Funded Grants

Coevolution across scales

In my examination of Orchids, hardly any fact has so much struck me as the endless diversity of structure, --the prodigality of resources,--for gaining the very same end, namely, the fertilisation of one flower by the pollen of another.

This quote is from one of Charles Darwin's lesser-known books, The Fertilization of Orchids, where he develops observations about coevolution, first introduced in The Origin of Species. Darwin describes in exquisite detail adaptations by orchids to bait and use insects for dispersing their pollen. He focuses on the perfection and cunningness of these adaptations, but were these adaptations a product of the coevolving species only?

The coevolutionary paradigm rests on a simple logic: individual organisms not only have to cope with their physio-chemical environments, but also must confront other evolving organisms, be this consuming them as resources, fighting them off as predators or parasites, cooperating with them as mutualists, or competing with them for resources or for reproductive opportunities. Failure at any of these can result in a shortened life-span and reduced reproductive output. This means that species interactions will have demographic consequences, and should there be heritable variation for traits, evolutionary consequences too. Insofar as biological form and function are imprints of environments, coevolution presents the unique possibility that different species are, in part, dynamically changing imprints of one another.

Coevolutionary dynamics play themselves out in time and in space. In time because the selection involved may occur over many generations or even perpetually. In space because adaptations at a certain place and at a certain time can be 'transmitted' via migration or gene flow to other sites, where they may compete with resident phenotypes and, if more successful, out-compete local adaptations. Developing theory to obtain an understanding of these processes is very challenging. First, environments are complex: they are composed of many abiotic factors such as temperature and humidity, as well as biotic ones in the form of communities of interacting species. Moreover, environments vary in space and in time, and the grain of this variation itself may be variable. Second, individuals of most species can move either within or between spatially isolated populations, change phenotypically during their lives, and differ genetically from individual to individual within a population.

Given this complexity, how predictable is coevolution? That is, to what extent will the same coevolutionary processes from the same initial conditions act in the same way to produce the same individual and community structures? To what extent do environments outside of a coevolving species interaction drive pattern in adaptation and biodiversity? If pattern is significantly influenced by variation in the interacting species themselves, is this explained by vagile or more conservatively expressed genes and traits? Are there types of coevolutionary interaction that are more likely to show stronger pattern than others? What happens to coevolution when trophic complexity is included?

These questions are central to evolutionary biology, but are far from being resolved. Part of the reason is because we are yet to develop the theoretical framework necessary to obtain answers that match both pattern and process in natural systems. A few studies have ventured into this domain, but none have assessed the many sources of complexity in any systematic way.

Moreover, although we are starting to tease apart coevolutionary pattern from laboratory and field examples, we haven't gone beyond the initial stages of inquiry, because we are either observing, or manipulating single or small numbers of factors. Should there be complex interactions between factors contributing to pattern, we may be reaching conclusions that are either incorrect or lack generality.

My argument is that we need to examine coevolutionary systems at different entry points in order to obtain an assessment of the factors driving their pattern. We can approach this by identifying and understanding environmental variables one at a time, or in simple combinations, and synthesize complexity without necessarily conducting a full experiment or analysis. Or, we can approach the problem from the other end, starting with full complexity, and delete unimportant factors one by one. An alternative to these scenarios is to employ frameworks of intermediate complexity. The idea is to compare and contrast one or more levels of complexity and experiment through single or multiple additions and deletions to arrive at a functional map of causation. The systematic use of different entry points is a promising way to make important discoveries, and significantly advance our understanding of the interacting forces that drive coevolution.

Over the past 15 years we have developed theory and conducted experiments to elucidate the roles of environment and biotic interactions in both antagonistic and mutualistic coevolutionary systems. We propose to build on these foundations with the goal of a general theoretical framework to reveal the relative roles played by exogenous environments and the interacting couple itself in coevolution between pathogens and their hosts. We are interested in discovering the driving mechanisms behind emergent patterns at three levels of resolution, and how these levels are interrelated and interact.

First, we will consider how the severity or 'virulence' of disease is influenced by the coevolution of infectivity traits in the pathogen and resistance traits in the host. This is a topic of major importance in epidemiology and population biology, as well as the more applied area of disease management. Theoretical approaches have investigated how organism biology, population ecology, immune systems, and genetics act and interact to determine pathogen virulence. We are starting to appreciate how both host behavior and physiological condition influence virulence, and in particular that the structure of contact networks can be a pivotal mediator of pathogen evolution. We will aim to understand the less studied phenomenon of how environmental change, be it transitory or progressive, in impacting transmission networks and the quality of the host as a habitat for the pathogen, translates into changes in virulence.

Second, we will relate virulence evolution in coevolving systems to community structure and the emergence of interactive networks between host and pathogen strains in simple two-species and complex multi-species communities. Much of our understanding of the coevolutionary process comes from population approaches: changes in the frequencies of interacting or non-interacting genotypes in pathogen and host. My group has recently contributed importantly to this research by showing how individual genotypes may establish and break links between one another, resulting in a dynamic network of specialist and generalist pathogens, and hosts of different vulnerabilities to the range of pathogens in the environment. What we need to know is how and why the structure of these “bipartite networks” changes in simple and complex environments.

Third, pathogens may multiply and spread via select types of host individual (so-called 'super-spreaders'). In some cases, this may result in severe epidemics followed by abrupt extinctions, but more generally super-spreading will lead to complex and possibly unpredictable epidemiological consequences at regional scales. A major, unresolved question is how the super-spreading phenomenon affects coevolutionary dynamics, and to what extent is the spread of disease primed by contingencies, such as structured or noisy environments. We need to know how coevolving networks are organized and collapse during and following epidemics; we also need to understand how certain virulent pathogen strains emerge and affect such events.

Our ultimate goal is a coevolutionary synthesis that will explain pattern at units from genes to communities and for different temporal and spatial scales. The proposed work will assess to what extent the finesse and spectacular nature of adaptations in coevolving species are influenced by exogenous environments.

These studies will have broader implications, since their key elements—individual traits, interaction networks and spatial structure--are properties of a variety of other complex systems. For instance, with appropriate modifications, this theory can be applied to human populations, including vaccination strategies, predicting the spatial spread of epidemics, and managing nosocomial diseases in hospitals. From a more social science and economics perspective our studies will have parallels with how cooperative exchanges are established and broken and how exploitation (analogous to virulence) emerges and evolves in different social environments.