Parasites evolve numerous strategies to manipulate and evade host defenses. And depending on the the cost of infection, hosts can evolve to resist or tolerate parasites. This reciprocal antagonism can drive rapid evolution (hence the Red Queen cartoon from Through the Looking Glass). Although there are numerous population genetic models that aim to explain how this process might proceed, they all rely on assumptions about how host and parasite genetic variation are connected to infection success. At present, there is limited empirical data to test these models, especially with respect to vertebrate hosts. Our work aims to fill this gap, and to answer fundamental questions such as:
- What genetic changes underlie host-parasite coevolution?
- How often are new genes or strategies deployed, as opposed to recycling existing variation?
- How does gene flow among many populations impact the rate and trajectory of (co)evolution?
- What ecological conditions lead to quantitative variation in selection, and how does this variation affect the genetic architecture of adaptations?
Sticklebacks and tapeworms: A powerful model for coevolutionary genetics
1) Plentiful natural diversity
- Marine threespine stickleback (Gasterosteus aculeatus) are highly susceptible to Schistocephalus solidustapeworms, but freshwater populations across the globe have evolved to resist the parasite. Interestingly, freshwater fish in different areas evolved resistance via different mechanisms, and parasites evolved to counter the resistance of their local hosts (Weber et al 2016).
2) Lab-based infections
- We can replicate the parasite’s complex life cycle in the lab. This allows us to perform thousands of controlled exposures between different host and parasite populations.
3) Excellent genomic resources
- The threespine stickleback genome is both sequenced and annotated (Ensembl). A draft genome of the parasite is available at ParaSite.WormBase.org.
4) MANY interesting traits
- The picture below shows traits that differ between fish from a High-infection Lake (H) and a No-infection Lake (N) (Weber et al (2017) PNAS)
Peromyscus is a genus of new world mice containing more than 50 species that exhibit astounding levels of diversity. These mice have adapted to most terrestrial habitats in North America, with some species diversifying into numerous ecotypes. This extreme diversity has long interested biologists, and recent studies have started to dissect the genetic, physiological, and environmental basis of adaptive differences. For example, Dr. Weber collaborated with Drs. Cynthia Steiner and Hopi Hoekstra to identify which genes evolved to create extremely light coat color in beach mice (P. polionotus leucocephalus; image to right), which helps them match the substrates on which they live.
Sexual selection manifests itself in many forms, including the extraordinarily large appendages that males use to defend territories and secure access to females. These structures range from the well-known antlers and tusks found in numerous mammals, to the enormous namesakes of stalk-eyed flies. While it is clear that large weapons are likely to both benefits and costs to their owners, there are few case studies that test ecological, genetic, and developmental predictions about what causes weaponry arms-races to escalate or fall apart.
Rhinoceros beetles as a model for sexually selected weapons
As a postdoc in the Emlen Lab, Dr. Weber examined the evolution of horn length in the Japanese rhinoceros beetle (Trypoxylus dichotomus, photo upper right). The species is distributed throughout China, Taiwan, the Korean peninsula, and Japan. In some populations, males develop large horns that they use to defend sap sites on hardwood trees, where female beetles frequently feed. But in other populations males develop relatively small horns. Females lack horns in all populations. The Emlen Lab and collaborators have already amassed a large knowledge about the developmental processes that give rise to horns. They extending this work by sequencing thousands of genetic loci and building a phylogeny from a geographically and morphologically diverse sample of rhino beetles (figure below). They also examined behavioral variation between the morphs in both field and lab settings. Together, this enabled us to address some of these questions:
- How many times has horn length increased or decreased?
- What ecological conditions drive increases or decreases in horn length?
- What genes and developmental pathways influence horn evolution?
- Are there costs or constraints to horn size?
- Do combat-related behaviors evolve in concert with horn evolution?
The lab’s research explores the process of adaptation in animals. Specifically, “how” and “why” do animals evolve complex traits to manage environmental pressures? To answer these questions, we draw from tools and theory associated with the fields of behavioral ecology, bioinformatics and genomics, biomechanics, ecology, evolutionary biology, immunology, molecular genetics, and quantitative genetics.
All projects employ the following approaches:
1) Identify traits that vary in ecologically meaningful ways
2) Characterize the locus (or loci) of evolution
- Identify the chromosomal regions (and lists of genes/mutations)
- Describe molecular and functional differences between alleles
- Experimentally manipulate interesting candidate genes in the lab
3) Test how alleles affect fitness in the wild
- Experiments that manipulate both genetic background and environment
- Comparative approaches that test for correlations between genetic changes and environmental variation, using data from many populations and species.
- Long-term field studies that measure allele frequency fluctuations across many generations.