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Host-Parasite Coevolution

Research Summary

Dan Bolnick is studying the ecological basis for geographic variation in parasite abundance, and how the immune system evolves in response to this geographic variation. He is using an emerging model organism, the threespine stickleback (Gasterosteus aculeatus), for this research.

Many host-parasite interactions take place in a complex geographic landscape. Environmental conditions such as climate, geology, and species composition vary across this landscape and can influence host-parasite interactions. My lab is investigating how the behavior and immune system of hosts evolve to adapt to parasites, and how this evolution is facilitated or constrained by geographic heterogeneity.

Threespine Stickleback as a Model Organism
The threespine stickleback (Gasterosteus aculeatus) is an emerging model organism in evolutionary genetics, due to the incredible diversity of this species. After the last ice age (~12,000 years ago) marine sticklebacks colonized freshwater habitats throughout northern Europe and North America. Sticklebacks invaded thousands of independent watersheds, providing us with a highly replicated 12,000-year-old evolutionary experiment as they diverged to adapt to many different habitats: estuaries, rivers, streams, marshes, and lakes of all sizes. Across these habitats, sticklebacks exhibit remarkable variation in size, behavior, skeletal morphology, feeding ecology, and breeding color. A growing community of biologists is studying the ecological and genetic basis for this diversity, aided by the development of a genetic linkage map, SNP array, and complete genome sequence (David Kingsley, HHMI, Stanford University School of Medicine).

A Geographic Mosaic of Parasites
My lab has found dramatic variation in parasite loads among stickleback populations. On northern Vancouver Island, sticklebacks in nearby lakes can have infection rates that span orders of magnitude: cestode infection rates can range from 0.00 percent up to more than 80 percent. Even more dramatically, adjoining lake and stream populations of sticklebacks exhibit almost non-overlapping parasite communities, despite being directly connected and subject to ongoing migration. This variation presents an exciting opportunity to examine how a vertebrate species adapts to spatially complex parasite communities. Our hope is that the principles uncovered from such a study can also be applied to understand the interaction between humans and our own geographically complex parasite communities.

Our first task has been to determine why parasite abundances and identities differ so dramatically among populations. One possibility is that parasite incidence is determined mostly by environmental parameters (e.g., water chemistry, presence of intermediate hosts). Consistent with this hypothesis, we have found correlations between habitat type and parasite incidence. A second hypothesis is that variation in parasite loads among populations is the result of coevolutionary oscillations. Hosts and their parasites are continually evolving new immunological defenses (or attack strategies). Recent theoretical models suggest that this coevolution leads to times when the host is "winning" and the parasites are rare, and times when the parasite is winning and is more abundant. If populations are sufficiently isolated from each other, they may be at different stages in such cycles, resulting in variation in parasite abundance. Reciprocal transplants of fish between alternate environments are helping us test this second possibility. We can thus determine whether parasite abundance is driven by the external environment or driven by the vulnerability of the hosts. This distinction is critical, because only in the former case will hosts be well adapted to locally common parasites.

Our next goal is to identify the genetic differences among stickleback populations that underlie differences in resistance (or vulnerability) to local parasites. Using both laboratory and field experiments, we are mapping the genomic location of quantitative trait loci (QTL) that influence the probability of infection. In addition, we are evaluating the effect of candidate genes, such as the major histocompatibility complex (MHC class IIB). The simplest possibility is that familiar immune system genes such as MHC are the primary means by which sticklebacks adapt to local parasites. It is also possible, however, that adaptation to parasites mostly entails avoidance or tolerance. For instance, sticklebacks could avoid cestodes by eliminating copepods (the intermediate host) from their diet. Thus, the behavioral ecology of the host may be fundamental to the host-parasite interaction. Tolerance might evolve when hosts cannot avoid or eliminate the parasite, but instead evolve to mitigate physiological effects of a given infection. By mapping the genes for antiparasite adaptations, we can determine the relative roles of host ecology, immunology, and physiology.

Evolution of Immune System Genes in a Geographic Mosaic
Once we have identified the gene(s) that play key roles in adapting to divergent parasite communities, we can begin to examine the evolutionary dynamics of these genes. In particular, what is the relationship between parasite load and selection on alleles at each candidate locus? Are specific alleles favored in the presence of specific parasites, or does selection favor allelic diversity per se? To answer these questions, we are using a combination of field experiments and population genetic models. In the field experiments, we expose different fish genotypes to different parasite communities, determine their infection rates, and directly measure fitness effects of alternate alleles at candidate loci.

The population genetic models take advantage of the natural 12,000-year-old experiment that has created many distinct watersheds with parallel examples of adaptation. We first use genetic markers throughout the genome to determine patterns of relatedness due to recent common ancestry and/or migration. We have found that populations within a watershed are each other's closest relatives. Within a watershed, genetic similarity between populations depends strongly on the steepness of streams separating habitable environments. In comparison to the background genome, genes involved in parasite avoidance, resistance, or tolerance will tend to be more divergent when parasite communities are divergent, or more similar if parasite communities are similar. By applying coalescent models, we can estimate the strength of selection on these genes, thereby determining the extent to which parasites are able to drive immune system evolution.

Within-Population Variability
Until recently, the major focus of my research has been to understand the evolutionary and ecological forces that maintain genetic variation within natural populations. Using theory and laboratory and field experiments, we have shown that Malthusian competition for resources generates strong natural selection that maintains genetic variation: individuals that use a unique resource are able to sidestep competition with their peers. As a result of this diversifying natural selection, individuals show distinctive "personalities" when it comes to selecting food resources. In sticklebacks, some individuals specialize on eating zooplankton, while other members of the same population specialize on eating insect larvae. We have shown that this dietary individuality is a common feature of species throughout the animal kingdom, from gastropods to insects, fish, birds, and mammals. Our work is thus beginning to shed light on the evolutionary origins of personality. We are continuing to investigate the mechanistic basis of individual variation by evaluating the roles of biomechanics, learning, gut microbial fauna, and social interactions in producing dietary variation.

One consequence of individuality in natural populations is that individuals may vary in parasite exposure. For instance, within a given population some individual sticklebacks prefer to eat copepods, and thus are infected by the tapeworm Schistocephalus solidus, whereas other individuals avoid copepods. This within-population variation in parasite exposure raises several questions. First, is individual foraging behavior dictated by immune system genotype (i.e., do sticklebacks select prey when they are well defended against associated parasites)? Second, how does ecological subdivision of the host population affect parasite population dynamics? Pathogens often require some minimum host population density to persist, and diet variation within the host population may reduce the effective number of hosts below this threshold, thus eliminating certain parasites.

A grant from the David and Lucile Packard Foundation provides partial support for these projects. Research on the maintenance of genetic variation within populations has received past support from the National Science Foundation.

As of May 30, 2012

Scientist Profile

Early Career Scientist
University of Texas at Austin
Experimental Evolutionary Biology, Genetics