1. ​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 (non-evolving) 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. 

Mean selfing rates (± one standard error) over the course of the experiment. Host populations were exposed to three different treatments: control (heat-killed S. marcescens; dotted line and triangular markers), fixed-parasite treatment (fixed strain of S. marcescens; dashed line and circle markers), copassaged (copassaged S. marcescens; solid line and square markers) for 33 generations.

2. ­Sedentary dark eyed-juncos (Junco hyemalis) maintain a higher prevalence of Plasmodium infections throughout the winter and early spring than migratory juncos in a seasonally sympatric population
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Long-distance migrations influence the physiology, behavior, and fitness of migratory animals throughout their annual cycles, and fundamentally alter their interactions with parasites. Several hypotheses relating migratory behavior to the likelihood of parasitism have entered the literature, making conflicting, testable predictions. To assess how migratory behavior of hosts is associated with parasitism, we compared haemosporidian parasite infections between two closely related populations of a common North American sparrow, the dark-eyed junco, that co-occur in shared habitats during the non-breeding season. One population is sedentary and winters and breeds in the Appalachian Mountains. The other population is migratory and is found in seasonal sympatry with the sedentary population from October through April, but then flies (900 km) northwards to breed. The populations were sampled in the wild on the shared montane habitat at the beginning of winter and again after confining them in a captive common environment until the spring. We found significantly higher prevalence of haemosporidian parasite infections in the sedentary population. Among infected juncos, we found no difference in parasite densities (parasitemias) between the sedentary and migrant populations and no evidence for winter dormancy of the parasites. Our results suggest that long-distance migration may reduce the prevalence of parasite infections at the population level. Our results are inconsistent with the migratory exposure hypothesis, which posits that long-distance migration increases exposure of hosts to diverse parasites, and with the migratory susceptibility hypothesis, which posits that trade-offs between immune function and migration increase host susceptibility to parasites. However, our results are consistent with the migratory culling hypothesis, which posits that heavily infected animals are less likely to survive long-distance migration, and with the migratory escape hypothesis, which posits that long-distance migration allows host populations to seasonally escape areas of high infection risk. 

​*Bird handling photo credit Ian Nichols

Prevalence of Plasmodium infections (as determined by qPCR) by population and time point. Red bars represent infection prevalence in the sedentary population, blue bars represent infection prevalence in the migrant population. Error bars represent 95% binomial confidence intervals. Asterisks above the bars indicate significant differences in prevalence between populations at each time point. Horizontal bars indicate comparisons in prevalence across time points.