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. The challenge, then, is to understand
how interactions can be so highly dynamic and yet persist across landscapes
and millennia. We therefore work at multiple time scales and spatial scales, studying traits and interactions that evolve rapidly and others that evolve more slowly.
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
problems to solve
Our lab’s approach has been to divide
the study of coevolution into three major problems to solve and then
to use a combination of ecological, genetic/molecular, and phylogenetic
techniques to analyze coevolution as a hierarchical process.
1) Species are collections
of genetically distinct populations. Any theory of how coevolution
organizes biodiversity must begin with an 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 problems
from an increasing diversity of perspectives.

Details
of some recent and current studies
How do coevolving interactions
vary across ecosystems, and what can we learn from these studies to help preserve coevolutionary interactions into the future amid environmental change?
Each local interaction between a pair of species, or among a group of species, is a mini-coevolutionary experiment. By studying the same interaction in multiple ecosystems, and asking how these local populations are genetically connected over large regions, we can start getting answers to how coevolution shapes the web of life over large geographic scales.
That requires interactions that are broadly distributed, are found easily in the field, and are easily manipulated both in the field and in the lab. We have studied a wide range of interactions over the past several decades, but one set of interactions has proven particularly useful. These are the interactions between prodoxid moths and their hostplants. Prodoxids includes the yucca moths that have coevolved with yuccas as their obligate pollinators, the Greya moths that are much more variable in their interactions with plants, and some other species.
The interactions between Greya moths and their hostplants have been particularly useful, because these interactions vary from mutualism to antagonism among ecosystems. Unlike yucca moths, Greya moths feed on small herbaceous
plants in the Saxifragaceae and Apiaceae. We have a
molecular phylogeny of the moths and the plants, which has helped us understand how the interaction has diverged as it has spread across large regions. 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.
We are currently focusing on two questions::

• How do coevolving moth and plant traits vary across the thousands of kilometers north to south over which the interaction occurs?
• How does coevolution proceed when multiple species are involved in the interaction rather than just a single pair of species?

What is the geographic scale of local
adaptation in coevolving interactions?
In recent years, we have also used interactions between coastal pines and mycorrhizal
fungi to explore questions on the spatial scale of coevolution. 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 former 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 studies. This work is reaching completion and we are moving on to other interactions to explore questions on the scale of local adaptation.


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

These studies have used 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. These studies are using Pseudomonas bacteria and bacteriophage to evaluate geographic selection mosaics in a very different kind of interaction between bactieria and phage. One of the goals of these studies is to understand the spatial scale at which local coadaptation, coevolutionary hotspots, and coevolutionary coldspots occur in these interactions in the field, rather than in the lab.
How
does coevolution shape large webs of interacting species?
Increasingly, we are asking questions about how large groups of species coevolve. These studies are using mathematical models and available data from other laboratories to ask how coevolution may shape the traits and patterns of specialization within large webs of interacting species. We are currently focusing on interactions among pollinators and plants and similar kinds of mutualistic interactions that are crucial for the functioning of most ecosystems worldwide but are under threat in many ecoystems.
Our mathematical studies of coevolving webs are being led by Paulo Guimarães, who was a postdoctoral associate in our lab and is now an assistant professor at the University of São Paulo, Brazil. 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 this work.
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, we continue to
explore a wide range of related questions on the coevolutionary process. These 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.
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