Social Evolution and Inclusive Fitness Theory

An Introduction

James A.R. Marshall

• Publisher: Princeton University Press
• Year: 2015
• ISBN:
  9781400866564
• Topic: Biological Sciences
• Subtopic: Biology
• Index: Biological Sciences

Social behavior has long puzzled evolutionary biologists, since the classical theory of natural selection maintains that individuals should not sacrifice their own fitness to affect that of others. Social Evolution and Inclusive Fitness Theory argues that a theory first presented in 1963 by William D. Hamilton—inclusive fitness theory—provides the most fundamental and general explanation for the evolution and maintenance of social behavior in the natural world.James Marshall guides readers through the vast and confusing literature on the evolution of social behavior, introducing and explaining the competing theories that claim to provide answers to questions such as why animals evolve to behave altruistically. Using simple statistical language and techniques that practicing biologists will be familiar with, he provides a comprehensive yet easily understandable treatment of key concepts and their repeated misinterpretations. Particular attention is paid to how more realistic features of behavior, such as nonadditivity and conditionality, can complicate analysis. Marshall highlights the general problem of identifying the underlying causes of evolutionary change, and proposes fruitful approaches to doing so in the study of social evolution. Social Evolution and Inclusive Fitness Theory describes how inclusive fitness theory addresses both simple and complex social scenarios, the controversies surrounding the theory, and how experimental work supports the theory as the most powerful explanation for social behavior and its evolution.

CHAPTER ONE

Social Behavior and Evolutionary Thought

1.1 EXPLANATIONS FOR APPARENT DESIGN

Animals, plants, and other organisms appear to be designed for some purpose. While the ultimate purpose may not always be clear to us, observers of the natural world can readily understand sophisticated “devices” such as the wing and the eye to be “designed” for flight and sight, respectively. Until the mid-nineteenth century, natural philosophy explained design in nature as being due to, and evidence for, the existence of a supernatural creator. One of the most famous late examples of this tradition is William Paley’s “argument from design” [Paley, 1802]; on discovering a pocket watch lying on a heath, the conclusion of any reasonable person is that, due to its apparent complexity and its evident purpose, it must have been designed, and therefore a designer (the watchmaker) must exist. Paley went on to argue that, should the discovered watch have an internal mechanism capable of producing copies of itself, the rational discoverer would still conclude that it had been designed for this purpose, in addition to its purpose of telling the time, and must still therefore have a designer. Similarly, the apparent complexity in construction of animals and plants, and fitness for a purpose which includes reproduction, means they must have been designed, and therefore a designer (God) must exist. Under such a view, of course, an anthropocentric natural theologist might conclude that the animals and plants around us have been designed, by the supernatural creator, with the primary purpose of giving us food to eat, natural resources with which to make things, and so on.

With the work of Charles Darwin and of Alfred Russel Wallace [Darwin and Wallace, 1858, Darwin, 1859], an alternative explanation for the appearance of design arrived and, simultaneously, the question of the ultimate purpose of organisms was answered. The ultimate purpose of organisms was to compete for individual reproduction, and the result of such competition was that natural selection would progressively improve their suitability for this purpose, thereby giving them the appearance of design. If flight would increase the chances of individual reproduction for members of a species, for example, then natural selection acting on heritable variation over many generations could fashion limbs into wings, and then progressively optimize them for the purposes of aerodynamically efficient flight. Design and purpose in nature were both explained, and the explanations did not suggest a supernatural designer.

Darwin and Wallace amassed significant empirical support for the theory of evolution through natural selection, in collections of animals from around the globe,¹ and Darwin also interacted with practitioners of artificial selection, such as pigeon breeders and farmers. Yet the new evolutionary theory was formulated without knowledge of how characteristics, which natural selection was supposed to act on, were inherited by offspring from their parents. In fact, only 8 years after Darwin and Wallace’s papers were read at the Linnean Society in London, Gregor Mendel discovered the particulate nature of inheritance in an abbey in Brno, through his experiments on pea morphology [Mendl, 1866]. Despite being contemporary with and crucially relevant to the theory of natural selection, Mendel’s results were ignored for over 30 years [Bateson, 1909]. Initially thought to be a replacement for Darwinian evolution, the field of genetics was ultimately reconciled with natural selection in a mathematical framework that came to be known as the “modern synthetic theory of evolution,” or “modern synthesis” for short [Huxley, 1942]. Primarily the work of three pioneers, Sewall Wright, J.B.S. Haldane, and R. A. Fisher (e.g., [Wright, 1932, Haldane, 1932, Fisher, 1930]), the modern synthesis gave a formal mathematical structure to Darwin and Wallace’s ideas that would enable them to be developed into a predictive theory as never before. Of particular importance, in The Genetical Theory of Natural Selection Fisher mathematically formalized individual reproductive success, which lies at the original heart of natural selection theory [Fisher, 1930]. Thus, with a few exceptions as discussed below, in explaining adaptation the modern synthesis firmly set the focus of natural selection at the level of the individual and their own direct reproduction.

1.2 NATURAL SELECTION AND SOCIAL BEHAVIOR

Although the examples described above of traits “designed” through natural selection are physical body parts, behaviors also have genetic components, and therefore can be shaped by natural selection. As William D. Hamilton put it very pithily, “It is generally accepted that the behaviour characteristic of a species is just as much the product of evolution as the morphology” [Hamilton, 1963]. Behaviors that improve the reproductive success expected by an individual often have a negative impact on reproduction of members of the same species; one obvious example is behaviors involved in competition over mates, such as in display and fighting by red deer stags (figure 1.1); by monopolizing access to females, a male improves his own reproductive success at the expense of other males. Natural selection theory as developed by Darwin, Fisher, and others has no problem explaining the evolution of such behaviors; indeed it predicts them. This theory acts according to the reproductive success of individuals, and when the side effects of any trait are to modify the reproductive success of unrelated individuals, these are irrelevant.

Other individual behaviors seem to impact on the reproduction of others in a much more “deliberate” manner, however. Examples of such social behaviors abound in the natural world. Quite possibly the most well-known examples are among the social insects, considered by Darwin himself [Darwin, 1859]. In these insect species, reproductive division of labor is observed, with one or more castes helping to raise offspring other than their own; this is referred to as eusociality [Crespi and Yanega, 1995]. The simplest pattern is that the daughters of a single reproductive female, the queen, forage for, defend, and raise her offspring. These worker daughters either have suppressed levels of reproduction, as in the honeybee Apis mellifera where workers may both reduce their own levels of reproduction and destroy eggs laid by other workers [Ratnieks and Visscher, 1989], or are completely functionally sterile, as in several species of leafcutter ant for example (figure 1.2). Cooperative breeding is also observed in vertebrates, including many species of birds (e.g., figure 1.3) and mammals, such as meerkats (Suricata suricatta; e.g., [Clutton-Brock et al., 1998]) and naked mole rats (Heterocephalus glaber; [Jarvis, 1981]).² Cooperative breeders exhibit similar behaviors to eusocial species, in that helpers forage for, and guard, the offspring of a single breeding pair, although helpers do not form a distinct caste and may subsequently become reproductives themselves [Crespi and Yanega, 1995]. The presence of helpers has been shown to improve reproductive success by the breeding pair (e.g., [Hatchwell et al., 2004]), yet the helpers necessarily forego their own reproduction while caring for offspring that are not their own (e.g., [Emlen, 1982]).

Figure 1.1: A red deer stag (Cervus elaphus). Stags possess large antlers which impact on performance in fights, dominance rank, and hence access to fertile females. Maintenance of a harem of females, and hence increased reproductive success, negatively impacts on the reproductive success of other males in the population. However, natural selection theory (as developed by Darwin, Fisher, and others) acting on individuals explains the evolution of antlers since the successful male’s net personal reproduction is increased as a result of having them. Photograph by Loeske Kruuk, reproduced from [Kruuk et al., 2014] with the permission of the photographer.

Less frequently appreciated, social behavior is also observed in microbes including amoebae and bacteria [West et al., 2007a]. In social amoebae (Dictyostelium sp.; figure 1.4) normally free-living individuals aggregate at times of ecological stress, with some amoebae sacrificing themselves to form a structure that raises other individuals up in order to facilitate their dispersal to new, potentially richer, locations (figure 1.4) [Raper, 1984]. In the bacterium Pseudomonas aeruginosa, as in many other microorganisms, individuals secrete siderophores, which scavenge iron from insoluble forms in the environment. Siderophore production is individually costly in metabolic terms, resulting in a reduced growth rate, but this is offset by the increase in growth rate that siderophores facilitate when iron is scarce [Griffin et al., 2004, Jiricny et al., 2010] (figure 1.5A). However, siderophores secreted by individual bacteria can also facilitate iron uptake by neighboring individuals, allowing them to benefit from an increased growth rate, even if those neighbors did not contribute to siderophore production themselves [Griffin et al., 2004, Jiricny et al., 2010] (figure 1.5B).

Figure 1.2: Leafcutter ants of the genus Atta have morphologically distinct worker castes [Wilson, 1980], such as this forager (carrying leaf) and minim (sitting on leaf). In eusocial insect colonies, a worker caste or castes are either partially or totally functionally sterile, reducing or foregoing individual reproduction in order to support the reproduction of their mother. Atta colombica workers, although still possessing functioning ovaries, are effectively sterile [Dijkstra et al., 2005, Dijkstra and Boomsma, 2006]. Photograph by Chris Tranter, reproduced with permission of the photographer.

Less munificent examples of social behavior have also been described. Let us take one important example: bacterial production of bacteriocins. Production of colicins by the bacterium Escherichia coli, for example, is fatal for producing cells, as well as killing neighboring cells within a narrow phylogenetic range [Riley and Wertz, 2002]. Thus, bacteriocin production is personally costly (colicin producers pay the ultimate price of death, thereby ceasing personal reproduction), as well as costly to the targets of the behavior. Similarly, Pseudomonas bacteria produce individually costly pyocins that inhibit growth of strains that do not possess corresponding immunity genes [Michel-Briand and Baysse, 2002], as illustrated in figure 1.6.

Figure 1.3: A long-tailed tit chick (Aegithalos caudatus) is fed an invertebrate by an adult helper. Long-tailed tits are facultatively cooperative breeders; individuals that have failed to breed successfully themselves may help to raise the offspring of another breeding pair by feeding their chicks until independence [Hatchwell and Sharp, 2006, Hatchwell et al., 2014]. Photograph by Ben Hatchwell, reproduced with permission of the photographer.

Some purely physical traits can also have positive or negative social effects on conspecifics. One example is aposematism, for example in caterpillars (figure 1.7), in which individuals evolve both to be unpalatable to predators, and to bear conspicuous markings that indicate their unpalatability. As described below, Fisher himself considered the problem of aposematism, the initial evolution of which would be personally costly since conspicuous markings increase the probability of detection by a predator. A conspicuous distasteful individual being consumed would benefit aposematic members of the same species, however, by informing the predator that conspicuous markings mean unpalatability and thereby deterring them [Fisher, 1930].³ Thus, while many social effects on conspecifics are due to behavior, not all are.

Examples such as these, and many others, have long presented a puzzle for evolutionary biology. The puzzle is that, under Darwin’s and Fisher’s views of natural selection acting on personal reproduction, it seems to make no evolutionary sense for individuals to reduce their personal reproductive success, possibly to zero, in order to have an effect on the reproduction of others. Natural selection should favor traits that increase personal reproductive success, hence personally costly traits of the kind described above should experience negative selection, and be eliminated from any population in which they appear. Yet the examples we have just seen seem not to be of transient social behaviors in the process of bein...

Table of contents

• Cover Page
• Title Page
• Copyright Page
• Dedication Page
• Contents
• List of Figures
• Preface
• Acknowlegments
• 1: Social Behavior and Evolutionary Thought
• 2: Models of Social Behavior
• 3: The Price Equation
• 4: Inclusive Fitness and Hamilton’s Rule
• 5: Nonadditive Interactions and Hamilton’s Rule
• 6: Conditional Behaviors and Inclusive Fitness
• 7: Variants of Hamilton’s Rule and Evolutionary Explanations
• 8: Heritability, Maximization, and Evolutionary Explanations
• 9: What Is Fitness?
• 10: Evidence, Other Approaches, and Further Topics
• Glossary
• Notes
• Bibliography
• Index