Garter snake eating newtI am an evolutionary biologist with wide interests in how the process of evolution takes place in natural populations. Much of my work focuses on interactions at different levels of biological organization, including coevolution between natural enemies, social interactions between individuals within populations, or epistasis and indirect genetic effects involving specific loci.

Many of the techniques I employ stem from quantitative genetics approaches to understanding variation and selection, but I also incorporate basic fieldwork, behavioral observations, manipulative experiments, and the comparative method. I also use theoretical modeling as a means of understanding some of the more complex sorts of interactions in nature. My work has involved a wide range of study taxa, including reptiles and amphibians, insects, and yes, even plants!

Predator-prey arms races

I continue to explore the coevolution of tetrodotoxin (TTX) toxicity in newts of the genus Taricha and resistance to TTX in garter snakes (Thamnophis). This work ranges from geographic studies of population genetics and structure across the landscape of the interaction, to molecular genetic studies of the basis of adaptive phenotypes, to biophysical studies of the pleiotropic effects of resistance phenotypes on nerve and muscle function. This work involves a broad network of collaborators at different institutions and some really creative and industrious students.

Recent work from Mike Hague in the Brodie Lab has demonstrated that TTX resistance in Thamnophis sirtalis arose twice through a common pathway of amino acid substitutions. A limited number of amino acid substitutions in the voltage gated sodium channel in skeletal muscle (NaV1.4) confer resistance to TTX. In garter snakes, the two resistant alleles in different lineages both began with the same initial change of an isoleucine to a valine, suggesting that this substitution had permissive effects that allowed subsequent increases in resistance.

The evolution of TTX resistance provides some exceptional opportunities to evaluate the predictability of evolutionary adaptation. Together with Charles Hanifin and Shana Geffeney (Utah State University) and Gabriela Toledo in the Brodie Lab, we are beginning to look at the resistance and biophysical impacts of individual amino acid substitutions using gene synthesis and the Xenopus heterologous expression system. By testing specific amino acid substitutions on different ancestral gene backgrounds, we plan to examine the convergence of adaptive walks in distantly related lineages (snakes, newts, fish, and octopus) that have all evolved TTX resistant NaV.

Collaborations with Joel McGlothlin (Virginia Tech) begun when he was a postdoc in the lab identified the diversity of NaV proteins expressed in garter snakes. Sequencing of the nine NaV paralogs in garter snakes revealed that the channels in peripheral nerves were also resistant to TTX, indicating that whole animal resistance requires changes in multiple proteins. A comparative study of NaV proteins across reptiles revealed that resistance of a peripheral nerve channel (NaV1.7) predates the evolution of snakes, and that another nerve channel (NaV1.6) became resistant roughly 50 MYA in four separate lineages. Exaggerated resistance of skeletal muscle (NaV1.4) only evolved in a few groups that already had resistant nerves. This pattern paints a picture of complex historical contingency dictating which species get caught in arms races.

Evolution of Social Behavior and Social Networks

I have a long standing interest in how interactions between conspecifics affect the evolutionary process. This work includes development of indirect genetic effect (IGE) and social selection theory, as well as empirical explorations of these topics.

I am currently exploring the evolution of social network structure and the impact of social network position on fitness in natural populations of the forked fungus beetle (Bolitotherus cornutus). This work is a multi-year field study of natural populations at Mountain Lake Biological Station (MLBS) in collaboration with Vince Formica (Swarthmore). Every year, we are lucky to have a spectacular group of undergraduate research assistants and REU students on the Beetle Crew that make the sampling of field observations of social behavior possible.

Through direct observation and genetic markers, we are able to collect fitness data roughly 500 adult beetles spread between 10-15 populations each season. Each of the beetles in our study area is individually marked with a unique three-letter code. Forked fungus beetles conduct all of their mating and reproductive behaviors on the surfaces of three species of bracket fungi that infect logs and snags in the forest. This structure creates subpopulations with limited exchange of individuals, so we can estimate the structure of social networks on individual logs.

Future work on this system is aimed at trying to understand the factors, genetic and environmental, that influence the structure of social networks. We know that some measures of social network position are consistently expressed by individual beetles in the laboratory. We do not yet know whether there are direct or indirect genetic effects on variation in social network position or group structure that would be required for these social phenotypes to be evolvable characters.

Evolution of G-matrices

G-matrices (genetic variance-covariance matrices) describe the architecture of quantitative genetic variation that underlies continuous traits. The G-matrix determines a population's response to selection in the short term, but its role in longer term evolutionary process is somewhat controversial. G-matrices are expected to evolve in both stochastic and deterministic ways, and may also be influenced by the environment.

Continuing collaborations allow me to explore the contexts in which G evolves, and how and when it influences trajectories of phenotypic diversification. With Lynda Delph (Indiana University) and Janet Steven (Christopher Newport University), I am continuing to analyze the results of experimental manipulations of artificial selection that were designed to test whether strong genetic correlations could be broken in Silene latifolia. We showed that in just a few generations of multivariate selection, extremely strong between sex correlations could be completely erased.

With Joel McGlothlin and Jonathan Losos (Harvard), we are analyzing the results of a massive breeding design that estimated G-matrices in seven species of Caribbean Anolis lizards. The experiment compares the architecture of genetic variation within and among islands, and within and among ectomorphs of lizards. This is the first data set to examine the evolution of G through an adaptive radiation in which history (age of divergence) is not confounded with selection. The results suggest that axes of genetic variation do indeed influence directions of phenotypic evolution over tens of millions of years.