Interaction and Coevolution

John N. Thompson

• Publisher: University of Chicago Press
• Year: 2014
• ISBN:
  9780226127323
• Topic: Biological Sciences
• Subtopic: Science General
• Index: Biological Sciences

"It is not only the species that change evolutionarily through interactions... the interactions themselves also change." Thus states John N. Thompson in the foreword to Interaction and Coevolution, the first title in his series of books exploring the relentless nature of evolution and the processes that shape the web of life. Originally published in 1982 more as an idea piece—an early attempt to synthesize then academically distinct but logically linked strands of ecological thought and to suggest avenues for further research—than as a data-driven monograph, Interaction and Coevolution would go on to be considered a landmark study that pointed to the beginning of a new discipline. Through chapters on antagonism, mutualism, and the effects of these interactions on populations, speciation, and community structure, Thompson seeks to explain not only how interactions differ in the selection pressures they exert on species, but also when interactions are most likely to lead to coevolution. In this era of climate change and swiftly transforming environments, the ideas Thompson puts forward in Interaction and Coevolution are more relevant than ever before.

CHAPTER

1

EVOLUTIONARY ECOLOGY, INTERACTION, AND COEVOLUTION

As species have evolved and multiplied over the past three and a half billion years, so have the interactions that link their life histories and shape their further evolution. Although interactions are often more ephemeral and certainly less tangible than species, they are as much a product of evolution as is bone, chitin, or cell wall: biological communities differ from zoos and botanical gardens because of the interactions between species. Therefore, the study of the origins and evolution of interactions between species is as crucial to an understanding of the evolution of life as is the study of the origins and evolution of species.

We know much about the effects of interspecific interactions on the life histories, morphologies, and behaviors of organisms and on the size, structure, and dynamics of populations. However, we lack an overall conceptual framework for the evolution of interactions that could suggest general patterns in the ways organisms respond evolutionarily to interactions and the ways interactions change over evolutionary time. If we can identify general patterns, then we can better understand the constraints that different kinds of interaction impose on the evolution of organisms and the changes that occur in the interaction structure of communities over evolutionary time.

My purpose in this book is toward a general theory for the evolution of interspecific interactions. Specifically, I focus on the following set of questions:

1. Are there general patterns in how interactions differ in the selection pressures that they exert on organisms?

2. Are there general patterns in how interactions are likely to change in their effects on the fitness of organisms over evolutionary time?

3. Under what ecological conditions is coevolution likely among interacting species?

That is, how do interactions differ evolutionarily, how do they change, and when do they generate reciprocal change among species?

Chapters 2 and 3 are devoted to the evolution of antagonistic interactions. I begin in Chapter 2 by considering differences in patterns of specialization, defense, and coevolution between parasites, grazers, and predators and their victims. This chapter emphasizes that the mode of interaction between species is critical to understanding how selection acts on interactions and when coevolution is likely. The conclusions of this chapter are carried through the remainder of the book. In Chapter 3 I contrast competition with other kinds of antagonistic interaction and consider the conditions under which long-term coevolution is likely between competitors.

Chapters 4, 5, and 6 concern the evolution of mutualisms. In Chapter 4 I discuss the close evolutionary relationship between antagonism and mutualism and argue that the commonness of mutualisms in communities often depends evolutionarily on the richness of antagonistic interactions. In Chapter 5 I consider general and specific aspects of life histories that favor the evolution of mutualisms. These two chapters provide the background for the range of ecological conditions that are likely to favor mutualisms, and Chapter 6 considers the subset of mutualisms that are likely to generate coevolution among mutualists.

Chapter 7 is a departure from the flow of argument on coadaptation in Chapters 2 through 6. This chapter considers the effects of different kinds of interaction on patterns of speciation and on the likelihood of cospeciation resulting from interactions. I differentiate cospeciation from simple phylogenetic tracking of one taxon on another. I argue also that the tempo of speciation may differ between species involved in the same interaction and this may influence importantly our views on the commonness of cospeciation.

Finally, Chapter 8 concentrates on a group of questions that form the basis for the study of the interaction structure of communities and for the importance of coevolution in structuring interactions within communities. These questions concern the pattern of development and change in interactions within and among communities in contemporary time—the patch dynamics of interactions—and the growth and change in interactions over evolutionary time through coadaptation, cospeciation, and collection of unrelated species into interactions.

Together the arguments in these chapters are an attempt toward a general framework within which to study the evolution of interactions, the likelihood of coevolution among interactions, and the interaction structure of communities. I emphasize throughout the conditions under which coevolution is likely or unlikely in the evolution of interactions. Natural communities are not superorganisms, but they are also not random collections of species with no evolutionary effects on each other. The study of patterns in coevolution can help us to understand where and when interactions will bind the gene pools of two or more species in a community through reciprocal evolutionary change.

THE COEVOLUTIONARY PERSPECTIVE

Coevolution is reciprocal evolutionary change in interacting species. The key word is reciprocal in the sense of mutual. In an interaction between two species, both species must undergo evolutionary change specifically in response to the interaction to be called a coevolved interaction. As Janzen (1980a) notes, simply showing mutual congruence of traits between a pair of species does not necessarily indicate coevolution has occurred. Upon entering a new habitat, a species will tend to interact with other species whose traits are most congruent with its own, as in phytophagous insects that colonize introduced plants (e.g. Strong, 1974, 1979). No coevolution may have occurred between the species in this instance. The concept of coevolution is a powerful tool for evolutionary theory and the use of the term coevolution, as well as its sister terms coadaptation and cospeciation, should be used carefully to describe only interactions where the evidence suggests that reciprocal evolution has occurred.

The other key part of the definition as given here is that coevolution involves the partial coordination of nonmixing gene pools. That is, it is an interspecific process. Although this is the way the terms coevolution and coadaptation are used mostly in evolutionary ecology, these terms have been used in other subdisciplines of evolutionary theory to describe coordinated evolution at lower levels in the hierarchical organization of life. Even Darwin used the term coadaptation in two senses in the Origin. In the introduction he wrote of the “coadaptations of organic beings to each other and to their physical conditions of life.” The first usage is the sense in which the term is used today in evolutionary ecology usually interchangeably with the term coevolution. The second usage relates more to the coordinated development of parts within an organism rather than to reciprocal adaptations between species. In addition, Dobzhansky (1970 and earlier) used the phrase coadapted gene complexes in the specific sense of mutual adjustment of closely linked genes that function together within chromosomes, and that usage continues within the field of population genetics (Lewontin, 1974; Roughgarden, 1979). At the level of molecular genetics, others have written of the coevolution of the genetic code (Lacey et al., 1975; Wong, 1975). Since there is no arbiter of terms in science, all of these uses are likely to continue side by side in the literature; in the following chapters coevolution (coadaptation) always means reciprocal change (adaptations) among interacting species.

THE DEVELOPMENT OF THE COEVOLUTIONARY PERSPECTIVE

The coevolutionary perspective has developed as a merger of several research orientations. Although a full history is not possible here, it is worthwhile to emphasize a few points to show the variety of research directions from which the perspective has developed. Ehrlich and Raven’s (1964) study on coevolution in butterflies and plants was certainly the paper that established the coevolutionary perspective as a major framework within which to study the evolution of interactions. Brues (1924) made similar arguments earlier for interactions between insects and plants (see Gilbert, 1979), but his arguments deal more with host shifts in insects than with reciprocal evolution and were made before the science of evolutionary ecology had developed sufficiently to incorporate a coevolutionary approach to the study of interactions. When Ehrlich and Raven’s paper appeared in 1964, however, evolutionary ecology was rapidly coalescing as a major branch of ecology. Lack’s studies of birds were cast explicitly in the framework of evolutionary ecology and his 1965 presidential address to the British Ecological Society was entitled “Evolutionary Ecology.” Hutchinson’s (1965) book The Ecological Theater and the Evolutionary Play also reflects the development of this orientation in ecology as does Orians’ (1962) paper entitled “Natural Selection and Ecological Theory.” The study of coevolution fit comfortably within the developing field of evolutionary ecology.

At least two other research approaches were also leading toward the development of a coevolutionary perspective in the early 1960s. Flor’s (1942, 1955) concept of gene-for-gene interactions between parasites and hosts, developed initially in the literature on phytopathology, was being introduced into the broader literature (e.g. Person et al., 1962). Mode’s (1958) paper in Evolution, entitled “A mathematical model for the co-evolution of obligate parasites and their hosts,” is probably the first mathematical model of the genetics of coevolution and is explicitly a model of Flor’s results on gene-for-gene interactions in flax and flax rust.

In addition, Pimentel’s studies of what he calls genetic feedback began appearing in 1961. These studies are aimed at understanding the relationship between coevolution and population regulation, although he does not use the term coevolution in his early papers. The logic of these experiments is as follows: organisms adapted to feeding on a host are able to achieve high population densities; these high densities create strong selection pressures on host populations and select for resistance to attack; this feeds back negatively on the enemy (predator or parasite) population; after many population cycles, enemy populations are ultimately limited and stability results (Pimentel, 1961). This effect has been shown to some extent in the housefly Musca domestica and its parasitoid Nasonia vitripennis when the parasite is interacting with resistant hosts as compared with susceptible hosts under laboratory conditions (Pimentel et al., 1978). The parasite populations on experimental (resistant) hosts oscillate around a lower mean, oscillate less in absolute numbers of individuals, and have an overall tendency toward decreased oscillation. This, of course, is only one facet of coevolution and under these conditions, the host is not freely evolving in response to the parasite from the start: the experiments were begun with populations of susceptible and resistant houseflies. Although the assumptions of the genetic-feedback models were highly restrictive (Łomnicki, 1971; Slatkin and Maynard Smith, 1979), the perspective of the experiments was nonetheless coevolutionary.

The study of coevolution, therefore, developed from a variety of research orientations and proceeded hand-in-hand with the development of evolutionary ecology as a major research framework. Janzen’s (1966, 1967) landmark study of acacias and acacia ants illustrated how coevolution could be studied through a combination of solid natural history observation and experimentation within natural communities. By 1975 a variety of interactions between animals and plants could be summarized from a coevolutionary perspective in the important volume on Coevolution of Animals and Plants edited by Gilbert and Raven. Mathematical modeling of coevolution in two-species systems also became an important direction for modeling in population genetics and evolutionary ecology in the 1970s (Roughgarden, 1979; Slatkin and Maynard Smith, 1979).

Together these approaches moved the study of coevolution toward analyses of general patterns among particular kinds of interaction. For example, Price (1977, 1980) asks how coevolution between parasites and their hosts could differ from coevolution between predators and prey, and Connell (1980) suggests why coevolution may be infrequent among competitors. This book, then, is part of the search for patterns in coevolution and in the evolution of interactions in general.

CHAPTER

2

PARASITISM, GRAZING, AND PREDATION

Antagonistic interactions occur between species because living organisms are concentrated packages of energy and nutrients (trophic interactions) and because resources are limited (competition). That species respond evolutionarily to these interactions is evident immediately; Darwin used antagonistic interactions more than any other kind to illustrate in the Origin of Species how selection works. The problem in evolutionary ecology, however, is not simply to catalog how species respond evolutionarily to antagonistic interactions but rather to discern patterns in how species respond.

Some evolutionary patterns may result from the ways organisms feed on other species. Organisms differ greatly in how they attack their victims, including whether they kill their victims, how long they remain to feed on a single victim before killing it or leaving it, and how many victims they feed upon during their lifetimes. These differences in modes of feeding influence how (1) organisms specialize on their victims, (2) victims defend themselves against enemies, and (3) coevolution proceeds between enemies and their victims. This chapter considers patterns in specialization, defense, and coevolution between parasites, grazers, and predators and their victims in an effort to find patterns in interaction and coevolution that transcend taxonomic boundaries.

MODES OF FEEDING

The number of ways of categorizing interactions between species is probably unlimited. Terms such as grazer, browser, predator, parasite, herbivore, and carnivore vary among researchers in the breadth or narrowness of their usage (Dindal, 1975; Starr, 1975). For example, Harper (1977) uses the term predation in a general way to describe all the different ways that herbivores feed on plants, whereas Lubchenko (1979) restricts the use of the term to consumers that kill their hosts. All classifications of interactions are necessarily artificial, and their functional purpose can be only as aids to grouping some of the differences in how species interact. Here I separate modes of feeding into parasitism, grazing, and predation because these categories seem useful in assessing some patterns in how selection acts on interacting species. These categories are no more discrete than the concepts of population or community, but like these latter concepts they provide a useful tool for comparative studies in ecology.

Parasitism

A parasite is an organism that lives throughout a major period of its life in or on a single host individual, deriving its food from the host and causing lowered survival or reproduction in the host. Although the term parasite is used most often with reference to small animals or microorganisms that live in or on larger animals—as suggested by the usual content of parasitology journals and texts—this way of obtaining food is common among many taxa. Parasites include, for example, parasitic fungi of plants, herbivores such as caterpillars and aphids that spend all of their larval or nymphal stages on a single host plant, insect parasitoids of other insects that live as larval parasites in their hosts but have a free living adult stage, as well as the parasites usually considered in parasitology such as the cestode parasites of animals. Including the interactions between some phytophagous insects and plants in the application of the term parasite does not broaden the use of the term beyond utility, as has been suggested by some authors (Holling, 1980; Brooks, 1981). Instead...