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Part 1
The Process of Adaptation
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1
Adaptive Evolution
If you read this book at the rate of about a chapter a day, by the time you finish it some species will have evolved. They will have been microbial species, and the populations will have evolved in ways almost imperceptible. If you have the right experimental tools, though, you can document the evolution. If you wait a little longer, say a year, the same will have had happened to some plants, insects, and other species with short generation times. We did not realize until recently the relentlessness of evolution, because we lacked the tools, and we often looked for it only where we expected we would most likely find itāprincipally in environments we have greatly changed.
In the old days of research on evolution, just a few decades ago, we hoped at best to catch glimpses of evolution in action. Scientists and nonscientists alike thought that evolutionary processes acted over long periods of time. We thought that any chance of seeing evolution occur would be due to luck or to extremely unusual circumstances. It was common for biologists to talk about āecological timeā as compared with āevolutionary time.ā Ecological processes happened quickly; evolutionary processes happened slowly.
Most of us biologists therefore felt we could ignore rapid evolution as a potential explanation for the changing patterns we often find in populations and biological communities. When asked for examples of evolution occurring over short timescales, we would rely on a few well-studied cases. We would point to the increases in dark-winged forms of peppered moths in regions of high industrial pollution, the rapid evolution of resistance to pesticides in some insects, or the continuing evolution of human influenza virus during the past century. There were some other examples from which we could choose, but few had been analyzed in detail. They were collectively viewed as the fortunate exceptions we could study.
Those days are over. Well-studied examples of ongoing evolution within our lifetimes are being published in professional journals at such a fast rate that it is hard to keep up with them. Even those of us who have studied the ongoing evolution of populations have become increasingly impressed by the speed at which some populations are evolving in nature. The examples come from studies in the fields of ecology, epidemiology, medicine, microbiology, agriculture, forestry, wildlife management, marine biology, fisheries biology, population genetics, and molecular biology. We have now come to expect that insects and weeds will evolve resistance to pesticides, influenza viruses will evolve at speeds that will keep epidemiologists nervous, and new strains of antibiotic resistant bacteria will continue to proliferate and cause concern within the medical community. We now know that even the simple act of harvesting fish populations has led to marked evolutionary changes in some species.
As we have come to realize the sometimes rapid pace of evolution, many biologists and some policy makers and resource managers have increasingly turned to the problem of how to manage it. How do we slow the rate at which insects evolve resistance to pesticides and bacteria evolve resistance to antibiotics? How do we conserve and restore biological communities amid global change that is driving evolutionary change in some species? How do we control invasive species that are evolving as they spread across new continents and oceans? Amid our growing appreciation of the pervasiveness of evolutionary change, just about every possible view has now been expressed on how human activities may alter the future evolution of species.
That discussion, though, only highlights the more long-standing debate in evolutionary biology of what drives ongoing evolutionary changeāsometimes quickly, sometimes more slowly, but ongoing nevertheless. We can point to particular cases and their causes: rising or falling temperatures, changing patterns of rainfall, sexual selection within species, competition, predation and trophic cascades, parasitism, mutualism, the balance between mutation and random loss of genes, and the occasional odd asteroid. These ad hoc explanations simply underscore the fact that almost all species live in a constantly changing world that demands evolutionary change in populations.
If we are to interpret how our world is changing through climate change, habitat modification, and the wholesale movement of species among continents, we need to understand much better the background chatter of endless year-to-year evolution and its causes. We need to know the extent to which continual evolutionary change is truly important in shaping and maintaining the web of life at every timescale and across every spatial scale.
This book explores the pace, genetics, and ecological drivers of adaptive evolutionary change. It is about why natural selection is generally stronger and adaptive evolution more dynamic than, until recently, we have thought. The early chapters focus on adaptive evolutionary change in populations over tens, hundreds, and thousands of years rather than millions of years. This is the part of evolutionary change that is most directly and immediately important to the ecological dynamics of biological communities, to the conservation of species, and to human society as species all around us continue to adapt amid environmental change. The later chapters explore the consequences of ongoing evolution for ecological speciation, adaptive radiation, and the continual reformulation of the web of life.
THE PROBLEM TO SOLVE
The great problem to solve about life on earth has gradually shifted over the past century and a half since Darwinās Origin of Species. We began with the problem of whether species evolve. The problem has been solved so completely that we are now faced with a problem at the opposite extreme. Why is evolution so relentless, altering populations generation after generation? After all, species generally seem well adapted to the environments in which they live, yet they continue to evolve even in environments that have not undergone major recent changes. Most of these evolutionary changes occur through modification of genes and traits that already have been subject to selection for many thousands of generations.
Superficially, these small changes seem like aimless evolutionary meanderings. Slowly, though, we have come to realize that these continual adjustments in adaptation are often surprisingly important to the persistence of populations. These small changes capture the ecology of evolution. That appreciation has made us realize that we need as deep an understanding of the ecological drivers of evolutionary change as we have tried to develop for the genetic and molecular processes that translate ecological selection into evolving traits. These chapters explore how our understanding is progressing.
We know the component parts of the process of adaptive evolution. It begins with differences among physical environments that impose selection on populations to adapt to local temperatures and the availability of water, light, and nutrients. Without major environmental change, populations become well adapted to their local physical conditions. Populations and species, though, do not live in a vacuum. They adapt, speciate, and go extinct as parts of continually changing webs of interacting species. Much of the ongoing evolution of each species is about exploiting other species and avoiding exploitation. The result is a process of reciprocal evolutionary changeācoevolutionāthat shapes the web of life in different ways in different environments. Occasionally those webs are torn apart by huge physical upheavals that lead to mass extinctions, creating new opportunities for diversification. Overall, the physical environments provide the basic templates for adaptation and diversification, but interactions among species multiply and modify, in myriad ways, how selection acts within and among those templates.
That much now seems obvious to us after many decades of hard-won paleontological, evolutionary, and ecological data. We are, though, still struggling with fundamental questions about the ecological structure and dynamics of evolutionary change. How can natural selection on species be so unrelenting without constantly reorganizing much of the web of life? If natural selection is so strong on populations, why are species not constantly undergoing directional evolutionary change? If natural selection often does not lead to directional change, then what forms of selection are most important in driving much of the generation-to-generation evolutionary change we see in populations? Is selection imposed by species on each other inherently different from selection imposed by physical environments? These questions are increasingly important at a time when we are altering the earthās physical environments and the web of life itself.
THE CENTRAL ARGUMENTS
This book weaves together two arguments on why evolution is so relentless. The central argument is that evolution is as much an ecological process as it is a genetic process. At a superficial level, we all know that, but the drive to understand the molecular mechanisms of evolution can make it seem at times that evolution can be understood mostly by a deeper understanding of molecular mechanisms alone. It cannot. Much of the dynamics of evolution is about the interplay between genes and environments (genotype-by-environment interactions) and about the ever-changing coevolution among species in different environments (genotype-by-genotype-by-environment interactions). Adaptation and adaptive diversification are, at their core, the result of the intermingling of molecular and ecological processes. Species are constantly adapting and re-adapting because they are forced to do so by the ever-changing web of life. Much of adaptive evolution, then, is about the continual redeployment of standing genetic variation in different ways in constantly changing physical and biotic environments. The pacesetters of day-to-day evolution seem to be at least as much, and maybe more, ecological rather than genetic.
The second argument is that much of adaptive evolution does not lead anywhere, yet these small changes are crucially important. These continual microevolutionary changes keep populations in the evolutionary game as they interact with other species that are themselves constantly evolving. These seemingly aimless meanderings are the essential dynamics of evolution, with directional change and speciation as occasional outcomes. Species do not fail to undergo sustained directional change because natural selection has been asleep on the job; species fail to undergo sustained directional change because natural selection time and again comes up with slightly variant ways of jury-rigging species to keep them as viable evolutionary products even as the world continues to change around them.
Together, these two arguments constitute a view of evolution that is unrelenting because selection on populations constantly changes as genes are expressed in different ways in different environments and as interactions among species vary in their effects among environments. Almost every major study of selection in nature has found differences either in the form or the strength of selection among years and among populations. Much of evolution is about selection that favors modest changes in degrees of novelty within populations and relatively modest divergence among populations. Most adaptive radiations of species are about variations on an ecological theme. This book, then, examines why evolution can appear to be either frenetic or sluggish, depending on the lens we use to examine it. Some chapters focus more on the pace and dynamics of evolutionary change, and others focus more on the drivers that fuel ongoing adaptive change.
THE EXPANDING STUDIES OF ADAPTIVE EVOLUTION
We have progressed in recent years in our understanding of adaptive evolution through work by ecologists painstakingly studying which individuals survive and reproduce in different environments and different years; coevolutionary biologists studying how species coadapt to each other across complex environments; microbiologists, population geneticists, physiologists, and developmental biologists examining experimental evolution and co-evolution in the laboratory; structural biologists analyzing how selection re-molds the shapes of organisms in different ecological contexts; molecular biologists exploring the mechanisms of evolutionary change; paleobiologists examining patterns of change over longer timescales; and theoreticians probing mathematical models of the rates of evolution. Rather than simply trying to infer how evolutionary processes might have created the patterns we see in nature, we now have the tools to study these processes directly in the laboratory and in nature. We can compare evolution in populations that have been manipulated directly by human activities with those only indirectly affected by our activities or with those in the few remaining environments still mostly free of human activities.
These studies have documented hundreds of cases of ongoing evolution of species over the past century (table 1.1). They are examples of what is sometimes called contemporary evolution (Hendry and Kinnison 1999). It is evolution on timescales that can affect the dynamics of populations, communities, and ecosystems. These studies in eco-evolutionary dynamics represent part of a renewed attempt to link the fields of ecology and evolutionary biology. The connections between these fields have waxed and waned over the past century, but these disciplines are now coming together again in new ways (Abrams and Matsuda 1997; Thompson 1998; Hairston et al. 2005; Whitham et al. 2006; Fussman et al. 2007; Kinnison and Hairston 2007; Wade 2007; Strauss et al. 2008; Bailey et al. 2009; Pelletier et al. 2009; Ellner et al. 2011; Schoener 2011).
Compiled lists and summaries of rapid evolution such as those in table 1.1 include taxa, traits, and trends as diverse as life itself (e.g., Thompson 1998; Hendry and Kinnison 1999; Kinnison and Hendry 2001; Reznick and Ghalambor 2001; Hairston et al. 2005; Carroll et al. 2007; Hendry et al. 2007; Ellner et al. 2011). Any such list would rise rapidly into the thousands if it included every case of a population evolving pesticide resistance or antibiotic resistance and every case of evolution in a local population caused by human activities. Examples of rapid evolution are limited much more by the number of biologists studying it than by the number of actual examples in nature.
The examples now include just about every kind of trait biologists have studied: morphology, physiological pathways, life histories, behaviors, and interactions with other species. They include native species living in their normal environments, native species living in environments greatly altered by humans, and introduced species living in environments either similar or different from where they lived in their native ranges. They include vertebrates, invertebrates, plants, fungi, and microbes. They involve not only examples of how populations adapt to their physical environments but also how they adapt to each other and to other species. Considered together, these examples have told us that rapid evolution is occurring in all major taxa in most environments. It is not limited to fast-growing microbes or insects or small plants, and it is not limited to highly modified environments that impose novel selection pressures on populations.
Table 1.1 Examples of ecologically important characteristics of species that have evolved in nature over the past two centuries
Notes: The list includes only a small sample of known cases of rapid evolution.
If we lengthen the timeline to thousands of years, evolutionary change becomes even more evident. Changes in climate, habitats, and the geographic distributions of species in the past 10,000ā12,000 years since the end of the Pleistocene have resulted in many populations that have diverged from each other as they have adapted to different environments. Deer mice (Peromyscus maniculatus) in the Sand Hills of Nebraska have evolved a light coat color rather than the normal dark color during the past 8,000 years (Linnen et al. 2009), and some crossbill populations have diverged to specialize on different conifers since the Pleistocene (Benkman 2010). The fastest observed rates have been in species that we are trying to manipulate for our own ends, but that is also where we most often look for rapid evolution. We know we are directly fueling the evolutionary process through our manipulation of other species, but we are coming to realize that our manipulations are often just a highly efficient and specialized form of what species everywhere impose on each other.
TRACKING RAPID EVOLUTION THROUGH QUIRKS IN LIFE HISTORIES
In some cases, quirks in the biology of species make it possible to track the genetic signatures of rapid evolution directly by comparing the current generation with ancestral generations. This approach, sometimes called resurrection ecology (Kerfoot and Weider 2004), has been used to study species with dormant stages, that can remain alive for many years and brought back later to an active state. These include, for example, invertebrates in which dormant eggs or other resting stages become buried in lake sediments. This approach has also long been the mainstay of studies of adaptive evolution in laboratory experiments on microorganisms that can be frozen alive and then...
