Unless you're Brad Pitt or Megan Fox, attracting mates can be a complicated process, and most will agree that some degree of competition is involved. Limited resources of value, whether they be other people, places to live, or food, will lead to competition among individuals or societies that attempt to secure them. Whether it is good or bad, natural or unnatural, competition underlies much of the current human condition.

To see what this has to do with Joan Roughgarden's book, The Genial Gene: Deconstructing Darwinian Selfishness, some history is useful. Charles Darwin proposed the theory of sexual selection as a corollary to natural selection because he recognized that animals possess many traits that appear detrimental to survival, such as encumbering decoration and gaudy coloration. He proposed that such traits are beneficial, even if they reduce survival, if they confer a long-term advantage in terms of relative mating success. Darwin recognized that such an advantage could accrue either because elaborate traits determined the outcome of male-male competition or because females preferred them.

The theory of sexual selection was largely discounted for 75 years or so, because although biologists (most of whom were males) agreed that malemale competition was obvious, they mostly disagreed that females actively influenced the distribution of mating. Yet over the last 50 years, biologists have documented time and again that female choice is often the most important process determining who mates with whom. Since this realization, evolutionary biologists and behavioral ecologists have embraced sexual selection as critical to understanding both morphological and behavioral diversity. The underlying premise that organisms compete for a limited resource, which determines success or failure in reproduction, is central not only to sexual selection but to many other ideas about the evolution of life.

In The Genial Gene, Roughgarden argues that we have it all wrong. Even Darwin had it all wrong, she holds: Sexual selection is “out” (as an intact theory). Also wrong is everyone who thinks that competition was important in the evolution of anything to do with sexual reproduction, the evolution of male and female gametes, secondary sexual traits, morphological differences between males and females, mating systems, parental care, enlarged brains in humans, and human attractiveness (to list just some areas). This is no small challenge. The author argues that almost 100 years of research on sex has, at some level, been misguided. Where have we all gone wrong? Roughgarden believes our mistake was being seduced by competition as a force underlying social behavior and sexual reproduction. What is the alternative? The author is convinced it is cooperation, and she expands on a theory of social selection (originally proposed by Mary Jane West-Eberhard) that she hopes will replace sexual selection.

Take mating systems, for example. The standard view is that whether a species is socially monogamous or polygamous is the result of a basic conflict of interest between the sexes (males attempting to mate with many females, females attempting to secure resources), and how this conflict is resolved in different ecological situations. Roughgarden instead argues that a species mating system is the result of cooperation between the sexes for the mutual benefit of both males and females in terms of successfully rearing offspring. The author acknowledges that competition exists, although she discounts widely accepted examples of conflict as cases of anthropomorphic exaggerations. Instead, she believes that the notion of a conflict of interest between the sexes is a “fad” rather than an underlying paradigm. Similarly, proponents of sexual selection generally acknowledge examples of cooperation in reproduction. The question that Roughgarden repeatedly raises, however, is: What is the prevalent state? Did sexual interactions evolve as a result of competition, with cooperation occurring rarely; or, as the author argues, is cooperation the common condition, with competition arising only under special circumstances? The question is anything but hair-splitting.

Any member of the educated public will grasp the basic ideas in the book, but The Genial Gene is clearly directed at those biologists who subscribe to sexual selection as a guiding principle. Roughgarden is on a mission to convince them that they have been misled.

The Genial Gene is a relatively short book (255 pages) in which to take on the entire discipline of sexual selection and social behavior, but it is just one in a collection of publications in which the author presents her case for cooperation and diversity. The natural history observations that underlie much of Roughgarden's social selection theory are summarized in Evolution's Rainbow (University of California Press, 2004 and 2009), and specific applications of the theory are detailed in many scientific publications. The author makes it clear in this book that more is yet to come.

Any member of the educated public will grasp the basic ideas in the book, but The Genial Gene is clearly directed at those biologists who subscribe to sexual selection as a guiding principle. Roughgarden is on a mission to convince them that they have been misled. She appears to face an uphill climb. For example, a 2006 paper by the author and colleagues in the journal Science (in which they present cooperation models as alternatives to sexual selection) brought several dozen criticisms from leading authorities in sexual selection.

This book consists of three parts. In Part I, “Cooperation and Teamwork,” the author presents her case that the theory of sexual selection is dead and outlines social selection. I found this part to be the most difficult to accept. Yes, the theory of sexual selection has problems explaining some behaviors; however, just as the theory of natural selection has been frequently modified (for example, to accommodate kin selection), so has the theory of sexual selection been modified as new data and ideas have come to light. The author's implication that sexual selection always refers to “passionate males” and “coy females” is wrong, given that it is well known that sometimes males invest more into raising offspring than females.

Additionally, in my opinion, the author carefully picks out research results that are difficult to explain by sexual selection, and ignores results that support it. Mate choice is an example, or specifically, the female choice for traits in males. In cases where males provide physical resources, theory suggests that females should evolve a preference based on these resources, and this preference has been observed in many studies. Roughgarden ignores these. Sexual selection theory has more difficulty accounting for cases where males provide only sperm; the evolution of female choice in these circumstances has been debated for 40 years. But, even if this “paradox of the lek” has not been completely resolved, the underlying premise of sexual selection (that the choosy sex should be careful in mating decisions) is not necessarily wrong.

Part II is “The Genetic System of Sex.” Here the author outlines alternative theories for the evolution of sexual reproduction: why sex evolved, why there are only two gametes, and why there is diversity of sexuality (male vs. female, hermaphroditism, etc.). I found this section quite enlightening. The author points out some plausible alternatives to standard explanations. For example, the standard explanation as to why sexually reproducing species have one large gamete (egg) and many small gametes of the other sex (sperm) is that disruptive selection on gamete size occurred through conflict among individuals producing gametes. But Roughgarden summarizes other models for the evolution of sperm and egg that do not rely on conflict.

Part III is “The Social System for Sex,” in which the author examines behavioral systems and asks whether theoretical questions are better tackled by a competition-based approach (e.g., considering evolutionaly stable strategies) or by a cooperation-based approach (e.g., Nash bargaining solutions). There are many game theoretic approaches to behavioral questions, and biologists should indeed consider all possible models. This part concludes with a chapter summarizing how Roughgarden's view affects a wide range of evolutionary questions.

The book ends with a section on evolutionary psychology and human sexual behavior that I consider a mistake. Roughgarden takes on subjects as wide ranging as secondary sexual characters, gender multiplicity, homosexuality, human attractiveness, the human brain, and rape without adequately introducing them and incorporating them into her main theme. It seems almost as though the author didn't have the time or space to deal with these issues but felt they needed to be mentioned. I left this section thinking that the author was as guilty of assuming that cooperation explains everything as are proponents of sexual selection when they assume that competition explains everything.

What is the bottom line? Even though I disagree with the author on some points, and though in some cases Roughgarden does her ideas a disservice by discounting well-documented observations of sexual conflict, I applaud her for shaking things up. I believe she is correct in some of her criticisms, and we should remember that competition in sexual interactions is an assumption that should be tested, rather than a factual starting point. We all need to be more careful in our thinking.