Preface of Darwinian Dynamics

Life exists as hierarchically nested levels of organization, in which higher level units are composed of lower level units (gene, chromosome, genome, cell, multicellular organism, society). How did this come about, and what are the implications of hierarchical organization for individuality and the meaning of fitness in evolutionary explanation? Cooperation among lower level units is central to the emergence of new higher levels, because only cooperation can trade fitness from lower to higher levels. My book is concerned with the study of cooperation, and the principles that guide the emergence of higher levels of organization. I have tried to show that there is a common set of principles and problems that bind the study of levels of organization as disparate as the gene, the cell, the multicellular organism and whole societies. I focus here on the early transitions in the history of life (from genes to networks of cooperating genes to that first individual, the cell), and on the transition from single celled organisms to multicellular ones.

These are exciting times for the study of cooperation. In the past, the study of cooperation has usually received less attention than the other two forms of ecological interaction, competition and predation. Scholars have generally viewed cooperation to be of limited interest, of special relevance to certain groups of organisms to be sure, the social insects, birds, our own species and our primate relatives, but not of general significance to life on earth. All that has changed with the study of evolutionary transitions and the emergence new units of selection. What began as the study of animal social behavior some 35 years ago, has now embraced the study of interactions at all biological levels. Instead of being seen as a special characteristic clustered in certain groups of social animals, cooperation is now seen as the primary creative force behind ever greater levels of complexity and organization in all of biology.

The benefit of group living results from cooperative interactions among group members. To create new levels of selection and organization in evolution, cooperation must be promoted among lower level units, while, at the same time, ways must be found of mitigating the inherent tendency of the lower level units to compete with one another through frequency-dependent fitness effects. Because cooperation is usually costly to the fitness of individuals within the group, defecting mutants can arise and take over the group, in the process destroying cooperation and the very conditions which made their increase possible in the first place. Cooperation is a critical factor in the emergence of new units of selection precisely because it trades fitness from the lower level (its costs) for increased fitness at the group level (its benefits). In this way, cooperation can create new levels of fitness.

The study of evolutionary transitions is the study of the emergence of new levels of fitness. Fitness is the most fundamental and unique concept in all of biology—pretty much everything else in biology is chemistry and physics, or a remnant of history. Although fundamental, it is difficult to define fitness and to explicate its role in evolutionary explanation, especially its role in evolutionary transitions. Fitness is both a cause and effect of evolutionary transitions. When it is traded between evolutionary units during cooperative interactions new levels of fitness and individuality may emerge. I hope to explain in the pages which follow how fitness is constructed out of evolutionary and population processes.

I take a dynamical point of view on evolution and on fitness concepts. Evolution has no enduring products—even organisms are of only fleeting existence, each born unique because of sex, each soon to die. Accordingly, I argue that to be construed correctly, fitness should apply to the process of genetic change—much as R. A. Fisher and G. Price envisioned—and not to products of evolution, such as organisms. I investigate fitness from the molecule level up to the level of the whole-organism. With the understanding made possible by recent developments in ecology, multilevel selection theory, and origin of life, it is now possible to present a theory of fitness. In so doing I give special attention to fitness levels, and their origins and transitions in the evolutionary process. Finally, I consider the philosophical implications of my theory of fitness for explanation in biology.

Before Darwin, design was understood as being a product of either the human mind or a Creator. A watch implies a watchmaker so argued William Payley in 1802. Darwin changed all that. Darwin argued that the design apparent in life arises out of processes intrinsic to life, not from extrinsic forces. Differential birth and death when happening in populations of organisms—and when related systematically to features in the environment—explains the well-designed features of organisms. The human eye, the grasp of the tiger’s paw, the match of the pollinator with the flower, even the human mind—all must arise out of the blindly mechanistic process Darwin called natural selection.

Sounds simple, almost too simple—for there is a lot of explaining to do. How does the theory of evolution actually go about explaining design? One concept is central—fitness. Fitness is what makes biology different. But what is fitness and where did it come from?

The great philosopher Karl Popper dismissed biology as not being science, because he thought its central doctrine "survival of the fittest" was a tautology. Who are the fittest he asked. Those who survive of course. Darwin’s great principle becomes the tautology "survival of those who survive," much to the exasperation of evolutionary biologists who have little fear that their science can be reduced to empty truisms. Popper’s challenge has been heard by a generation of philosophers of biology who have come to the rescue of evolutionary science. By in large, these defenses have followed Darwin’s lead and viewed fitness as a property of organisms.

It is easy to be confused by organisms, fitted as they are with such wondrous designs. Organisms are born and they die. In between this birthing and dying they may have offspring, some more than others according to the traits they posses and their environment. But this birthing and dying of organisms is only a part of the selection process, for the organism does not exist in isolation. In many situations, especially during evolutionary transitions, other factors dominate and interfere with the individual as the maximizing agent. Of particular concern to the major transitions in evolution are the frequency-dependent fitness effects within populations that frustrate emergence of higher levels of organization. The organism is not a maximizing agent, but this does not mean that the organism is not a unit of selection, as Dawkins argues, rather it means that there is more to natural selection than maximizing individual fitness. Organizational matters like multiple levels of selection, genetic factors like epistasis, linkage and recombination, and ecological factors like population density and age structure, can intervene and decouple organism fitness from evolution. I argue that a dynamically sufficient concept of fitness cannot relate to an overall property of organisms but instead must be associated with the dynamics of evolutionary change. The modern theory of evolution demands this dynamical view of fitness.

I develop a formal theory for the evolution of interactions using the dynamics of natural selection. Of course the founding fathers of evolutionary biology (Fisher, Wright and Haldane) developed a basic selection theory—so what has changed? There have been three key developments in the last 30 or so years that make possible the synthesis I wish to make. First, the abstract selection coefficient of the old theory has been unpacked and connected to ecology and behavior, especially with regard to the role of interactions in affecting fitness. In Fisher’s view, as embodied in his fundamental theorem of natural selection, the environment only deteriorates in time undermining the state of adaptation of the population. What was once a black box, the environment, has now been given explicit ecological content. Population biologists and ecologists understand the environment far better and represent it explicitly in their models. Of central importance to evolutionary transitions, is the role of interactions with other members of the population. Second, we understand in far greater detail the multilevel nature of selection and how natural selection occurs simultaneously at different hierarchical levels: gene, chromosome, cell, organism, group, and species. As a result of this multilevel approach, cooperation among different levels becomes not only possible but likely. I use the covariance approach to selection to embrace this multilevel setting. Finally, we have a sufficient theory of the origin of life and genetic information. We understand where fitness comes from and how it emerged from chemistry and physics.

Armed with these recent developments and a dynamical theory of selection, I reconsider Popper’s challenge and its fallout in the philosophical literature. How does evolutionary theory explain design and the fitness and individuality of evolutionary units?