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Summary of our laboratory’s research

Our laboratory’s research is devoted to developing a robust framework for the science of coevolutionary biology. The major problem we are pursuing is how the process of coevolution organizes the earth's biodiversity. Coevolution is reciprocal evolution between interacting species driven by natural selection. It is responsible for many of the major events in the history of life, and it is a major force in the organization of biological communities. The coevolutionary process shapes interacting networks of species at local levels, regional levels, and global levels. It weaves the threads of biodiversity into a rich and resilient fabric.

We now know that coevolution is a relentless process, creating ever-changing geographic mosaics in how species interact with one another. Populations of one species often become adapted to local populations of other species.

We also now know that these local coevolutionary changes can sometimes occur on time scales of less than a hundred years, indicating that there is often no real difference between ecological time and evolutionary time. Despite this constant change, some coevolving interactions persist for millions of years. The challenge, then, is to understand how highly dynamic interactions coevolve and persist across landscapes and millennia.

The Geographic Mosaic Theory of Coevolution

The geographic mosaic theory of coevolution argues that coevolving interactions have three components that collectively drive ongoing coevolutionary change:

Geographic selection mosaics: Natural selection on interspecific interactions varies among populations partly because there are geographic differences in how fitness in one species depends upon the distribution of genotypes in another species. That is, there is often a genotype-by-genotype-by-environment interaction in fitnesses of interacting species.

Coevolutionary hotspots: Interactions are subject to reciprocal selection only within some local communities. These coevolutionary hotspots are embedded in a broader matrix of coevolutionary coldspots, where local selection is non-reciprocal or where only one of the participants occurs.

Trait remixing: The genetic structure of coevolving species changes through new mutations, gene flow across landscapes, random genetic drift, and extinction of local populations. These processes contribute to the shifting geographic mosaic of coevolution by continually altering the spatial distributions of potentially coevolving genes and traits.

Understanding how these components of the coevolutionary process interact is becoming increasingly important as climate change, fragmentation of environments, and spread of invasive species are changing our biological landscapes worldwide.

We use a combination of ecological, populational, molecular, phylogeographic, and mathematical approaches to probe the structure and dynamics of coevolving interactions. We study a wide range of interactions from antagonistic to mutualistic, using a wide range of taxa. In recent years, we have used interactions as different as those between pollinators and herbaceous plants, mycorrhizal fungi and conifers, and bacteria and bacteriophage to explore how coevolution proceeds in different forms of interaction. All our work is directed toward understanding the links among microevolutionary processes (evolutionary dynamics within local populations), mesoevolutionary processes (geographic mosaics of evolving and coevolving species) and macroevolutionary patterns (the patterns observed among diversifying lineages).

The three major focus areas

Our lab’s approach has been to divide the study of coevolution into three major focus areas and then to use a combination of ecological, genetic/molecular, and phylogenetic techniques to analyze coevolution as a hierarchical process.

1) Almost all species are collections of genetically distinct populations. Any theory of how coevolution organizes biodiversity must begin with an empirical understanding of this nearly universal property of species, and of how it influences local adaptation and specialization in interacting organisms.

2) Coevolving interactions are often locally transient and geographically variable, yet many persist regionally for millions of years. An important goal of coevolutionary biology is therefore to understand how the temporal and geographic dynamics of interspecific interactions shape coevolution.

3) Coevolving interactions commonly form networks of species rather than simply pairs of species. The problem to solve is whether coevolution shapes these networks in predictable ways.

Most of the published papers from our laboratory, including my three books on coevolution (Thompson 1982, 1994, 2005), address these three central foci from an increasing diversity of perspectives.

Details of some recent and current studies

How do coevolving interactions vary across broad geographic landscapes, and what can we learn from these studies to help preserve coevolutionary interactions into the future amid environmental change?

We are using the interactions between Greya moths and their hostplants to evaluate these questions. These moths are the closest living relatives of yucca moths, whose interactions with yuccas are one of the classic textbook cases of coevolution between mutualists. Unlike yucca moths, Greya moths feed on small herbaceous plants in the Saxifragaceae and Apiaceae, and the interactions range geographically from antagonism to mutualism. We have a molecular phylogeny of the moths and the plants. We also have developed a large-scale molecular phylogeographic database for Greya politella, the most widely distributed member of the genus, and we have similar genetic data for the two major lineages of hostplants used by Greya politella: Lithophragma and Heuchera. These past and ongoing studies have provided us with a molecular template for understanding how populations, traits, and ecological outcomes with hostplants have evolved across western North America. Current studies using these interactions are exploring two lines of inquiry:

• How do moth and plant traits, and the ecological outcomes associated with these traits, vary over the thousands of kilometers north to south in western North America in which the interaction occurs? John Thompson, Anna Liisa-Laine (University of Helsinki), Christopher Schwind, and multiple other current and past members of the laboratory are involved in these studies.

• How do local networks of related species of Greya moths and related species of their hostplants vary geographically? What is the comparative phylogeographic structure of these coevolving networks?

What is the geographic scale of local adaptation in coevolving interactions?

In recent years, we have used interactions between coastal pines and mycorrhizal fungi to explore this question. These studies have taken advantage of the observation that several species of pine are restricted to a narrow band of coastal environments from Alaska to Baja California, and these pines harbor specialized mycorrhizal fungi in the genus Rhizopogon. That structure makes it easier than in many interactions to interpret the geographic scale of local coadaptation. Jason Hoeksema, a postdoctoral associate in our lab who is now an assistant professor at University of Mississippi, has led the work on these continuing studies. Christopher Schwind, who is currently our laboratory manager, has been closely involved with the day-to-day maintenance of these experiments.

How do geographic selection mosaics and gene flow shape the rate and trajectory of coevolving interactions?

These studies are using laboratory microcosms of E. coli and T7 phage to explore the dynamics of rapid coevolution. The experiments have been designed to test specific predictions of the geographic mosaic theory of coevolution. The work involves experimentally induced coevolution followed by sequencing of the genes undergoing selection. These studies began as a collaboration between our laboratory and Brendan Bohannan’s laboratory at Oregon State University, with Samantha Forde as the postdoctoral associate who spearheaded this work. Robert Holt from University of Florida and Ivana Gudelj and Robert Beardmore, both from Imperial College, London have been closely involved in the modelling aspects of these studies in recent years. Samantha Forde is now an adjunct faculty member at UCSC, and we continue to collaborate on these studies.

Our laboratory is now also involved in a new collaboration on microbial coevolution with Angus Buckling's laboratory at Oxford University. Postdoctoral associate Britt Koskella is leading that effort and is working currently at Oxford University. These studies are using Pseudomonas bacteria and bacteriophage to evaluate geographic selection mosaics in a very different kind of interaction between bactieria and phage.

How does coevolution mold large webs of interacting species?

These studies are using mathematical models and available data from other laboratories to ask how coevolution may shape the traits and patterns of specialization of interacting species in communities in which many species are involved in an interaction. Current work is focused on interactions among pollinators and plants and similar kinds of mutualistic interactions that are crucial for the functioning of most ecosystems worldwide.

Our mathematical studies of coevolving webs are being led by postdoctoral associate Paulo Guimarães, who has extensive training in network theory. Pedro Jordano from the Estación Biológica de Doñana in Seville, Spain is collaborating directly with us on this work and Jordi Bascompte, from the same institute, has provided ongoing insights into topology of species networks.

We are also collaborating with Victor Rico-Gray from the Instituto de Ecología in Xalapa on analyses of temporal changes in networks of ant-plant interactions in Mexico amid invasion by new ant species. These studies are taking advantage of large datasets that he and Cecilia Diaz, also from the Instituto de Ecología, have collected during the past decade.

Other Research Questions

In addition to these questions, our laboratory is continuing to explore a wide range of related questions on how the genetic, geographic, phylogenetic, and ecological structure of species shapes the coevolutionary process. Our efforts include investigations into how the evolution of plant polyploidy has shaped coevolution between plants and animals, how outcomes of interactions vary temporally on the time scale of decades, and how changes in species ranges and the introduction of novel species may alter the dynamics of coevolution.