Review of : Andrew, F. G. Bourke . 2011 . Principles of Social Evolution . Oxford University Press , Oxford . xii , 267 Pages . ISBN13: 9780199231157; ISBN10: 019923115X

Scientists are famously nerdy, their heads up in the clouds, but socially unaware, unconcerned, or perhaps simply awkward or inept. One is tempted to think that social detachment can clear the way for understanding the material world, where intents, strategies, alliances, and social cheating play no role. This account is less than the full truth, for we all know many counterexamples of scientists who are socially adept. A different kind of counterexample was provided by W. D. Hamilton. Although fitting the brainy but socially awkward stereotype, he focused his genius on the topic of sociality itself, unveiling the evolution of a vast world in animal behavior ruled by phenomena much like those intents, strategies, alliances, and social cheating.

Andrew Bourke's Principles of Social Evolution updates Hamilton's insights, but it is not a book for those who still regard the business of social evolution as only “the beehive and the baboon troop.” The field of social evolution did indeed get its start in the world of animal behavior, but it has long since delved into deeper questions. In fact, almost from the very beginning, Hamilton and other early sociobiologists began to ponder issues like cooperation and conflict among genes within organisms. At this level, they re-encountered the same kinds of questions that we see in groups of animals. Should I cooperate with my neighbor? Are there fitness gains to be had from helping other copies the same gene, or from social feedbacks to my own fitness? How do I avoid being exploited by noncooperators, and might it be better to defect myself to try to exploit my cooperative neighbors? You can ask these questions of genes in a cell, of organelles like mitochondria and chloroplasts, and of cells in multicellular groups.

John Maynard Smith and Eors Szathmáry took this a step farther and noted that once in a great while, overcoming the sometimes formidable barriers to cooperation leads to major evolutionary transitions. The prokaryotic cell, the eukaryotic alliance, sex, multicellularity, and superorganismal colonies are all results of such cooperative transitions. It is largely this theme that Bourke develops, building from the original arguments and evidence based on animal behavior. He opens by asking us to imagine ourselves as scientifically curious and well-equipped protozoans from one and half billion years ago. By virtue of their teeny instruments, including a time machine, they discover with shock that their future is dominated by unspeakably immense beasts, and that each of these is composed of innumerable normal individuals (i.e., unicellular ones), stuck together and twisted into diverse specialized forms. Twirling the time machine dials in the other direction, they are again astounded, this time learning that the ancient world consists exclusively of prokaryotes, some of which form the building blocks of their own complex little eukaryotic bodies. This opening passage is the most sustained of a number of colorful riffs, as if there were a popular book yearning to emerge from this one. These are fun, although most of the book is real science with writing that is necessarily more staid. Yet, it is remains much more accessible than Maynard Smith and Szathmáry's Major Transitions.

Bourke divides the main part of the book among three stages in a major transition. Social group formation is about the forces that initially select for cooperation. Social group maintenance is primarily concerned with control of cheaters—variants that might exploit the cooperation without paying the costs. Social group transformation describes the process by which cooperation becomes so integrated that a new level of organization evolves—a major evolutionary transition. This structure lends the book a bit of a progressivist air; it sometimes seems as if social group formation and maintenance are simply steps on the way to transformation. Bourke makes it clear, however, that the process can stop at any point, that formation does not necessarily lead to maintenance, and maintenance does not necessarily lead to transformation. But there is a sort of progressive element to evolution inherent in the major-transitions framework, or in the multilevel selection framework. Every once in a while, formerly independent units become so cooperatively integrated that a new level of individuality emerges, with such far-reaching consequences that the process can hardly be reversed.

Bourke divides the types of major transition, and the types of sociality, into two, following a suggestion I made some years ago in a review of Maynard Smith and Szathmáry's book. I called the two types fraternal and egalitarian, playing off the French revolutionary slogan, with a third category, libertarians, being the noncooperators. Fraternal cooperation is based on helping relatives who tend to share the cooperation gene. Egalitarian cooperation relies on gains to the cooperator's own personal fitness, usually mediated through mutualistic interactions with members of another species. It is no surprise then, that from the growing number of theoretical frameworks with which one can view social evolution, Bourke chooses to rely primarily on Hamilton's inclusive fitness thinking. Much of the early part of the book is devoted to clearly laying out how this approach works, and the rest of the book exemplifies how effective it has been. The basic distinction between helping genes in your own body and helping copies in some one else's body is simple and has far-reaching consequences. Most notably, only fraternal associations can evolve sterility among some of their members, whereas egalitarian ones derive their name from the fact the members can gain only if they all continue to reproduce.

The book touches repeatedly on instances of cooperation at many levels, but Bourke focuses most of his effort on two of these: the grouping of cells in multicellular individuals and the grouping of individuals into colonies. It makes sense to focus on these two kinds of major transitions because they are the most accessible to study, being more recent than events like the origin of cells. They are also among the most similar, both being fraternal transitions where some individuals completely give up reproduction to help relatives. It also makes sense because they show multiple instances of major evolutionary transitions, and even more instances of cases that did not make the full transition to a new level of organization. Some social insect colonies, like those of the honey bee, can be reasonably argued to be organismal in their own right. But many social insect colonies are not, and so provide great opportunities for studying the process.

Bourke is himself a social insect researcher, and some portions of the book revisit issues from his earlier masterful work, Social Evolution in Ants (coauthored with Nigel Franks). But here these issues are set against and compared to comparable ones having to do with cooperation of cells in multicellular groups. Sometimes the parallels seem close and other times less so. Protection from predation seems to have played an important role in the origin of sociality in many social insects, and perhaps in many multicellular organisms. But Bourke also notes other diverse advantages to sociality in different taxa. For example, in some groups multicellularity is advantageous because it promotes dispersal, and in other groups because it promotes sedentariness, and neither of these seems important in social insects.

Once groups have arisen, the control of conflicts comes about in both groups through some combination of high relatedness and enforcement or power. In social insect colonies, high relatedness is pervasive and apparently essential. All eusocial origins appear to be from ancestors that were singly mated, so that relatedness among the progeny would be undiluted by multiple paternity (multiple mating arose later in some groups, like honey bees and some fungus-growing ants, after cooperation was well entrenched). But because most social insects are sexual, relatedness within their colonies is not unity and so some potential conflicts remain to be controlled by enforcement. In small colonies the queen may be able to dominate workers and keep them from reproducing. In larger colonies, where this is less likely, the remarkable phenomenon of worker policing often evolves, with workers preventing each other from reproducing.

When cells combine into multicellular groups, the balance of relatedness and enforcement appears different, at least for those that do undergo the transition to multicellular individuals. Most of these are uniclonal; they typically start from a single cell that divides repeatedly, yielding a group of cells that are essentially completely related to each other. That means that conflicts are greatly reduced from the very beginning, although they may need to evolve means to reject of any foreign cells they encounter. Aside from this, perhaps little enforcement is necessary, however, Rick Michod has shown that conflicts could be an issue even in clonal organisms if cheater mutants arise with sufficiently high frequency. Bourke therefore considers the difficult question of whether traits like early germline sequestration might have evolved to limit spread of selfish mutants and enforce cooperative behavior.

Perhaps the most novel part of the Bourke's scheme is the topic of social group transformation. Here Bourke builds partly on his own prior work on transformation in the social insects. It is clear that the most complex colonies, by a variety of measures, tend also to be large ones. For example, leaf-cutter ants and army ants have very large colonies, and also have multiple castes and elaborate ways of making a living, agriculture on the one hand, and nomadic style of cooperative predation on the other. A similar trend holds for multicellular organisms. On average, the larger the organism, the greater the complexity, as measured by number of cell types.

Bourke therefore proposes, following John Bonner and others, a size-complexity hypothesis for fraternal cooperators (but not egalitarian ones where a high degree of specialization is already present in the joining of two species with different talents). This hypothesis postulates that a positive feedback loop develops between size of the group and its complexity, with increased size selecting for increased complexity, and vice versa. The idea is appealing, and evidence such as the correlations described above is somewhat in accord with it, but I think we have a long way to go before we reach the level of understanding that we have for the other two stages of the process. Bourke treats the evidence honestly and points out its weaknesses as well as its strengths. The correlations are not terribly strong. There are certain organisms with many cell types that have orders of magnitude fewer cells than certain organisms with fewer cell types. And to the extent the correlations are true, we want to understand the full range of variation. If there are positive feedbacks, what causes some organisms get stuck at medium levels of complexity? Are they on their way to higher levels, or do the positive feedbacks apply only in some circumstances?

Part of the problem is that we have shifted from what I would call questions of heritability to questions of selection. In considering the origin and maintenance of cooperation, a vital question is how the cooperative trait gets transmitted when its benefits may go to some one other than the actor. This question of heritability has a relatively simple answer for fraternal organisms: high relatedness. Once organisms solve that problem and have reduced conflicts, we are left with the question of why some low-conflict groups become ever more complex, and others do not. This step seems to be what seals, or does not seal, a major transition. The transition to another level of selection has occurred, but how major will it be? The answers here must lie not in the fairly well-understood area of genetic transmission but in the much more complex challenges posed by environments (ecology) and in the much more complex ways that organisms respond to them (physiology).

For those who simply want the behavior of the beehive and the baboon troop, there may be other books that are more suitable. But for those who want to understand how baboons, beehives, and inclusive fitness have changed our view of the deep structure of life, Principles of Social Evolution is a great place to start.

Thanks to Joan Strassmann for useful comments on an earlier draft.

Associate Editor: M. Wade