Evolution of Behavior, Society, and Humans
Allen J. Moore
This section presents the current view of animal behavior and animal societies, and their application and relevance to human evolution, reflecting the return of researchers to the original integration of these themes promoted by Darwin in The Descent of Man and Selection in Relation to Sex. Darwin treated the evolution of behavior, society, and humans more extensively and exclusively in this follow-up to On the Origin of Species because these traits represented a particular challenge for the theory of natural selection. Why is there so much variation in behavior? How can apparently cognitively complex and advanced behavior (such as mate choice) evolve? What leads to the evolution of diverse mating systems and the associated morphological variations? Why should animals live in societies, cooperate, and help each other? And importantly, given the complexity of humans and human societies, can we find homologous traits between humans and other animals and simpler social systems? The Descent of Man provided answers to these questions and showed that social systems and complex behavior exist throughout the animal kingdom. Darwin recognized that behavior can be one of the most complex traits to evolve and can have profound consequences for species, including our own, in driving rapid evolution and promoting great variation both within and among populations and species. Humans may be especially interesting to us, but they aren’t special. What began as a challenge to the theory of evolution by natural selection—complex social behavior—has become one of the richest veins of research for testing and validating our current understanding of evolution.
The Descent of Man and Selection in Relation to Sex is arguably now nearly as influential as On the Origin of Species, and its title only hints at what was to become a major focus of research in biology in the twentieth century and beyond: investigating the evolutionary mechanisms of sexual selection, and understanding the diversity of mating systems and behavior. Although research and acceptance of sexual selection grew more slowly than research on natural selection, we have come to realize that just as natural selection provides an explanation for much more than the existence of different species, sexual selection explains much more than the descent of humans. In fact, following the Modern Synthesis, research on selection in relation to sex conspicuously ignored humans and focused more on understanding mating and animal behavior in general. Research into sexual selection, mating systems, communication, and social interactions was especially popular but mostly focused on insect, birds, fish, and mammals other than humans. Currently, this research is increasingly being applied to understanding human societies, behavior, and evolution as we find there are many shared aspects of behavioral evolution.
Our focus on Darwin’s theory of sexual selection raises a question for modern biologists: Are natural selection and sexual selection conceptually distinct mechanisms of evolution (as Darwin himself believed)? Or is sexual selection better considered as subsumed by natural selection? There is little agreement on this point, and a separation of sexual selection is often implied. Certainly, that is one explanation for this section and its greater focus on ideas developed in the Descent of Man over On the Origin of Species. Yet from a modern population genetic perspective, the contribution of reproductive success is not distinct from the contribution of survival to fitness—defined as the spread of an allele in a population relative to all other alleles in that population. As Futyma states in his introduction to Section III, “Natural selection occurs whenever there is a consistent, average difference in fitness (reproductive success) among sets of ‘individuals’ that differ in some respect that we may refer to as phenotype.” Under these definitions, sexual selection is the subset of natural selection dealing with fitness differences arising from competition for mates. Heuristically, however, it is convenient to treat them as distinct. We (like Darwin) often speak of natural selection as providing the limit to sexual selection. Following Darwin, we use sexual selection to explain the evolution of traits that would appear to be counter to the action of natural selection, that is, those traits that would appear to hinder survival rather than enhance it. So as a means of generating hypotheses, it is useful to consider them separate; however, that is not to suggest that sexual selection in any way contradicts natural selection or somehow provides a challenge or alternative. The expansion of natural selection to concepts that help explain unusual traits—such as kin selection explanations of altruism, or sexual selection explanations for elaborated traits expressed during mating—simply strengthens the logic of natural selection. The same is true for modern extensions of natural and kin selection to multilevel selection.
In this section we explore our current understanding of evolution of complex behavior and social systems—those traits that Darwin suggested might be considered problematic for natural selection—with examples from amoebas to mammals. We start out with proximate influences on behavior and how these relate to evolution. Darwin foresaw much, but he didn’t anticipate the discovery of the mechanisms of inheritance, DNA, and molecular genetics! Yet for behavior to evolve, there must be heritable genetic variation, as in any trait that evolves. In chapter VII.1, Yehuda Ben-Shahar provides an overview of genetic influences on behavior and why this matters. We often hear of “genes for” a behavior, but this shorthand is simplistic, misleading, and unfortunate. There is much more to behavior genetics than discovering “the gene for” some behavior. Understanding the influence of genetics on the diversity of behaviors, and when, where, and how this influence matters and varies, is in its infancy. Even less well understood are the details of the genes-brain-behavior relationship for most traits. The natural connection between these different levels is likely to center around hormones, and in chapter VII.2, Ellen Ketterson, Jonathan Atwell, and Joel McGlothlin explore the ways in which hormones and behavior are linked. Ultimately, our understanding of these causal mechanisms of behavior strongly shapes our understanding of the evolution of behavior and interactions.
One of the most powerful associations between understanding human behavior and exploring evolution occurred when George Price recognized that game theory, developed to explain human behavior associated with economics, could be applied to animal behavior and evolutionary problems in the 1970s. In chapter VII.3 John McNamara provides an overview of the remarkable advances in this area since Price’s paper appeared (coauthored with one of the major figures in subsequent theoretical developments in the field, John Maynard Smith). Game theory continues to be one of the most powerful paradigms for understanding the evolution of adaptive behavior.
Chapters VII.4, VII.5, and VII.6 cover the details of evolution by sexual selection. Rhonda Snook describes mating system evolution in general in chapter VII.4. She shows how understanding the mating systems of organisms provides insights into the evolutionary potential of populations. (The diversity of mating systems is in large part what inspired the theory of sexual selection by Darwin.) In chapter VII.5, Christine Miller explores how male-male competition results in the evolution of elaborate traits, while in chapter VII.6 Michael Jennions and Hanna Kokko explore how mate choice may do the same. There are clear connections between these chapters, but Darwin recognized two distinct mechanisms of sexual selection: male-male competition and female mate choice. In recent years there has been a focus on female mate choice, originally the more controversial of the two mechanisms. Now that evidence for female mate choice is overwhelming, we are seeing a return to an interest in male-male competition and how it influences sexual selection. Of course, total sexual selection reflects a combination of all mechanisms. Moreover, it is not always the females that choose and the males that compete; the sex roles may well be reversed, depending on the mating system.
Chapter VII.7 moves to communication, which is a fundamental part of most animal social systems yet presents special difficulties for understanding its evolution. Communication is one of those traits (like social dominance) that make little sense as a property of an individual by itself, as by definition communication involves interaction between at least two individuals. Michael Greenfield provides our current understanding of how communication evolves, and covers the various modalities involved in communication.
One of Darwin’s main concerns in The Descent of Man was the evolution of society. The simplest social group is a parent and offspring, and in chapter VII.8, Mathias Kölliker, Per Smiseth, and Nick Royle provide an overview of the evolution of parental care, and the importance of cross-generational effects for evolution. Chapter VII.9, by Joan Strassmann and David Queller, considers the theoretical basis for the roles of cooperation and conflict in structuring interactions, from cells (single cells to multicellularity) to organisms. Michael Cant follows in chapter VII.10 with a consideration of cooperative breeding, using insects and vertebrates as examples. Thus, the chapters on parental care and cooperative breeding represent a continuum of social interactions, linked by our current understanding of how cooperation and conflict evolve.
The preceding chapters focus mostly on animals and diversity, but as Darwin suggested, sexual selection is a driving force in structuring the evolution of humans and human society. The prolonged association of parents and children is key, and drives a competition for mating partners because of the extreme investment in offspring by humans. Virpi Lummaa in chapter VII.11 expands on this theme by describing current understanding of human behavioral ecology, which is very much influenced by parent-offspring and even grandparent-grandoffspring interactions. Human behavior presents special challenges for researchers, given the limit on the types of studies that are feasible. It also yields special rewards, as there is additional complexity to consider. No more complex is the consideration of “moral facilities” Darwin discusses in The Descent of Man. Robert Richardson, in chapter VII.12, presents the modern attempt to apply evolutionary approaches to understanding human psychology. As he shows, this effort has been only somewhat successful thus far, partly because the social interactions in humans are highly developed. This is not the complete justification, however, as shown when we return to animals and consider the most highly developed societies in eusocial organisms such as ants, bees, and wasps. Laurent Keller and Michel Chapuisat discuss the evolution of eusociality in chapter VII.13. Finally, Marc Hauser concludes a consideration of the trait we typically consider to be quintessentially human by examining cognition in chapter VII.14.
One of the dangers of evolutionary biology is simply to assume everything we see is adaptive and evolved “for” a specific purpose. Evolution, however, can be a powerful hypothesis for explaining why animals behave as they do, as demonstrated most clearly when we consider how evolutionary reasoning allows us to explore traits that on the surface, do not appear adaptive. In chapter VII.15 Nathan Bailey discusses traits such as behavior to attract predators, cannibalism, and same-sex sexual behavior as examples that allow us to explore the power of evolutionary approaches to understanding behavior. Finally, Jacob Moorad and Daniel Promislow explore aging and menopause in chapter VII.16, traits that are the exceptions that prove the rule for evolution. On the face of it, forgoing reproduction, aging, and dying are the embodiment of nonadaptive behaviors, yet evolutionary tests provide powerful insights for why these traits exist.
Some of the richest research themes in evolutionary biology have explored behavior. The diversity of behavior in the natural world is breathtaking, as are the often-elaborate traits associated with behavior. Our own species is characterized by complex social interactions, prolonged periods of parental care, extended family interactions, and competition for mates. Darwin recognized this and in his 1871 book, The Descent of Man and Selection in Relation to Sex, gave us a framework for exploring this diversity in nature. Behavior fascinates us, perhaps because it is both familiar and mysterious. It also provides a window on how evolution structures biodiversity and reveals the commonalities among organisms, from microbes to humans.