Curtis M. Lively

Parasite adaptation to locally common host genotypes.

According to the Red Queen hypothesis—which states that interactions among species (such as hosts and parasites) lead to constant natural selection for adaptation and counter-adaptation—the disproportionate evolutionary success of parasites on common host genotypes leads to correlated selection for sexual reproduction and local adaptation by the parasite population. Here we determined whether local adaptation is due to disproportionate infection of common host genotypes, and, if so, whether infection of common host genotypes is due to commonness per se, or some other aspect of these genotypes. In a reciprocal cross-inoculation experiment parasites occupying the same geographical area (sympatric) infected locally common host genotypes significantly more often than rare host genotypes, whereas parasites occupying separate geographical areas (allopatric) showed no such significant difference. A mixed source of parasites (containing F1 hybrids) also showed no difference in infection between rare and common host genotypes. These results show that local adaptation results from parasite tracking of locally common host genotypes, and, as such, a necessary condition of the Red Queen hypothesis is met.

MIGRATION, VIRULENCE, AND THE GEOGRAPHIC MOSAIC OF ADAPTATION BY PARASITES

The geographic mosaic theory of coevolution is predicated on structured populations of interacting species where gene flow and the force of selection can vary among populations, leading to a mosaic of traits in space. Here, I briefly review some recent studies of adaptation by a sterilizing parasite to structured populations of a freshwater snail. The results show geographic structure as expected under the geographic mosaic model. I then consider the effects of virulence and migration on local adaptation by parasites using a computer simulation. The results suggest that high virulence and low migration contribute to the strength of local adaptation by parasites. Highly virulent parasites showed adaptation to local hosts for migration rates of up to 10% of the population per generation. In addition, because of the dynamic nature of host‐parasite coevolution, the magnitude of local adaptation fluctuates over time. During some points in the cycle, parasites may be no more effective at infecting individuals from local host populations, even though they would be shown to be locally adapted if examined over enough generations. Contrary to expectation, parasite local adaptation was not affected by giving the parasite a longer generation time than the host, but differences in local selection intensities had a dramatic effect.

HOST-PARASITE COEVOLUTION: EVIDENCE FOR RARE ADVANTAGE AND TIME-LAGGED SELECTION IN A NATURAL POPULATION

In theory, parasites can create time‐lagged, frequency‐dependent selection in their hosts, resulting in oscillatory gene‐frequency dynamics in both the host and the parasite (the Red Queen hypothesis). However, oscillatory dynamics have not been observed in natural populations. In the present study, we evaluated the dynamics of asexual clones of a New Zealand snail, Potamopyrgus antipodarum, and its trematode parasites over a five‐year period. During the summer of each year, we determined host‐clone frequencies in random samples of the snail to track genetic changes in the snail population. Similarly, we monitored changes in the parasite population, focusing on the dominant parasite, Microphallus sp., by calculating the frequency of clones in samples of infected individuals from the same collections. We then compared these results to the results of a computer model that was designed to examine clone frequency dynamics for various levels of parasite virulence. Consistent with these simulations and with ideas regarding dynamic coevolution, parasites responded to common clones in a time‐lagged fashion. Finally, in a laboratory experiment, we found that clones that had been rare during the previous five years were significantly less infectible by Microphallus when compared to the common clones. Taken together, these results confirm that rare host genotypes are more likely to escape infection by parasites; they also show that host‐parasite interactions produce, in a natural population, some of the dynamics anticipated by the Red Queen hypothesis.

Predator-induced shell dimorphism in the acorn barnacle Chthamalus anisopoma

Field experiments were conducted in order to determine the nature of shell dimorphism in the acorn barnacle Chthamalus anisopoma and the adaptive significance of the atypical form. The typical morph has the conical shape which is characteristic of acorn barnacles, while the atypical morph appears bent over, with the rim of its aperture oriented perpendicular to its base. The experiments showed that: 1) the bent‐over morphology is an environmentally‐induced developmental response to the presence of a carnivorous gastropod (Acanthina angelica) and 2) that “bents” are more resistant than “conics” to specialized predation by this snail. The results also showed that predation by A. angelica is patchy and heaviest in the near vicinity of cracks and crevices, which it uses as refuges during periods of tidal inundation. Because predation is patchy and bents are less fecund and grow slower than conics, the conditional developmental strategy is likely to be favored over strict genetical control of shell morphology.

Canalization Versus Developmental Conversion in a Spatially Variable Environment

A model is presented for the evolution of developmental control in a spatially variable environment. Individuals are assumed to disperse at random into one of two patches (one harsh and the other benign) and use one of three developmental strategies for the production of one of two discrete morphological types. Two of the strategies are unconditional (develop as either the stress-tolerant or the nontolerant morph), and the third strategy depends on the environment. Invasion criteria are used to determine the conditions under which each of the three pure strategies are evolutionarily stable and the conditions under which the population is expected to contain some mixture of these strategies at equilibrium. The results demonstrate that environmental control of development requires a cost to the stress-tolerant morphology, and that the average probability of making the right choice is greater than 50%. The range of patch frequencies over which environmental control is stable increases with increases in these two parameters. The results also suggest that the two morphs may be maintained by a mixture of unconditional strategies (i.e., genetically determined polymorphism) for a narrow range of patch frequencies. Unlike the environmentally induced dimorphism, however, the genetically determined dimorphism requires for its maintenance that the morphs compete within the patches for resources. Finally, the results suggest that a mixture of genetic and environmental control is an evolutionarily stable state under some conditions. These conditions are the same as those required for the maintenance of genetically determined dimorphism, except that the average probability of making the right choice must be greater than 50%. Under mixed control, some fraction of the population shows canalized development and the remaining fraction shows developmental conversion when exposed to the appropriate cue. That such a mixture of strategies could persist in evolutionary time might explain the results of some studies that indicate partial genetic and partial environmental control of phenotypes.

Adaptation by a parasitic trematode to local populations of its snail host

In each of two reciprocal cross‐infection experiments, a digenetic trematode (Microphallus sp.) was found to be significantly more infective to snails (Potamopyrgus antipodarum) from its local host populations. This gives strong evidence for local adaptation by the parasite and indicates that there is a genetic basis to the host–parasite interaction. It is suggested that the parasite should be able to track common snail genotypes within populations and, therefore, that it could be at least partially responsible for the persistence of sexual subpopulations of the snail in those populations that have both obligately sexual and obligately parthenogenetic females.

Running with the Red Queen: Host-parasite coevolution selects for biparental sex

Outcrossing provides better survival than self-fertilization during coevolution between a host and its parasite. Most organisms reproduce through outcrossing, even though it comes with substantial costs. The Red Queen hypothesis proposes that selection from coevolving pathogens facilitates the persistence of outcrossing despite these costs. We used experimental coevolution to test the Red Queen hypothesis and found that coevolution with a bacterial pathogen (Serratia marcescens) resulted in significantly more outcrossing in mixed mating experimental populations of the nematode Caenorhabditis elegans. Furthermore, we found that coevolution with the pathogen rapidly drove obligately selfing populations to extinction, whereas outcrossing populations persisted through reciprocal coevolution. Thus, consistent with the Red Queen hypothesis, coevolving pathogens can select for biparental sex.

THE GEOGRAPHY OF COEVOLUTION: COMPARATIVE POPULATION STRUCTURES FOR A SNAIL AND ITS TREMATODE PARASITE

Gene flow and the genetic structure of host and parasite populations are critical to the coevolutionary process, including the conditions under which antagonistic coevolution favors sexual reproduction. Here we compare the genetic structures of different populations of a freshwater New Zealand snail (Potamopyrgus antipodarum) with its trematode parasite (Microphallus sp.) using allozyme frequency data. Allozyme variation among snail populations was found to be highly structured among lakes; but for the parasite there was little allozyme structure among lake populations, suggesting much higher levels of parasite gene flow. The overall pattern of variation was confirmed with principal component analysis, which also showed that the organization of genetic differentiation for the snail (but not the parasite) was strongly related to the geographic arrangement of lakes. Some snail populations from different sides of the Alps near mountain passes were more similar to each other than to other snail populations on the same side of the Alps. Furthermore, genetic distances among parasite populations were correlated with the genetic distances among host populations, and genetic distances among both host and parasite populations were correlated with “stepping‐stone” distances among lakes. Hence, the host snail and its trematode parasite seem to be dispersing to adjacent lakes in a stepping‐stone fashion, although parasite dispersal among lakes is clearly greater. High parasite gene flow should help to continuously reintroduce genetic diversity within local populations where strong selection might otherwise isolate “host races.” Parasite gene flow can thereby facilitate the coevolutionary (Red Queen) dynamics that confer an advantage to sexual reproduction by restoring lost genetic variation.

The Red Queen and Fluctuating Epistasis: A Population Genetic Analysis of Antagonistic Coevolution

Host‐parasite coevolution has been shown to provide an advantage to recombination, but the selective mechanism underlying this advantage is unclear. One possibility is that recombination increases the frequency of advantageous genotypes that are disproportionately rare because of fluctuating epistasis. However, for this mechanism to work, epistasis for fitness must fluctuate over a very narrow timescale: two to five generations. Alternatively, recombination may speed up the response to directional selection by breaking up linkage disequilibria that decrease additive genetic variance. Here we analyze the results of a numerical simulation of host‐parasite coevolution to assess the importance of these two mechanisms. We find that linkage disequilibria may tend to increase, rather than decrease, additive genetic variance. In addition, the sign of epistasis changes every two to five generations under several of the parameter values investigated, and epistasis and linkage disequilibrium are frequently of opposite signs. These results are consistent with the idea that selection for recombination is mediated by fluctuating epistasis. Finally, we explore the conditions under which an allele causing free recombination can spread in a nonrecombining host population and find general agreement between the predictions of a population genetic model of fluctuating epistasis and our simulation model.

The Maintenance of Sex, Clonal Dynamics, and Host‐Parasite Coevolution in a Mixed Population of Sexual and Asexual Snails

Sexual populations should be vulnerable to invasion and replacement by ecologically similar asexual females because asexual lineages have higher per capita growth rates. However, as asexual genotypes become common, they may also become disproportionately infected by parasites. The Red Queen hypothesis postulates that high infection rates in the common asexual clones could periodically favor the genetically diverse sexual individuals and promote the short‐term coexistence of sexual and asexual populations. Testing this idea requires comparison of competing sexual and asexual lineages that are attacked by natural parasites. To date no such data have been available. Here, we report on long‐term dynamics and parasite coevolution in a “mixed” (sexual and asexual) population of snails (Potamopyrgus antipodarum). We found that, within 7–10 years, the most common clones were almost completely replaced by initially rare clones in two different habitats, while sexuals persisted throughout the study period. The common clones, which were initially more resistant to infection, also became more susceptible to infection by sympatric (but not allopatric) parasites over the course of the study. These results are consistent with the Red Queen hypothesis and show that the coevolutionary dynamics predicted by the theory may also favor sexual reproduction in natural populations.