Picking up where his influential The Coevolutionary Process left off, John N. Thompsonsynthesizes the state of a rapidly developing science that integrates approaches from evolutionary ecology, population genetics, phylogeography, systematics, evolutionary biochemistry and physiology, and molecular biology. Using models, data, and hypotheses to develop a complete conceptual framework, Thompson also draws on examples from a wide range of taxa and environments, illustrating the expanding breadth and depth of research in coevolutionary biology.
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The Geographic Mosaic of Coevolution
By John N. Thompson
The University of Chicago Press
Copyright © 2005 The University of Chicago
All right reserved.
The Overall Argument
This book uses the unifying framework of the geographic mosaic of coevolution to confront the major challenges in coevolutionary research: how species coevolve as groups of genetically distinct populations, how coevolving interactions can be locally transient yet persist for millions of years, and how networks of species coevolve. It is one thing to understand that a local interaction between a pair of populations eventually reaches genetic equilibrium under constant selection. It is quite another to understand how interspecific interactions are sometimes held together across millennia as species expand, contract, and diversify across complex and ever-changing landscapes. Local interacting pairs of populations are genetically linked to other populations of the same species, and these geographically variable interactions are embedded within even broader interaction networks.
The geographic and network complexity of interactions enriches the coevolutionary process. There is no more reason to expect a priori that multi-specific interactions prevent coevolution than there is to expect that multiple influences of the physical environment-temperature, salinity, water, and light availability-prevent the evolution of populations. Whether researching evolution in general or coevolution in particular, all populations are confronted with multiple selection pressures and evolutionary processes. The scientific problem is to understand how species evolve in the midst of multiple conflicting selection pressures, and how species coevolve across complex landscapes amid interactions with multiple other species.
Much of evolution is coevolution-the process of reciprocal evolutionary change between interacting species driven by natural selection. Most species survive and reproduce only by using a combination of their own genome and that of at least one other species, either directly or indirectly. Species evolve to a large degree by co-opting and manipulating other free-living species or by acquiring the entire genomes of other species through parasitic or mutualistic symbiotic relationships. The evolution of biodiversity is therefore largely about the evolution of interaction diversity.
As the science of coevolutionary biology has matured, we have been returning to a Darwinian appreciation of the entangled bank and an ecological approach to evolution that was largely put on hold during much of the twentieth century amid the excitement of the discovery of genes and the subsequent growth of population genetics and molecular biology. (See Thompson 1994 for a history of coevolutionary biology.) Those genetic and molecular tools have now become part of a renaissance in coevolutionary research, because they have begun to uncover the role of coevolution in the genomic and geographic complexity of life. Even hypotheses of speciation are increasingly based upon ecological and genetic processes driven directly by evolving interspecific interactions, whether by competition or by parasites that manipulate host reproduction.
Not all interactions are tightly coevolved. Nevertheless, as we learn more each year about the evolutionary ecology and genetics of species, we are finding that coevolution is a pervasive and ongoing influence on the organization of biodiversity. We now know that interactions between species can evolve and coevolve within decades. Appreciation of the speed of coevolution is increasing as the disciplines of ecology and evolutionary biology have encompassed studies of pathogens and parasites and incorporated molecular approaches. The traditional study organisms of ecology-plants, insects, rocky-intertidal invertebrates, fish, amphibians, reptiles, birds, and mammals-are now being complemented by studies of a wider array of invertebrates, fungi, bacteria, and viruses. During the past twenty years, the bacterial genus Wolbachia and similar intracellular symbionts have moved from being seen as interesting but esoteric causes of reproductive isolation or male sterility in a few insect species to becoming recognized as potential major causes of differentiation in the life history and population structure of a diverse mix of invertebrates. A universe of previously unknown and rapidly evolving interactions is opening as new molecular and ecological tools allow us to probe a wider range of the diversity of life.
We are also beginning to understand better the profound effects of coevolution on human societies. Human history is partly a history of coevolution with the parasites and pathogens that have shaped the spread of our species and our cultures worldwide. The story of human agriculture is to a great degree the story of human-induced coevolution between crop plants and rapidly evolving parasites and pathogens. In recent years, the fields of epidemiology, agriculture, aquaculture, forestry, and conservation biology have all become increasingly attuned to the importance of ongoing coevolution and its effects on our lives. We have, in fact, made manipulation of the coevolutionary process a central part of our human repertoire. We spend billions of dollars a year on antibiotic development, and we are working toward engineering genes to help us fight our battles with parasites, using gene against gene and parasite against parasite.
These efforts are a continuation in different forms of the coevolutionary process that has molded the organization of life on earth. There is now little question that coevolution has shaped many of the major events in the history of life. Even a short list of these events encompasses most species. The eukaryotic cell originated from coevolved symbiotic interactions that became so tightly integrated that one of the species was shaped into the organelles we now call mitochondria. The same happened again in the formation of plants, creating the organelles we now call chloroplasts. Colonization of land by plants may have been made possible through mutualistic interactions with mycorrhizal fungi. Further proliferation of plants occurred partly through coevolved interactions between flowers and pollinators and partly through coevolution with other mutualists, as well as with herbivores and pathogens. The more than seventeen thousand orchid species are thought to rely upon mycorrhizal fungi for nutrition in the early stages of development following germination, because the dustlike seeds of most orchids carry little in the way of nutritional reserves. Primary succession in terrestrial environments relies heavily upon the coevolved interactions called lichens, and subsequent succession depends in many communities upon the coevolved nitrogen-fixation symbioses between rhizobial bacteria and legumes. The very survival of many vertebrate and invertebrate species depends upon obligate coevolved symbionts that reside either within their digestive tract or in special organs, allowing them to digest plant or other tissues. In the ocean, coral reefs, which form the substrate for some of the earth's most diverse biological communities, rely upon coevolved symbioses between corals and zooanthellae and upon additional interactions between corals and algae-feeding fish, although how coevolution has shaped some of these interactions is still poorly understood. The list continues to grow.
It has taken decades for evolutionary biology to begin shifting from a restricted view of species as adapting and diversifying across "environments" to a more coevolutionary view of species as inherently dependent upon other species. It will take longer still to fully integrate interspecific interactions and coevolution into our understanding of evolutionary processes. How much of adaptation is actually coadaptation with other species? How much of population structure is due directly to coevolving interactions? How much of speciation is driven by interactions with other species? To what extent are the widespread genetic polymorphisms found in many taxa maintained by coevolution? How much has coevolution contributed to the persistence of some species across millions of years? How much of the overall organization of communities, regional biotas, continents, and oceans results directly or indirectly from the coevolutionary process?
The developing framework for coevolutionary research is allowing us to begin answering these questions. We now know that the outcomes of coevolution between a pair or group of species can differ across the geographic ranges of the interacting species. We have moved from a view of coevolution as a stately, long-term process that molds species over eons to one in which coevolution constantly reshapes interacting species across highly dynamic landscapes.
The Geographic Mosaic as the Organizing Framework of Coevolution
The goal of coevolutionary biology should be to understand how reciprocal evolutionary change shapes interspecific interactions across continents and oceans and over time. The fundamental premise of this book is that coevolution is an inherently geographic process that results from the genetic and ecological structure of species. The overall argument draws on the conclusions of two previous books (Thompson 1982, 1994) and on the empirical data and models for coevolutionary dynamics that have appeared especially over the past decade through the work of an ever-widening community of researchers. As I hope these chapters show, we now have a science of coevolutionary biology that provides a conceptual framework, specific hypotheses that follow from that framework, and predictions that can be tested within natural populations.
The framework of coevolution is built upon four fundamental attributes of species and interspecific interactions that provide the raw materials for ongoing coevolution (chapters 2 and 3). Most species are collections of genetically differentiated populations, and most interacting species do not have identical geographic ranges. Species are phylogenetically conservative in their interactions, and that conservatism often holds interspecific relationships together for long periods of time. Most local populations specialize their interactions on only a few other species. The outcomes of these interspecific interactions differ within and among communities.
Through these attributes, interactions are simultaneously held together at the species level even as they diversify among populations. Species become locally adapted to other species (chapter 4), and they continue to evolve rapidly, thereby blurring the artificial distinctions between ecological time and evolutionary time (chapter 5). These adaptations create a small set of classes of local coevolutionary dynamics, including coevolving polymorphisms, coevolutionary alternation, coevolutionary escalation, attenuated antagonism, coevolving complementarity, coevolutionary convergence, and coevolutionary displacement (chapter 5). The transient local coevolutionary dynamics between any two or more species often differ among populations at any moment in time. The resulting mosaic of local adaptation and coadaptation in interspecific interactions establishes the basic structure of the coevolutionary mosaic.
The mosaic constantly changes as coevolving species continually adapt, counteradapt, diverge from other populations, and occasionally undergo speciation. The geographic mosaic theory of coevolution argues that these broader dynamics-which go beyond local coevolution-have three components (chapter 6):
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 genotypebygenotype-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 nonreciprocal. Trait remixing. The genetic structure of coevolving species also 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 alleles and traits. Through this tripartite process, coevolution produces identifiable ecological and evolutionary dynamics across landscapes (chapter 6). Populations differ in the traits shaped by an interaction. Coevolved traits are well matched between species in some communities but sometimes mismatched in others. Most locally coevolved traits do not scale up to produce long-term directional change in the traits of interacting species. Traits shaped by coevolving interactions ratchet in particular directions and become fixed in a species only through occasional selective sweeps across all populations of interacting species or through diversifying coevolution that creates new species (chapter 7). Most of the time, coevolution moves species around in genetic and ecological space without any sustained direction. These ongoing dynamics provide us ways of analyzing coevolution by using eleven forms of evidence and drawing on approaches from multiple subdisciplines (chapter 8).
The various classes of local coevolutionary dynamics fit within the broader geographic mosaic of coevolution, and part 2 develops specific hypotheses with predictions for further research (chapters 9-15). How the geographic mosaic molds these classes depends upon the mode of interaction among species. Within antagonistic trophic interactions, predation, grazing, and parasitism have different effects on the structure of coevolutionary selection. The geographic structure of interactions can sustain coevolving polymorphisms between parasites and hosts, while generating a mix of habitats in which traits are matched or mismatched (chapter 9). Under some conditions multispecific coevolution between parasites and hosts favors optimal allelic diversification in these polymorphisms (chapter 9), and it may favor the maintenance of sexual reproduction (chapter 10). Predators and grazers, and some parasites, often actively choose among multiple victim species, creating mosaics of coevolving networks through geographic differences in relative preference and the process of coevolutionary alternation, sometimes coupled with escalation (chapter 11).
The continuum in forms of interaction from mutualistic symbioses to mutualism between free-living species is as fundamental to the geographic mosaic of coevolution as is the continuum from parasitism to grazing and predation. Mutualisms coevolve through a combination of complementarity of traits (e.g., nutritional requirements of hosts and mutualistic symbionts; shapes of flowers and hummingbird bills) and convergence of traits within networks (e.g., convergent floral traits among species). The importance of coevolutionary convergence as part of the process differs among the forms of mutualism. Local adaptation sometimes favors the evolution of attenuated antagonism within symbiotic interactions (chapter 12). Those interactions that create reciprocal fitness benefits coevolve through selection toward mutualistic monocultures and complementary symbionts (chapter 12), creating geographic mosaics (chapter 13). Local adaptation among free-living mutualists also favors complementarity among interacting species, but it also favors convergence of unrelated taxa. These two classes of coevolutionary dynamics contribute to predictable network structure even as species composition changes across landscapes (chapter 14).
The remaining major outcome, coevolutionary displacement, results from a geographic mosaic in the intensity and form of interaction among species that share similar resources or habitats (chapter 15). Species may become displaced in traits or habitat use through competition, either alone or combined with other forms of interaction, and guilds of species may become displaced in similar ways across landscapes. Local character displacement in a pair of species is therefore only one component of the overall geographic mosaic of coevolutionary displacement.
The developing framework for coevolutionary biology provides an increasingly solid basis for the establishment of a science of applied coevolutionary biology (chapter 16). Selective breeding and genetic modification of crops and livestock for resistance against parasites is a form of human-induced coevolution that has some similarities to natural coevolution but also many differences from it. The development of antibiotics and vaccines has created, in effect, surrogate genes and a process of surrogate coevolution that we are now trying to manage. More broadly, our worldwide modification of landscapes and transport of species over vast distances is creating interactions with geographic configurations that differ in some ways from anything most species have experienced in the past.
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Table of Contents
Part 1 - The Framework of Coevolutionary Biology
1. The Overall Argument
2. Raw Materials for Coevolution I: Populations, Species, and Lineages
3. Raw Materials for Coevolution II: Ecological Structure and Distributed Outcomes
4. Local Adaptation I: Geographic Selection Mosaics
5. Local Adaptation II: Rates of Adaptation and Classes of Coevolutionary Dynamics
6. The Conceptual Framework: The Geographic Mosaic Theory of Coevolution
7. Coevolutionary Diversification
8. Analyzing the Geographic Mosaic of Coevolution
Part 2 - Specific Hypotheses on the Classes of Coevolutionary Dynamics
9. Antagonists I: The Geographic Mosaic of Coevolving Polymorphisms
10. Antagonists II: Sexual Reproduction and the Red Queen
11. Antagonists III: Coevolutionary Alternation and Escalation
12. Mutualists I: Attenuated Antagonism and Mutualistic Complementarity
13. Mutualists II: The Geographic Mosaic of Mutualistic Symbioses
14. Mutualists III: Convergence within Mutualistic Networks of Free-Living Species
15. Coevolutionary Displacement
16. Applied Coevolutionary Biology
Appendix: Major Hypotheses on Coevolution