Coevolutionary interactions with parasites constrain the spread of self-fertilization into outcrossing host populations.
Given the cost of sex, outcrossing populations should be susceptible to invasion and replacement by self-fertilization or parthenogenesis. However, biparental sex is common in nature, suggesting that cross-fertilization has substantial short-term benefits. The Red Queen hypothesis (RQH) suggests that coevolution with parasites can generate persistent selection favoring both recombination and outcrossing in host populations. We tested the prediction that coevolving parasites can constrain the spread of self-fertilization relative to outcrossing. We introduced wild-type Caenorhabditis elegans hermaphrodites, capable of both self-fertilization, and outcrossing, into C. elegans populations that were fixed for a mutant allele conferring obligate outcrossing. Replicate C. elegans populations were exposed to the parasite Serratia marcescens for 33 generations under three treatments: a control (avirulent) parasite treatment, a fixed (nonevolving) parasite treatment, and a copassaged (potentially coevolving) parasite treatment. Self-fertilization rapidly invaded C. elegans host populations in the control and the fixed-parasite treatments, but remained rare throughout the entire experiment in the copassaged treatment. Further, the frequency of the wild-type allele (which permits selfing) was strongly positively correlated with the frequency of self-fertilization across host populations at the end of the experiment. Hence, consistent with the RQH, coevolving parasites can limit the spread of self-fertilization in outcrossing populations.
Department of Biology, Indiana University, Bloomington, IN 47401.
Samuel P
SP
Slowinski
Department of Biology, Emory University, Atlanta, Georgia 30322.
Levi T
LT
Morran
Department of Biology, Indiana University, Bloomington, IN 47401.
Raymond C
RC
Parrish
Department of Biology, Indiana University, Bloomington, IN 47401.
Eric R
ER
Cui
Department of Biology, Indiana University, Bloomington, IN 47401.
Amrita
A
Bhattacharya
Department of Biology, Indiana University, Bloomington, IN 47401.
Curtis M
CM
Lively
Institute of Ecology and Evolution, University of Oregon, Eugene, OR 97403.
Patrick C
PC
Phillips
D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000382:microbiology / Q000502:physiology; D029742:Caenorhabditis elegans Proteins / Q000235:genetics; D019143:Evolution, Molecular; D054884:Host-Pathogen Interactions / Q000235:genetics*; D006824:Hybridization, Genetic; D009154:Mutation; D012641:Selection, Genetic; D057945:Self-Fertilization; D012705:Serratia / Q000235:genetics* / Q000472:pathogenicity
D029742:Caenorhabditis elegans Proteins
Breeding system; Red Queen hypothesis; coevolution; evolution; host-parasite coevolution; sex