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Host mating system and coevolutionary dynamics shape the evolution of parasite avoidance in Caenorhabditis elegans host populations

Published online by Cambridge University Press:  28 June 2017

McKenna J. Penley  and
Levi T. Morran
McKenna J. Penley
Affiliation:
Department of Biology, Emory University, 1510 Clifton Rd, Atlanta, Georgia 30322, USA
Levi T. Morran*
Affiliation:
Department of Biology, Emory University, 1510 Clifton Rd, Atlanta, Georgia 30322, USA
*
Author for correspondence: Levi T. Morran, E-mail: [email protected]
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Abstract

Hosts exhibit a variety of defence mechanisms against parasites, including avoidance. Both host–parasite coevolutionary dynamics and the host mating system can alter the evolutionary trajectories of populations. Does the nature of host–parasite interactions and the host mating system affect the mechanisms that evolve to confer host defence? In a previous experimental evolution study, mixed mating and obligately outcrossing Caenorhabditis elegans host populations adapted to either coevolving or static Serratia marcescens parasite populations. Here, we assessed parasite avoidance as a mechanism underlying host adaptation. We measured host feeding preference for the coevolved and static parasites vs preference for Escherichia coli, to assess the evolution of avoidance behaviour within our experiment. We found that mixed mating host populations evolved a preference for E. coli relative to the static parasite strain; therefore, the hosts evolved parasite avoidance as a defence. However, mixed mating hosts did not exhibit E. coli preference when exposed to coevolved parasites, so avoidance cannot account for host adaptation to coevolving parasites. Further, the obligately outcrossing host populations did not exhibit parasite avoidance in the presence of either static or coevolved parasites. Therefore, both the nature of host–parasite interactions and the host mating system shaped the evolution of host defence.

Keywords

adaptationself-fertilizationcoevolutionarms race
Type
Research Article
Information
Parasitology , Volume 145 , Issue 6 , May 2018 , pp. 724 - 730
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Copyright
Copyright © Cambridge University Press 2017 

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References

Bell, G (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality. Berkley, CA: University of California Press.Google Scholar
Buchon, N, Silverman, N and Cherry, S (2014) Immunity in Drosophila melanogaster–from microbial recognition to whole-organism physiology. Nature Reviews Immunology 14, 796–810.CrossRefGoogle ScholarPubMed
Busch, JW, Neiman, M and Koslow, JM (2004) Evidence for maintenance of sex by pathogens in plants. Evolution 58, 2584–2590.Google ScholarPubMed
Carvalho, S, et al. (2014) The role of hermaphrodites in the experimental evolution of increased outcrossing rates in Caenorhabditis elegans. BMC Evolutionary Biology 14, 116.CrossRefGoogle ScholarPubMed
Chang, HC, Paek, J and Kim, DH (2011) Natural polymorphisms in C. elegans HECW-1 E3 ligase affect pathogen avoidance behaviour. Nature 480, 525–529.CrossRefGoogle Scholar
Chapuisat, M, et al. (2007) Wood ants use resin to protect themselves against pathogens. Proceedings of the Royal Society B: Biological Sciences 274, 2013–2017.CrossRefGoogle ScholarPubMed
Dudley, R and Mitton, K (1990) Parasite deterrence and the energetic costs of slapping in howler monkeys, Alouatta palliata. Journal of Mammalogy 71, 463–465.CrossRefGoogle Scholar
Ebert, D (1994) Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 1084–1086.CrossRefGoogle ScholarPubMed
Engelmann, I and Pujol, N (2010) Innate immunity in C. elegans. Advances in Experimental Medicine and Biology 708, 105–121.CrossRefGoogle ScholarPubMed
Feener, DHJ and Moss, KAG (1990) Defense against parasites by hitchhikers in leaf-cutting ants: a quantitative assessment. Behavioral Ecology and Sociobiology 26, 17–29.CrossRefGoogle Scholar
Felsenstein, J (1974) The evolutionary advantage of recombination. Genetics 78, 737–756.CrossRefGoogle ScholarPubMed
Fisher, RA (1930) The Genetical Theory of Natural Selection. Oxford: Clarendon Press.CrossRefGoogle Scholar
Frézal, L and Félix, M-A (2015) C. elegans outside the Petri dish. Elife 4, e05849. doi:10.7554/eLife.05849.CrossRefGoogle ScholarPubMed
Gibson, AK, et al. (2015) The evolution of reduced antagonism-A role for host-parasite coevolution. Evolution 69, 2820–2830.CrossRefGoogle ScholarPubMed
Glater, EE, Rockman, MV and Bargmann, CI (2014) Multigenic natural variation underlies Caenorhabditis elegans olfactory preference for the bacterial pathogen Serratia marcescens. G3 (Bethesda) 4, 265–276.CrossRefGoogle ScholarPubMed
Greischar, MA and Koskella, B (2007) A synthesis of experimental work on parasite local adaptation. Ecology Letters 10, 418–434.CrossRefGoogle ScholarPubMed
Hamilton, WD (1980) Sex versus non-sex versus parasite. Oikos 35, 282–290.CrossRefGoogle Scholar
Hart, BL (1990) Behavioral adaptations to pathogens and parasites: five strategies. Neuroscience & Biobehavioral Reviews 14, 273–294.CrossRefGoogle ScholarPubMed
Hart, BL (1994) Behavioral defense against parasites: interactions with parasite invasiveness. Parasitology 109, S139–S151.CrossRefGoogle ScholarPubMed
Hartfield, M and Keightley, PD (2012) Current hypotheses for the evolution of sex and recombination. Integrative Zoology 7, 192–209.CrossRefGoogle ScholarPubMed
Hill, WG and Robertson, A (1966) The effect of linkage on the limits to artificial selection. Genetics Research 8, 269–294.CrossRefGoogle ScholarPubMed
Hodgson, EE and Otto, SP (2012) The red queen coupled with directional selection favours the evolution of sex. Journal of Evolutionary Biology 25, 797–802.CrossRefGoogle ScholarPubMed
Jaenike, J (1978) An hypothesis to account for the maintenance of sex within populations. Evolutionary Theory 3, 191–194.Google Scholar
Kaltz, O and Shykoff, JA (1998) Local adaptation in host-parasite systems. Heredity (Edinburg) 81, 361–370.CrossRefGoogle Scholar
Laine, AL (2005) Spatial scale of local adaptation in a plant-pathogen metapopulation. Journal of Evolutionary Biology 18, 930–938.CrossRefGoogle Scholar
Laine, AL (2007) Detecting local adaptation in a natural plant-pathogen metapopulation: a laboratory vs. field transplant approach. Journal of Evolutionary Biology 20, 1665–1673.CrossRefGoogle Scholar
Lefevre, T, et al. (2010) Evidence for trans-generational medication in nature. Ecology Letters 13, 1485–1493.CrossRefGoogle ScholarPubMed
Litman, GW, Rast, JP and Fugmann, SD (2010) The origins of vertebrate adaptive immunity. Nature Reviews Immunology 10, 543–553.CrossRefGoogle ScholarPubMed
Lively, CM and Dybdahl, MF (2000) Parasite adaptation to locally common host genotypes. Nature 405, 679–681.CrossRefGoogle ScholarPubMed
Lively, CM and Morran, LT (2014) The ecology of sexual reproduction. Journal of Evolutionary Biology 27, 1292–1303.CrossRefGoogle ScholarPubMed
Masri, L, et al. (2013) Sex differences in host defence interfere with parasite-mediated selection for outcrossing during host-parasite coevolution. Ecology Letters 16, 461–468.CrossRefGoogle ScholarPubMed
Meisel, JD and Kim, DH (2014) Behavioral avoidance of pathogenic bacteria by Caenorhabditis elegans. Trends in Immunology 35, 465–470.CrossRefGoogle ScholarPubMed
Moore, J (2012) Parasites and the Behavior of Animals. Oxford: Oxford University Press.Google Scholar
Morgan, AD, Gandon, S and Buckling, A (2005) The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437, 253–256.CrossRefGoogle Scholar
Morran, LT, Parmenter, MD and Phillips, PC (2009) Mutation load and rapid adaptation favour outcrossing over self-fertilization. Nature 462, 350–352.CrossRefGoogle ScholarPubMed
Morran, LT, et al. (2011) Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333, 216–218.CrossRefGoogle ScholarPubMed
Morran, LT, et al. (2013) Temporal dynamics of outcrossing and host mortality rates in host-pathogen experimental coevolution. Evolution 67, 1860–1868.CrossRefGoogle ScholarPubMed
Morran, LT, et al. (2014) Experimental coevolution: rapid local adaptation by parasites depends on host mating system. American Naturalist 184(Suppl. 1), S91–S100.CrossRefGoogle ScholarPubMed
Muller, HJ (1932) Some genetic aspects of sex. American Naturalist 66, 118–138.CrossRefGoogle Scholar
Penley, MJ, Ha, G and Morran, LT (unpublished result). Evolution of Caenorhabditis elegans resistance under selection by the bacterial parasite Serratia marcescens. PLoS ONE.Google Scholar
Pradel, E, et al. (2007) Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proceeding of the National Academy of Sciences USA 104, 2295–2300.CrossRefGoogle ScholarPubMed
Schedl, T and Kimble, J (1988) fog-2, A germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119, 43–61.CrossRefGoogle ScholarPubMed
Schulenburg, H and Ewbank, JJ (2004) Diversity and specificity in the interaction between Caenorhabditis elegans and the pathogen Serratia marcescens. BMC Evolutionary Biology 4, 49.CrossRefGoogle ScholarPubMed
Singer, MS, Mace, KC and Bernays, EA (2009) Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS ONE 4, e4796.CrossRefGoogle ScholarPubMed
Slowinski, SP, et al. (2016) Coevolutionary interactions with parasites constrain the spread of self-fertilization into outcrossing host populations. Evolution 70, 2632–2639.CrossRefGoogle ScholarPubMed
Taylor, EL (1954) Grazing behavior and helminthic disease. Animal Behaviour 2, 61–62.CrossRefGoogle Scholar
Teotonio, H, et al. (2012) Evolution of outcrossing in experimental populations of Caenorhabditis elegans. PLoS ONE 7, e35811.CrossRefGoogle ScholarPubMed
Thompson, JN (1994) The Coevolutionary Process. Chicago: University of Chicago Press.CrossRefGoogle Scholar
Thompson, JN (2005) The Geographic Mosaic of Coevolution. Chicago: University of Chicago Press.CrossRefGoogle Scholar
Zhang, Y, Lu, H and Bargmann, CI (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438, 179–184.CrossRefGoogle ScholarPubMed
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