Plant-Herbivore Interactions

As is the case with most supposedly modern concepts in evolutionary biology, the idea of coevolution, or reciprocal evolutionary change between interacting species, actually goes back to Charles Darwin. In the introduction to The Origin of Species (1859), he wrote: …In considering the Origin of Species, it is quite conceivable that a naturalist, reflecting on the mutual affinities of organic beings, on their embryological relations, their geographical distribution, geological succession, and other such facts, might come to the conclusion that species had not been independently created, but had descended, like varieties, from other species. Nevertheless, such a conclusion, even if wellfounded, would be unsatisfactory, until it could be shown how the innumerable species inhabiting this world have been modified, so as to acquire that perfection of structure and coadaptation which justly excites our admiration. It is, therefore, of the highest importance to gain a clear insight into the means of modification and coadaptation…. Early on, then, Darwin pointed out the importance of interactions among organisms in determining evolutionary change, as opposed to “external conditions such as climate, food,” or even “the volition” of the organism itself. Interactions among organisms, however, take many forms. Antagonistic interactions, in which one species benefits and the other is harmed, are themselves diverse. Among those interactions in which both species are animals, the gamut runs from predation, in which one species kills and consumes several individuals of the other species during its lifetime, to parasitism, in which one species merely saps the “reserves” and rarely kills its host. Intermediate and unique to the phylum Arthropoda is parasitoidism, in which one species kills its prey, as does a predator, but, like a parasite, is normally restricted to a single host individual. A comparable continuum exists for interactions between an animal and a plant species; these associations are usually referred to as forms of herbivory (with parasitoidism akin to internal seed feeders of plants). In mutualistic interactions, both species benefit from the interaction. Mutualisms can involve interactions between animals and plants, generally in which a food reward from the plant is exchanged for mobility provided by the animal partner.

Life Cycles

I have a Hardin cartoon on my office door. It shows a series of animals thinking about the meaning of life. In sequence, we see a lobe-finned fish, a salamander, a lizard, and a monkey, all thinking, “Eat, survive, reproduce; eat, survive, reproduce.” Then comes man: “What's it all about?” he wonders. Organisms live to reproduce. The ultimate selective pressure on any organism is to survive long enough and well enough to pass genetic material to a next generation that will also be successful in reproducing. In this sense, then, every morphological, physiological, biochemical, or behavioral adaptation contributes to reproductive success, making the field of life cycle evolution a very broad one indeed. Key components include mode of sexuality, age and size at first reproduction (Roff, this volume), number of reproductive episodes in a lifetime, offspring size (Messina and Fox, this volume), fecundity, the extent to which parents protect their offspring and how that protection is achieved, source of nutrition during development, survival to maturity, the consequences of shifts in any of these components, and the underlying mechanisms responsible for such shifts. Many of these issues are dealt with in other chapters. Here I focus exclusively on animals, and on a particularly widespread sort of life cycle that includes at least two ecologically distinct free-living stages. Such “complex life cycles” (Istock 1967) are especially common among amphibians and fishes (Hall and Wake 1999), and within most invertebrate groups, including insects (Gilbert and Frieden 1981), crustaceans, bivalves, gastropods, polychaete worms, echinoderms, bryozoans, and corals and other cnidarians (Thorson 1950). In such life cycles, the juvenile or adult stage is reached by metamorphosing from a preceding, free-living larval stage. In many species, metamorphosis involves a veritable revolution in morphology, ecology, behavior, and physiology, sometimes taking place in as little as a few minutes or a few hours. In addition to the issues already mentioned, key components of such complex life cycles include the timing of metamorphosis (i.e., when it occurs), the size at which larvae metamorphose, and the consequences of metamorphosing at particular times or at particular sizes. The potential advantages of including larval stages in the life history have been much discussed.

Population Structure

Population structure is a ubiquitous feature of natural populations that has an important influence on evolutionary change. In the real world, populations are not homogenous units; instead, they develop an internal structure, created by the physical properties of the environment and the biological characteristics of the species (such as dispersal ability). However, our basic ecological and population genetic models generally ignore population structure and focus on randomly mating (panmictic) populations. Such structure can profoundly change the evolution of a population. In fact, the myriad of influences that population structure exerts can only be hinted at in a single chapter. Since an exhaustive review is not possible, I will focus on presenting the conceptual issues linking mathematical models of population structure to empirical studies. To do this, it is useful to recognize two different kinds of population structure that both reflect and influence evolutionary change. The first is genetic structure. This is defined as the nonrandom distribution of genotypes in space and time. Thus, genetic structure reflects the genetic differences that develop among the different components of one or more populations. The second is what I will call proximity structure, defined by the size and composition of the group of neighbors that influence an individual’s fitness. Fitness is commonly influenced by local intraspecific interactions. Perhaps the most obvious example is competition. When individuals compete for some resource, they don’t usually compete equally with every other member of the population; in general, they compete only with a few of the most proximate individuals. These two forms of population structure, genetic structure and proximity structure, provide a foundation for understanding why we have shifted away from viewing populations as homogenous units. For good reason, this is a theme that is explored in many of the other chapters in this book. Genetic structure can develop within a population over a single generation, generally either as a result of local family associations or as a result of spatial variation in selection. For example, limited seed dispersal results in genetic correlations among neighbors even in the face of long-distance pollen movement, due to the clustering of maternal half sibs.

Evolutionary Conservation Biology

Conservation biology as a discipline focused on endangered species is young and dates only from the late 1970s. Although conservation of endangered species encompasses many different biological disciplines, including behavior, ecology, and genetics, evolutionary considerations always have been emphasized (e.g., Frankel and Soule 1981). Many of the applications of evolutionary concepts to conservation are ones related to genetic variation in small or subdivided populations. However, the critical status of many endangered species makes both more precision and more caution necessary than the general findings for evolutionary considerations. On the other hand, the dire situations of many endangered species often require recommendations to be made on less than adequate data. Overall, one can think of the evolutionary aspects of conservation biology as an applied aspect of the evolution of small populations with the important constraint that any conclusions or recommendations may influence the actual extinction of the populations or species under consideration. From this perspective, all of the factors that influence continuing evolution (i.e., selection, inbreeding, genetic drift, gene flow, and mutation; e.g., Hedrick 2000) are potentially important in conservation. The evolutionary issues of widest concern in conservation biology—inbreeding depression and maintenance of genetic variation— can be seen in their simplest form as the joint effects of inbreeding and selection, and of genetic drift and mutation, respectively. However, even in model organisms such as Drosophila, the basis of inbreeding depression and the maintenance of genetic variation are not clearly understood. In addition, findings from model laboratory organisms may not provide good insight into problems in many endangered species, the most visible of which are generally slowly reproducing, large vertebrates with small populations. Here we will first focus on introductions to two important evolutionary aspects of conservation biology: the units of conservation and inbreeding depression. Then, we will discuss studies in two organisms as illustrations of these and related principles—an endangered fish species, the Gila topminnow, and desert bighorn sheep—to illustrate some evolutionary aspects of conservation. In the discussion, we will mention some of the other evolutionary topics that are relevant to conservation biology.

Predicting the Outcome of Biological Control

The movement of humans around the earth has been associated with an amazing redistribution of a variety of organisms to new continents and exotic islands. The natural biodiversity of native communities is threatened by new invasive species, and many of the most serious insect and weed pests are exotics. Classical biological control is one approach to dealing with nonindigenous species. If introduced species that lack natural enemies are competitively superior in exotic habitats, introducing some of their predators (herbivores), diseases, or parasitoids may reduce their population densities. Thus, the introduction of more exotic species may be necessary to reduce the competitive superiority of nonindigenous pests. The intentional introduction of insects as biological control agents provides an experimental arena in which adaptations and interactions among species may be tested. We can use biological control programs to explore such evolutionary questions as: What characteristics make a natural enemy a successful biological control agent? Does coevolution of herbivores and hosts or predators (parasitoids) and prey result in few species of natural enemies having the potential to be successful biological control agents? Do introduced natural enemies make unexpected host range shifts in new environments? Do exotic species lose their defense against specialized natural enemies after living for many generations without them? If coevolution is a common force in nature, we expect biological control interactions to demonstrate a dynamic interplay between hosts and their natural enemies. In this chapter, I consider biological control introductions to be experiments that might yield evidence on how adaptation molds the interactions between species and their natural enemies. I argue that the best biological control agents will be those to which the target hosts have not evolved resistance. Classical biological control is the movement of natural enemies from a native habitat to an exotic habitat where their host has become a pest. This approach to exotic pests has been practiced since the late 1800s, when Albert Koebele explored the native habitat of the cottony cushion scale, Icrya purchasi, in Australia and introduced Vadalia cardinalis beetles (see below) to control the cottony cushion scale on citrus in California. This control has continued to be a success.

Mutualisms

The unusual behavior of cleaner fish has attracted both popular and scientific curiosity since its discovery early in the 20th century. These fish apparently make their living by removing external parasites from “host” fishes of other species (some also remove bacteria or diseased and injured tissue). When they approach cleaners, hosts assume an unusual motionless posture that allows cleaners to feed from their scales, from their gill cavities, or even inside their mouths. For their trouble, cleaner fish get a meal, and hosts get a good cleaning. The interaction between cleaner fish and their hosts is generally classified as a mutualism, or mutually beneficial interaction between species. Stories about this and other mutualisms have become staples of nature documentaries and the popular literature and have helped lure many students into a lifetime of studying biology. From the perspective of evolutionary ecology, however, the cleaner-host relationship is anything but straightforward (Poulin and Grutter 1996). First, it is not at all clear that this interaction confers reciprocal fitness benefits. Despite several decades of effort, only one study has shown that cleaners significantly reduce hosts’ parasite loads (Grutter 1999), and none has yet demonstrated that reducing parasite loads increases host success. Since cleaners often gouge the host’s flesh, particularly when parasites are few, the interaction is often more costly than beneficial. Second, if cleaning does not confer an advantage, it is not evident why hosts should tolerate and even actively solicit cleaners’ attention. In fact, sometimes hosts lure cleaners only to eat them, but the conditions under which it might be beneficial for a host to doublecross its cleaners like this remain unexplored. Third, we don’t really understand how cleaning behaviors arose in the first place, considering that the first individuals that approached hosts to feed on parasites were very likely eaten. Despite this constraint, cleaning has apparently evolved multiple times; it is found in at least five families, in both marine and freshwater species, and in both the temperate zone and the tropics.

The Evolutionary Ecology of Movement

Organisms move, and their movement can take place by walking, swimming, or flying; via transport by another organism (phoresy); or by a vehicle such as wind or current (Dingle 1996). The functions of movement include finding food or mates, escaping from predators or deteriorating habitats, the avoidance of inbreeding, and the invasion and colonization of new areas. Virtually all life functions require at least some movement, so it is hardly surprising that organisms have evolved a number of structures, devices, and behaviors to facilitate it. The behavior of individuals while moving and the way this behavior is incorporated into life histories form one part of this chapter. This discussion focuses on the action of selection on the evolution of individual behavior, on how specific kinds of movement can be identified from the underlying behavior and physiology, and on the functions of the various movement behaviors. The other major part of our discussion focuses on the consequences of movement behaviors for the ecology and dynamics of populations. The pathways of the moving individuals within it can result in quite different outcomes for a population. First, movements may disperse the members of the population and increase the mean distances among them. The separation may be a result of paths more-or- less randomly chosen by organisms as they seek resources, or it may be a consequence of organisms avoiding one another. In contrast to dispersing them, movement may also bring individuals together either because they clump or congregate in the same habitat patch or because they actively aggregate through mutual attraction. Clumping can also lead to aggregation and mutually attracting social interactions. A classic example is the gregarious (aggregating) phase of the desert locust (Schistocerca gregaria), in which huge swarms of many millions of individuals first congregate in suitable habitats and then develop and retain cohesion based on mutual attraction. The foraging swarms make the locust a devastating agricultural pest over much of Africa and the Middle East (Farrow 1990; Dingle 1996). It is the aggregation of locusts that makes them such destructive pests; they would be far less harmful if the populations dispersed.

Cooperation and Altruism

People have always been fascinated by cooperation and altruism in animals, in part to shed light on our own propensity or reluctance to help others. Darwin’s theory added a certain urgency to the subject because the principle of “nature red in tooth and claw” superficially seems to deny the possibility of altruism and cooperation altogether. Some evolutionary biologists have accepted and even reveled in this vision of nature, giving rise to statements such as “the economy of nature is competitive from beginning to end . . . scratch an ‘altruist’ and watch a hypocrite bleed”. Others have gone so far in the opposite direction as to proclaim the entire earth a unit that cooperatively regulates its own atmosphere (Lovelock 1979). The truth is somewhere between these two extremes; cooperation and altruism can evolve but only if special conditions are met. As might be expected from the polarized views outlined above, achieving this middle ground has been a difficult process. Science is often portrayed as a heroic march to the truth, but in this case, it is more like the Three Stooges trying to move a piano. I don’t mean to underestimate the progress that been made—the piano has been moved—but we need to appreciate the twists, turns, and reversals in addition to the final location. To see why cooperation and altruism pose a problem for evolutionary theory, consider the evolution of a nonsocial adaptation, such as cryptic coloration. Imagine a population of moths that vary in the degree to which they match their background. Every generation, the most conspicuous moths are detected and eaten by predators while the most cryptic moths survive and reproduce. If offspring resemble their parents, then the average moth will become more cryptic with every generation. Anyone who has beheld a moth that looks exactly like a leaf, right down to the veins and simulated herbivore damage, cannot fail to be impressed by the power of natural selection to evolve breathtaking adaptations at the individual level. Now consider the same process for a social adaptation, such as members of a group warning each other about approaching predators.

Mating Systems

The study of mating is one of the most active areas in evolutionary ecology. What fuels this research is curiosity about a stunning diversity of ways in which zygotes are formed. Many plants and some animals can reproduce without combining gametes. Many other plants combine gametes but do so within the same individual (selfing). Still other plants and animals require a gamete from another individual to stimulate reproduction but do not incorporate the genetic material contained in that gamete in the offspring. Finally, many organisms combine gametes produced from different individuals in sexual reproduction, but the ways in which these individuals get together to reproduce are also amazingly diverse and have major implications for how selection acts in these populations. Why are there so many different ways to reproduce? Answering this question is a major challenge for evolutionary ecologists. Our approach begins with how a variety of ecological factors affect selection on reproductive traits. Because many reproductive traits show genetic variation, diversity in selective pressures can lead to a diversity of evolutionary changes. Thus, understanding the evolutionary ecology of mating systems can help to interpret the significance of this variation and can provide new insight into related phenomena. For example, costs of female reproduction associated with development of offspring greatly impact other aspects of the life history, and males are often limited by mates (Savalli, this volume). Factors such as levels of selfing, inbreeding depression, and allocation of resources play a part in mating systems of both plants and animals (Waser and Williams, this volume), and sex allocation theory has been used in both plants and animals to explore the evolution of hermaphroditism and unisexuality (Campbell 2000; Orzack, this volume). This chapter explores some of the major forces affecting mating systems. Our treatments of plants and animals differ in emphasis, but our goal is to use the perspective of evolutionary ecology to define more fully the similarities, differences, and diversity in plant and animal mating systems, and to highlight potentially interesting yet currently unanswered questions. Diversity in patterns of zygote production arises in part from ecological factors influencing two issues: selection on the evolution of sexual reproduction itself and differentiation of the sexes.

Ecological Specialization and Generalization

Anyone who is even slightly acquainted with plants or animals knows that different species inhabit different parts of the world, live in different habitats, and, in the case of animals, eat some imaginable kinds of food and not others. As with many other familiar facts, it may not occur to us to ask why the geographic and ecological ranges of species are limited, until we realize that species vary drastically in their geographic, ecological, and physiological amplitudes. The bracken fern (Pteridium aquilinum) is broadly distributed in temperate climates of every continent (except Antarctica), whereas the curly-grass fern (Schizaea pusilla) is limited to parts of eastern Canada and central New Jersey in the United States. The black-billed magpie (Pica pica) is a familiar bird from western Europe through eastern Asia and from Alaska to the Great Plains of North America, but the very similar yellow-billed magpie (Pica nuttalli) is restricted to central California. What accounts for the much narrower distribution of one than the other species? Related species often differ in the variety of habitats they occupy. The thistle Cirsium canescens is restricted to well-drained sandhills in the American prairie, whereas Cirsium arvense is a European species that has become a rampant weed in North America, growing in many types of soil. The endangered Kirtland's warbler (Dendroica kirtlandii) nests only in stands of jack pine of a certain age, while its relatives, such as the yellow warbler (Dendroica aestiva), nest in many types of vegetation and have far broader geographic ranges as well. (Species with narrow and broad habitat associations are referred to as stenotopic and eurytopic, respectively.) Stenotopic species or populations frequently have a narrower tolerance of certain physical variables than do others. Most plants and animals from warm tropical environments cannot survive freezing temperatures, and Antarctic notothenioid fishes cannot tolerate temperatures above 6°C. In contrast, species that inhabit environments where the temperature varies widely often have broad temperature tolerance. In many such species, individuals are capable of biochemical and physiological alterations that acclimate them to pronounced changes in temperature.