of our laboratory’s research
laboratory’s research is devoted to developing a robust
framework for the science of coevolutionary biology. We are attempting to understand how the process of coevolution contributes to the organization of
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 organizing the web of life. Coevolution shapes networks of interacting species
at local levels, regional levels, and global levels. It weaves
the threads of biodiversity into a rich and resilient fabric.
Coevolution, like all evolution, is a relentless
process, creating ever-changing geographic mosaics in how species
interact with one another. Local populations of one species often become
adapted to local populations of other species. Even the same species of predators and prey, parasites and hosts, competitors, and mutualists interact and coevolve with each other in different ways in different ecosystems. The connections among local populations create a kaleidoscope of patterns of adaptation over larger geographic scales. At a time when ecosystems are changing quickly worldwide, it has become increasingly important for us to understand how environmental changes affect the evolution of interactions among species at local scales through global scales.
These evolutionary changes can occur quickly. Local coevolutionary changes can sometimes occur on time
scales of only a few decades, indicating that there is
often no real difference between ecological time and evolutionary
time. The challenge is to understand
how interactions can be so highly dynamic and yet sometimes persist across landscapes
and millennia. If we can understand how persistence occurs in relatively unmodified ecosystems, then we will be in a much better position to manage the earth's biodiversity in the increasingly human-dominated ecosystems worldwide.
In our research, we therefore work at multiple time scales and spatial scales, studying some traits and interactions that evolve rapidly and others that evolve more slowly. We study populations in relatively pristine environments, populations in highly modified environments, populations living in experimental microcosms where we observe evolution under highly controlled conditions, and mathematical models to help guide our questions and interpretations. We study a wide range of species, including microbes, plants, fungi, insects, and vertebrates, looking for common patterns and processes that shape of life.
Geographic Mosaic Theory of Coevolution
geographic mosaic theory of coevolution argues that coevolving
interactions have three components that collectively drive ongoing
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
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
We have studied the geographic of coevolution in interactions
ranging from those are antagonistic to others that are mutualistic.
In recent years, we have used interactions as different as those
between pollinators and herbaceous plants, mycorrhizal fungi
and conifers, and bacteria and bacteriophages 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 begins with three observations and the evolutionary and coevolutionary questions that follow from those observations:
1) Species are collections
of genetically distinct populations. Our studies of evolution and coevolution begin with this nearly universal property of species. We are trying to understand how adaptation begins with selection on local populations, and is then reshaped over large geographic scales through genetic connections among populations.
2) Local populations are often transient, but interactions between species sometimes persist for millions of years. We are trying to understand the ecological and genetic conditions that allow long-term persistence of interactions and how human activities may be altering those conditions.
3) Coevolving interactions often form webs of species
rather than simply pairs of species. We are trying to understand how coevolution shapes these webs and whether the webs evolve in predictable
ways under different ecological conditions.
Most of the published papers
from our laboratory, my three books on coevolution
(Thompson 1982, 1994, 2005) and my book on why evolution is relentless (Thompson 2013), address these central problems
from multiple perspectives.
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, we ask how these local populations are genetically connected over large regions, which helps us start to get answers on how coevolution shapes the web of life over large geographic scales.
These studies require interactions that are broadly distributed, are found easily in the field, and are easily manipulated in experiments. We have studied multiple interactions over the past several decades, including those between prodoxid moths and their hostplants. Prodoxids include 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. See, for example, Thompson et al. (2010) Ecology Letters and Thompson and Rich (2011) Journal of Biogeography.
We are currently focusing on two questions:
• How do coevolving traits vary across thousands of kilometers?
• 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 these studies. This work is reaching completion and we are moving on to other interactions to explore questions on the scale of local adaptation in mutualistic and antagonistic interactions between species. See for example the paper by Hoeksema et al. (2012) in Ecology.
do geographic selection mosaics and gene flow shape the rate
and trajectory of coevolving interactions? And how can hosts coevolve with multiple parasite species?
These studies initially 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 has involved experimentally
induced coevolution over time scales of hundreds of generations. The studies began as a collaboration between our laboratory
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 were closely involved in the modelling aspects of these studies. Samantha Forde is now an adjunct faculty member at UCSC, and is continuing these experiments.
Subsequently, our lab been involved in a collaboration on microbial coevolution with Angus Buckling's laboratory, formerly of Oxford University and now at the University of Exeter. Britt Koskella began, and led, the work when she was a postdoctoral associated working in our laboratories. These studies have used Pseudomonas bacteria and bacteriophage to evaluate geographic selection mosaics in the field and in the lab. 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 as compare with results in the lab. Some of the work has also been devoted to understanding how bacteria evolve resistance when they must coevolve simultaneously with multiple phage types. Britt is now NERC Fellow and faculty member at the University of Exeter. See, for example, Koskella et al. (2011) Proceedings of the Royal Society B, Koskella et al. (2012) Proceedings of the Royal Society of London B, and Thompson (2012) Microbe.
does coevolution shape large webs of interacting species?
Increasingly, we are asking questions about how large groups of species coevolve within and among ecosystems. These studies are using mathematical models and available data from other laboratories to ask how coevolution may shape interactions within large webs of interacting species. We are particularly interested in how evolution, even over short time scales, shapes how species assemble into webs ("network") and how extinction of species may affect subsequent evolution within webs.
We are currently focusing on interactions among plants, pollinators, and frugivores, and similar kinds of mutualistic interactions that are crucial for the functioning of most ecosystems worldwide but are under threat in many ecosystems.
Our collaborative 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. See, for example, Guimarães et al. (2011) Ecology Letters.
Other Research Questions
In addition to these questions, we continue to
explore a wide range of related questions on the coevolutionary process, the relentlessness of evolution, and the processes that shape the web of life in our constantly changing world.
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