.

The Red Queen hypothesis offers one potential explanation. The models of Maynard Smith and others showed that the environment must be “bloody-minded” to maintain sex (Maynard Smith 1985). Imagine that environmental conditions strongly favor a single phenotype. The associated genotype increases in frequency. Only a few generations later though, conditions change. The very same phenotype is now specifically disfavored. Such fickle, fluctuating selection can counterbalance the costs of sex, because sexual lineages retain the genetic variation needed to continually adapt (Maynard Smith 1971b, 1978).

From where might such “bloody-minded” selection arise? Certainly no abiotic force commonly shifts in the rapid, specific way required by the models. What about the biotic world? Selection by coevolving antagonists meets our criteria (Hamilton 1975; Levin 1975; Jaenike 1978; Hamilton 1980, Hamilton et al. 1990). Let’s assume that natural enemies (e.g. parasites) specifically attack one, or a subset, of the host genotypes in a population. Host genotypes that have a fitness advantage will increase in frequency, becoming common. The most successful enemies are then those that specifically attack these common host genotypes (i.e. the most abundant resource). The biotic environment now specifically selects against these formerly fit genotypes. We know this model as the Red Queen hypothesis (Bell 1982).

evoedu
Classic Red Queen oscillations in the frequency of a host genotype and the parasite genotype that infects it. Data generated by students playing the Red Queen game (Gibson et al. 2015 Evol Educ Outreach) – see Teaching Resources

A key prediction of the Red Queen hypothesis is that sex should be maintained in the presence of coevolutionary selection (there is much fantastic work testing this prediction, e.g. Morran et al. 2011 and Lively et al. 1987). The freshwater snail P. antipodarum is commonly infected by the sterilizing trematode parasite Microphallus. We can measure susceptibility to Microphallus in the lab. We first expose a group of hosts to a fixed dose of Microphallus and then measure the proportion of infected hosts. We know that, in this system, susceptibility is rooted in the interaction of coevolving host and parasite genotypes. For example, susceptibility is highest when hosts are exposed to local, coevolving parasites. Susceptibility can thus serve as a measure of coevolutionary selection. In contrast, prevalence is only partly rooted in coevolutionary genetics (susceptibility) (Gibson et al. 2016 Am Nat, discussed here). Therefore, infection prevalence should be an inaccurate proxy for testing the relationship between coevolutionary selection and sex. This is a general point – infection prevalence typically has a major environmental component that may obscure any relationship between prevalence and coevolution. In spite of this, prevalence is the most common proxy used to measure coevolutionary selection.

We predicted that, if coevolving parasites maintain sex in P. antipodarum, 1) susceptibility should correlate positively with the proportion of sexual snails at a site, and 2) susceptibility should be a stronger predictor of variation in sexual frequency than is infection prevalence. Gibson et al. (2016 Evolution) tests these predictions.  We find that susceptibility is tightly positively correlated with the proportion of sexual females around our small study lake, Lake Alexandrina. Susceptibility can in fact explain the vast majority of variation in sex. Consistent with our second prediction, the distribution of sex is more closely linked to susceptibility than to prevalence.

 

“Indeed, nothing is more impressive in the biology of parasites than the  lengths to which they will go in order to retain amphimixis, or at least cling  to some remnant of sexuality.”

~ Graham Bell, The Masterpiece of Nature (1982), pages 379-380

The Red Queen and parasite sex

Parasites are often overlooked in favor of their charismatic hosts. Yet parasites in particular should experience strong coevolutionary selection. Indeed, selection is expected to be stronger on obligate parasites: failure to infect might mean death. Hence the reproductive strategies of parasites are an interesting, though largely unexplored, realm for the Red Queen.

The Red Queen hypothesis predicts that sexual reproduction should be more common in parasitic taxa than in their free-living relatives (Bell 1982). Jesualdo Arturo Fuentes and I tested this prediction in the Nematode phylum, which shows remarkable variation in reproductive mode and in ecology (i.e. parasitism has arisen multiple times in the Nematoda).  We use phylogenetic comparative methods to test for correlations between the evolutionary transitions in reproduction and ecology. As predicted, outcrossing is significantly correlated with parasitism of animal hosts. We find that selfing and asexuality evolve far more readily on free-living than on animal parasitic lineages. Interestingly, outcrossing is not correlated with parasitism of plant hosts. Our results argue that the Red Queen is an explanation, at least in part, for the macroevolutionary distribution of outcrossing in nematodes (Gibson and Fuentes 2015 Evolution).

Some amazing nematodes

Left: Pratylenchus sp, female: Original drawing made by W.E. Chambers. Figure 1 from Cobb, N.A. 1917 Ag Res. 11(1): 27-33. Originally published as Tylenchus penetrans 

Right: Enoplus sp.: Original drawing made by W.E. Chambers for N.A. Cobb 1915: Nematodes and their Relationships, Figure 42, p. 484. Property of Nematology Investigations, USDA, Beltsville, MD. Images provided by Zafar Handoo.

References

  • Bell, G. 1982. The Masterpiece of Nature: the Evolution and Genetics of Sexuality. University of California Press, Berkeley.
  • Hamilton, W. D. 1975. Gamblers since life began: barnacles, aphids, elms (a review). Quart Rev Biol 50:175-180.
  • Hamilton, W. D. 1980. Sex versus non-sex versus parasite. Oikos 35:282-290.
  • Hamilton, W. D., R. Axelrod, and R. Tanese. 1990. Sexual reproduction as an adaptation to resist parasites (a review). Proc Natl Acad Sci USA 87:3566-3573.
  • Hartfield, M. and Keightley, P.D. 2012. Current hypotheses for the evolution of sex and recombination. Int Zool 7: 192-209.
  • Jaenike, J. 1978. An hypothesis to account for the maintenance of sex within populations. Evol Theor 3:191-194.
  • Levin, D. A. 1975. Pest pressure and recombination systems in plants. Am Nat 109:437-451.
  • Lively, C. M. 1987. Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature 328:519-521.
  • Lively, C.M. and Morran, L.T. 2014. The ecology of sexual reproduction. J Evol Biol 27: 1292-1303.
  • Maynard Smith, J. 1971. What use is sex? J Theor Biol 30:319-335.
  • Maynard Smith, J. 1978. The Evolution of Sex. Cambridge University Press, Cambridge, UK.
  • Maynard Smith, J. 1985. The evolution of recombination. J Gen 64:159-171.
  • Morran, L., O. Schmidt, I. Gelarden, R. Parrish II, and C. M. Lively. 2011. Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333:216-218.
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