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, 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 [Crespiand 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...