Host-parasite coevolution; origin and maintenance of sex

Antagonistic coevolution

The costs of parasitism lead to antagonistic coevolution between hosts and parasites.

Hosts can evolve resistance (typically by closing the compatibility filter) or tolerance (focusing on resistance this week).

• Red Queen (cyclic)
  • new alleles arise frequently
  • frequency-dependent selection: rare alleles in the parasite, or host, have an advantage
  • resistance alleles tend to be monomorphic
  • different possible genetic systems: gene-for-gene, matching alleles, etc.

(Gibson and Lively (2019); see also Dybdahl and Storfer (2003))

• matching alleles: e.g. host has a self-nonself recognition system (typical in inverts); parasite succeeds if it matches (i.e. looks like host). Favors local adaptation, cycling/variation, dilution effects.
• inverse matching alleles: host matches many parasite signals (e.g. vertebrate antibody/antigen matching); parasite succeeds if it does not match any of the host antibodies. Doesn’t favour rare host genotypes, anti-dilution effects.
• gene-for-gene: like inverse matching, but there is a “universal infector” that doesn’t match anything (i.e. infects everything) (Plants: R genes, Avr genes). Wikipedia:

Because there would be no evolutionary advantage to a pathogen keeping a protein that only serves to have it recognised by the plant, it is believed that the products of Avr genes play an important role in virulence [= ability to infect] in genetically susceptible hosts

Stahl et al. (1999): Arms races in a disease-resistance locus of Arabidopsis

• trench warfare/arms race (unidirectional)
  • resistance builds up until benefits balanced by costs
  • resistance alleles polymorphic
  • short-term stabilizing selection
  • long-term frequency cycling

Antagonistic coevolution and sex

Sex and variations: we consider dioecy or gonochory (individuals are either male or female), but there are many variations: individuals may be sequential or simultaneous hermaphrodites. They may self-fertilize or outcross to different degrees.

Costs of sex: mating failure (vs. reproductive assurance), cost of males, cost of meiosis (when only half your genes make it into your offspring, you essentially pay a 50% fitness cost). Cost of outbreeding (breaking up co-adapted gene complexes).

Simplest if we just think of cost of meiosis and advantages of recombination, although other costs and benefits do apply.

Advantages of sex (not necessarily parasite-related)

• Muller’s ratchet (fixation of deleterious alleles within lineages) [small (10–100 individuals) populations only];
• “Kondrashov’s hatchet” (Kondrashov 1993) (an analogue that works in large populations, with epistasis); natural selection is more effective at purging deleterious mutations. Also see Keightley and Otto (2006) on mutation purging.
• Hard (frequency-independent) habitat selection: allows sexual populations to inhabit transient niches that may not be available to asexuals; increases probability of making it through bad years
• Soft (frequency-dependent) or “tangled bank” habitat selection: allows sexual populations to avoid competition better, since they can use a wider variety of niches

Requirements for RQ dynamics

• heritable variation in host resistance to parasites
• heritable variation in parasite infectivity
• specificity

Snails and trematodes

Lively, Dybdahl and others have studied the interaction of parasitism and sexual reproduction extensively in New Zealand lakes (they started collecting about 15 years ago) where there are mixed clonal (triploid) and sexual (diploid) populations of New Zealand mud snail, Potamopyrgus antipodarum which are parasitized by a castrating cestode, Microphallus spp. Genetic (electrophoretic) variability exists in hosts; gene flow of parasites is higher than gene flow of hosts, which helps the RQ work

Primary theories for the variation in frequency of sexual snails among and within lakes:

• Resistance tradeoffs: genetic tradeoff between competitive ability and resistance to parasites
• Reproductive assurance: asexuals ensure reproduction and avoid costs of mating (assuming sexuals have some other advantage)
• Lottery: sexuals survive in a wider range of (micro)habitats
• Tangled bank: rare offspring of sexuals experience less competition
• Red Queen: sexuals (or uncommon clones) resist parasites better

		resistance tradeoffs		reproductive assurance		lottery		tangled bank	Red Queen
	findings	negative corr between comp ability of asex & parasite load	negative corr between freq of asex & parasite load	asex↑at low pop density	asex ↑in unstable env	asex fail alone in habitats OK for sex	asex ↑in temporally variable env	sex ↑in variable, high-comp env	sex ↑ in high-parasite env	time-lagged host-para matching	local adaptation
Curtis M. Lively (1987)	more sexuals in lakes; sexuals correlated with parasites across lakes		no				no	yes	yes
Curtis M. Lively (1989)	parasites infect local hosts better, regardless of distance										yes
Curtis M. Lively (1992)	no corr between pop density and sex freq			no
Jokela and Lively (1995); Fox et al. (1996)	sex corr w/ parasites within lakes								yes
Dybdahl and Lively (1997)	time-lagged assoc betw parasites & common clones									yes
Jokela et al. (1997)	sex doesn’t outcompete asex in absence of parasites	no
Dybdahl and Lively (1998)	association between parasites and previously common clones									yes
Krist et al. (2000)	snails in shallow water more susceptible
C. M. Lively and Dybdahl (2000)	assoc between para & prev common local, but not non-local, hosts									yes	yes
C. M. Lively et al. (2004)	meta-analysis: asex more resistant than sex to allopatric paras										yes
Koskella, Lively, and Koella (2007)	paras less infective to exp infection with current vs time-lagged paras									yes

Potential problems for the Red Queen

• RQ may not work without strong parasite effects on host fitness
• can sexuals compete against a diverse set of clones?
• is a tiny bit of sex enough to maintain variation without losing the advantages of asexuality?
• why is there so much obligate sexuality/outcrossing?
• persistent asexual lineages (e.g. bdelloid rotifers, but see Schwander (2016))

Other theories (Meirmans and Neiman 2006)

• Muller’s ratchet plus RQ: Parasites drive population fluctuations which tend to fix deleterious mutations in asexual lineages. Predicts: Frequent parasite-induced population crashes (removing parasites should remove the crashes); Relative fitness of the population should be higher after crashes
• Tangled bank plus RQ: Mechanism: parasite resistance determines competitive ability. Predicts: competitive outcomes (between common and rare clones, or between sexuals and asexuals) should vary in the presence and absence of parasites

In all of this, we need to be careful distinguishing the true effects of sexual reproduction. Ecologists tend to assume it produces “more variable” offspring, but this is not necessarily the case. What sex really does is to allow recombination of different genotypes … what is the true relationship between sexual reproduction and variability? It depends on population size, how frequently asexual lineages are split off from the sexual population and how, etc. etc.. (Importance of epistasis: (Metzger et al. 2016))

References

Dybdahl, Mark F., and Curtis M. Lively. 1997. “Host–Parasite Interactions: Infection of Common Clones in Natural Populations of a Freshwater Snail (Potamopyrgus Antipodarum).” Proceedings of the Royal Society of London. Series B: Biological Sciences 260 (1357): 99–103. https://doi.org/10.1098/rspb.1995.0065.

———. 1998. “Host‐parasite Coevolution: Evidence for Rare Advantage and Time‐lagged Selection in a Natural Population.” Evolution 52 (4): 1057–66. https://doi.org/10.1111/j.1558-5646.1998.tb01833.x.

Dybdahl, Mark F., and Andrew Storfer. 2003. “Parasite Local Adaptation: Red Queen Versus Suicide King.” Trends in Ecology & Evolution 18 (10): 523–30. https://doi.org/10.1016/S0169-5347(03)00223-4.

Fox, Jennifer A., Mark F. Dybdahl, Jukka Jokela, and Curtis M. Lively. 1996. “Genetic Structure of Coexisting Sexual and Clonal Subpopulations in a Freshwater Snail (Potamopyrgus Antipodarum).” Evolution 50 (4): 1541–48. https://doi.org/10.1111/j.1558-5646.1996.tb03926.x.

Gibson, Amanda K., and Curtis M. Lively. 2019. “Genetic Diversity and Disease Spread: Epidemiological Models and Empirical Studies of a Snail–Trematode System.” In Wildlife Disease Ecology: Linking Theory to Data and Application, edited by Andy Fenton, Dan Tompkins, and Kenneth Wilson, 32–57. Ecological Reviews. Cambridge: Cambridge University Press. https://doi.org/10.1017/9781316479964.002.

Jokela, Jukka, and Curtis M. Lively. 1995. “Spatial Variation in Infection by Digenetic Trematodes in a Population of Freshwater Snails (Potamopyrgus Antipodarum).” Oecologia 103 (4): 509–17. https://doi.org/10.1007/BF00328690.

Jokela, Jukka, Curtis M. Lively, Mark F. Dybdahl, and Jennifer A. Fox. 1997. “Evidence for a Cost of Sex in the Freshwater Snail Potamopyrgus Antipodarum.” Ecology 78 (2): 452–60. https://doi.org/10.1890/0012-9658(1997)078[0452:EFACOS]2.0.CO;2.

Keightley, Peter D., and Sarah P. Otto. 2006. “Interference Among Deleterious Mutations Favours Sex and Recombination in Finite Populations.” Nature 443 (7107): 89–92. https://doi.org/10.1038/nature05049.

Kondrashov, A. S. 1993. “Classification of Hypotheses on the Advantage of Amphimixis.” Journal of Heredity 84 (5): 372–87. https://doi.org/10.1093/oxfordjournals.jhered.a111358.

Koskella, Britt, Curtis M Lively, and J. Koella. 2007. “Advice of the Rose: Experimental Coevolution of a Trematode Parasite and Its Snail Host.” Evolution 61 (1): 152–59. http://www.bioone.org/doi/abs/10.1111/j.1558-5646.2007.00012.x.

Krist, A. C, C. M Lively, E. P Levri, and J. Jokela. 2000. “Spatial Variation in Susceptibility to Infection in a Snail-Trematode Interaction.” Parasitology 121: 395–401.

Lively, C. M, M. E Dybdahl, J. Jokela, E. E Osnas, and L. E Delph. 2004. “Host Sex and Local Adaptation by Parasites in a Snail-Trematode Interaction.” American Naturalist 164 (5): S6–18.

Lively, C. M, and M. F Dybdahl. 2000. “Parasite Adaptation to Locally Common Host Genotypes.” Nature 405 (6787): 679–81.

Lively, Curtis M. 1987. “Evidence from a New Zealand Snail for the Maintenance of Sex by Parasitism.” Nature 328 (6130): 519–21. https://www.nature.com/articles/328519a0.

———. 1989. “Adaptation by a Parasitic Trematode to Local Populations of Its Snail Host.” Evolution 43 (8): 1663–71. https://academic.oup.com/evolut/article-abstract/43/8/1663/6869249.

———. 1992. “Parthenogenesis in a Freshwater Snail: Reproductive Assurance Versus Parasitic Release.” Evolution 46 (4): 907–13. https://doi.org/10.1111/j.1558-5646.1992.tb00608.x.

Meirmans, Stephanie, and Maurine Neiman. 2006. “Methodologies for Testing a Pluralist Idea for the Maintenance of Sex.” Biological Journal of the Linnean Society 89 (4): 605–13. https://doi.org/10.1111/j.1095-8312.2006.00695.x.

Metzger, César M. J. A., Pepijn Luijckx, Gilberto Bento, Mahendra Mariadassou, and Dieter Ebert. 2016. “The Red Queen Lives: Epistasis Between Linked Resistance Loci.” Evolution 70 (2): 480–87. https://doi.org/10.1111/evo.12854.

Schwander, Tanja. 2016. “Evolution: The End of an Ancient Asexual Scandal.” Current Biology 26 (6): R233–35. https://doi.org/10.1016/j.cub.2016.01.034.

Stahl, Eli A., Greg Dwyer, Rodney Mauricio, Martin Kreitman, and Joy Bergelson. 1999. “Dynamics of Disease Resistance Polymorphism at the Rpm1 Locus of Arabidopsis.” Nature 400 (6745): 667–71. https://doi.org/10.1038/23260.

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Last updated: 2023-10-23 14:05:18.368203