Levi T. Morran

Experimental Coevolution: Rapid Local Adaptation by Parasites Depends on Host Mating System*

Host-parasite interactions can drive rapid, reciprocal genetic changes (coevolution), provided both hosts and parasites have high heritabilities for resistance/infectivity. Similarly, the host’s mating system should also affect the rate of coevolutionary change in host-parasite interactions. Using experimental coevolution, we determined the effect of obligate outcrossing verses partial self-fertilization (mixed mating) on the rate of evolutionary change in a nematode host (Caenorhabditis elegans) and its bacterial parasite (Serratia marcescens). Bacterial populations were derived from a common ancestor. We measured the effects of host mating system on host adaptation to the parasite. We then determined the extent of parasite adaptation to their local host populations. Obligately outcrossing hosts exhibited more rapid adaptation to parasites than did mixed mating hosts. In addition, most of the parasites became adapted to infecting their local hosts, but parasites from obligately outcrossing hosts showed a greater level of local adaptation. These results suggest that host populations evolved along separate trajectories and that outcrossing host populations diverged further than partially selfing populations. Finally, parasites tracking outcrossing host populations diverged further than parasites tracking the partially selfing host populations. These results show that the evolutionary trajectories of both hosts and parasites can be shaped by the host’s mating system.

Experimental Evolution as an Underutilized Tool for Studying Beneficial Animal-Microbe Interactions.

Microorganisms play a significant role in the evolution and functioning of the eukaryotes with which they interact. Much of our understanding of beneficial host–microbe interactions stems from studying already established associations; we often infer the genotypic and environmental conditions that led to the existing host–microbe relationships. However, several outstanding questions remain, including understanding how host and microbial (internal) traits, and ecological and evolutionary (external) processes, influence the origin of beneficial host–microbe associations. Experimental evolution has helped address a range of evolutionary and ecological questions across different model systems; however, it has been greatly underutilized as a tool to study beneficial host–microbe associations. In this review, we suggest ways in which experimental evolution can further our understanding of the proximate and ultimate mechanisms shaping mutualistic interactions between eukaryotic hosts and microbes. By tracking beneficial interactions under defined conditions or evolving novel associations among hosts and microbes with little prior evolutionary interaction, we can link specific genotypes to phenotypes that can be directly measured. Moreover, this approach will help address existing puzzles in beneficial symbiosis research: how symbioses evolve, how symbioses are maintained, and how both host and microbe influence their partner’s evolutionary trajectories. By bridging theoretical predictions and empirical tests, experimental evolution provides us with another approach to test hypotheses regarding the evolution of beneficial host–microbe associations.

Nematode-bacteria mutualism: Selection within the mutualism supersedes selection outside of the mutualism.

The coevolution of interacting species can lead to codependent mutualists. Little is known about the effect of selection on partners within verses apart from the association. Here, we determined the effect of selection on bacteria (Xenorhabdus nematophila) both within and apart from its mutualistic partner (a nematode, Steinernema carpocapsae). In nature, the two species cooperatively infect and kill arthropods. We passaged the bacteria either together with (M+), or isolated from (M−), nematodes under two different selection regimes: random selection (S−) and selection for increased virulence against arthropod hosts (S+). We found that the isolated bacteria evolved greater virulence under selection for greater virulence (M−S+) than under random selection (M−S−). In addition, the response to selection in the isolated bacteria (M−S+) caused a breakdown of the mutualism following reintroduction to the nematode. Finally, selection for greater virulence did not alter the evolutionary trajectories of bacteria passaged within the mutualism (M+S+ = M+S−), indicating that selection for the maintenance of the mutualism was stronger than selection for increased virulence. The results show that selection on isolated mutualists can rapidly breakdown beneficial interactions between species, but that selection within a mutualism can supersede external selection, potentially generating codependence over time.

The evolution of reduced antagonism—A role for host–parasite coevolution

Why do some host–parasite interactions become less antagonistic over evolutionary time? Vertical transmission can select for reduced antagonism. Vertical transmission also promotes coevolution between hosts and parasites. Therefore, we hypothesized that coevolution itself may underlie transitions to reduced antagonism. To test the coevolution hypothesis, we selected for reduced antagonism between the host Caenorhabditis elegans and its parasite Serratia marcescens. This parasite is horizontally transmitted, which allowed us to study coevolution independently of vertical transmission. After 20 generations, we observed a response to selection when coevolution was possible: reduced antagonism evolved in the copassaged treatment. Reduced antagonism, however, did not evolve when hosts or parasites were independently selected without coevolution. In addition, we found strong local adaptation for reduced antagonism between replicate host/parasite lines in the copassaged treatment. Taken together, these results strongly suggest that coevolution was critical to the rapid evolution of reduced antagonism.

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.

The Integral Role of Genetic Variation in the Evolution of Outcrossing in the Caenorhabditis elegans-Serratia marcescens Host-Parasite System

Outcrossing is predicted to facilitate more rapid adaptation than self-fertilization as a result of genetic exchange between genetically variable individuals. Such genetic exchange may increase the efficacy of selection by breaking down Hill-Robertson interference, as well as promoting the maintenance of within-lineage genetic diversity. Experimental studies have demonstrated the selective advantage of outcrossing in novel environments. Here, we assess the specific role of genetic variation in the evolution of outcrossing. We experimentally evolved genetically variable and inbred populations of mixed mating (outcrossing and self-fertilizing) Caenorhabditis elegans nematodes under novel ecological conditions—specifically the presence of the virulent parasite Serratia marcescens. Outcrossing rates increased in genetically variable host populations evolved in the presence of the parasite, whereas parasite exposure in inbred populations resulted in reduced rates of host outcrossing. The host populations with genetic variation also exhibited increased fitness in the presence of the parasite over eight generations, whereas inbred populations did not. This increase in fitness was primarily the result of adaptation to the parasite, rather than recovery from initial inbreeding depression. Therefore, the benefits of outcrossing were only manifested in the presence of genetic variation, and outcrossing was favored over self-fertilization as a result. As predicted, the benefits of outcrossing under novel ecological conditions are a product of genetic exchange between genetically diverse lineages.

Restoration of pyrethroid susceptibility in a highly resistant Aedes aegypti population

Insecticide resistance has evolved in disease vectors worldwide, creating the urgent need to either develop new control methods or restore insecticide susceptibility to regain use of existing tools. Here we show that phenotypic susceptibility can be restored in a highly resistant field-derived strain of Aedes aegypti in only 10 generations through rearing them in the absence of insecticide.

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

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.

Evolution of Caenorhabditis elegans host defense under selection by the bacterial parasite Serratia marcescens

Parasites can impose strong selection on hosts. In response, some host populations have adapted via the evolution of defenses that prevent or impede infection by parasites. However, host populations have also evolved life history shifts that maximize host fitness despite infection. Outcrossing and self-fertilization can have contrasting effects on evolutionary trajectories of host populations. While selfing and outcrossing are known to affect the rate at which host populations adapt in response to parasites, these mating systems may also influence the specific traits that underlie adaptation to parasites. Here, we determined the role of evolved host defense versus altered life history,in mixed mating (selfing and outcrossing) and obligately outcrossing C. elegans host populations after experimental evolution with the bacterial parasite, S. marcescens. Similar to previous studies, we found that both mixed mating and obligately outcrossing host populations adapted to S. marcescens exposure, and that the obligately outcrossing populations exhibited the greatest rates of adaptation. Regardless of the host population mating system, exposure to parasites did not significantly alter reproductive timing or total fecundity over the course of experimental evolution. However, both mixed mating and obligately outcrossing host populations exhibited significantly reduced mortality rates in the presence of the parasite after experimental evolution. Therefore, adaptation in both the mixed mating and obligately outcrossing populations was driven, at least in part, by the evolution of increased host defense and not changes in host life history. Thus, the host mating system altered the rate of adaptation, but not the nature of adaptive change in the host populations.

Turnover in local parasite populations temporarily favors host outcrossing over self-fertilization during experimental evolution

Abstract The ubiquity of outcrossing in plants and animals is difficult to explain given its costs relative to self‐fertilization. Despite these costs, exposure to changing environmental conditions can temporarily favor outcrossing over selfing. Therefore, recurring episodes of environmental change are predicted to favor the maintenance of outcrossing. Studies of host–parasite coevolution have provided strong support for this hypothesis. However, it is unclear whether multiple exposures to novel parasite genotypes in the absence of coevolution are sufficient to favor outcrossing. Using the nematode Caenorhabditis elegans and the bacterial parasite Serratia marcescens, we studied host responses to parasite turnover. We passaged several replicates of a host population that was well‐adapted to the S. marcescens strain Sm2170 with either Sm2170 or one of three novel S. marcescens strains, each derived from Sm2170, for 18 generations. We found that hosts exposed to novel parasites maintained higher outcrossing rates than hosts exposed to Sm2170. Nonetheless, host outcrossing rates declined over time against all but the most virulent novel parasite strain. Hosts exposed to the most virulent novel strain exhibited increased outcrossing rates for approximately 12 generations, but did not maintain elevated levels of outcrossing throughout the experiment. Thus, parasite turnover can transiently increase host outcrossing. These results suggest that recurring episodes of parasite turnover have the potential to favor the maintenance of host outcrossing. However, such maintenance may require frequent exposure to novel virulent parasites, rapid rates of parasite turnover, and substantial host gene flow.