Category: Uncategorized

Evolution’s Rainbow, from sparrows’ stripes to lizard lesbianism

Evolution’s Rainbow, from sparrows’ stripes to lizard lesbianism

Evolutionary biology is not just the study of how living things change over time, but the study of how the diversity of living things changes over time. Diversity is the raw material sculpted by natural selection, carved into more-or-less discrete chunks by speciation, and lost forever in extinction.

Joan Roughgarden is even more preoccupied with diversity than most evolutionary biologists. Some of her earliest published studies examine the evolution of optimum niche width, the range of resources a species uses, using mathematical modeling [$a] and empirical studies of resource and habitat use in Anolis lizards [$a]. Roughgarden didn’t treat a species as a uniform group, but a collection of individuals all making a living in slightly different ways. Among other subjects, her work informed thinking about ecological release, the changes that reshape populations freed from predators or competitors.

White-throated sparrows are just one species with more than two gender roles.


This interest in the evolutionary context of diversity would eventually become much more personal. In 1998, she came out as transgendered, taking the name Joan after decades spent establishing her scientific reputation under the name she was given at birth, Jonathan. In addition to the challenges inherent to gender transition, Roughgarden’s expertise intersects with her identity in one awkward question: in a biological world shaped by natural selection, how can we explain the evolution of lesbians, gay men, and transgendered people—individuals who are not interested in sexual activity that passes on their genes?

Roughgarden’s answer was to begin a program of research questioning the dominant way of thinking about sex in an evolutionary context. In 2004, she presented her conclusions comprehensively in the book Evolution’s Rainbow, calling for biologists to re-think they way they understood and described sexual behavior throughout the animal kingdom. As another biologist with an admitted personal interest in the question, I’ve found Evolution’s Rainbow to be a great starting point for thinking about sexuality in an evolutionary context.

Human sexuality as one stripe in nature’s rainbow

Cover image from Google Books.Evolution’s Rainbow takes aim at the idea that most sexual species are divided into neat, binary reproductive roles, in which males aggressively court females who judge them to find the healthiest mate—a model with little room for same-sex attractions, or more than two gender roles. Darwin conceived of this sexual selection to explain traits and behaviors that did not improve an individual’s odds of survival—or, indeed, could even reduce them—but that were, he suggested, involved in demonstrating a male’s health and virility.

However, Darwin’s very Victorian thinking doesn’t have much place for same-sex sexuality, or gender roles outside the male-female binary. Roughgarden argued that sexuality in the animal kingdom is much more varied than the aggressive males-choosy females binary. She holds that this diversity of behavior is better explained by a new model, which she terms social selection. The first several chapters of the book are dominated by the first of these points, and Roughgarden rounds up a tremendous array of sexual behaviors. To highlight just three that particularly struck me:

White-throated sparrows (pictured above) have evolved social roles separate from their sexual roles. Male and female white-throated sparrows may have one of two plumage morphs, each associated with different levels of aggressiveness—sparrows with bright white facial stripes sing and respond to other sparrows’ songs to defend a nesting territory; birds with duller, “tan” stripes sing less frequently and are less territorial. Mated pairs of sparrows are most successful when they’re mixed, but it doesn’t matter whether the male or the female in a pair is the aggressive one. Mated pairings between tan-striped males and white-striped females have just as many chicks [$a] as pairings between white-striped males and tan-striped females. Roughgarden proposes that, like the sparrows’ stripes, many traits biologists have understood to be signals for sexual roles are actually signaling social roles that need not be strictly associated with males or females.

Are smaller bluegill males “sneakers,” or helpers? Photo by IcK9s.To take another example, male bluegill sunfish may follow one of two developmental pathways, with differing reproductive strategies. Some male bluegills—large males—do not reproduce until they grow big enough to defend a nesting territory; females lay eggs in territories defended by males they favor. Other male bluegills begin their reproductive lives at a much smaller size, by fertilizing unattended eggs in the large males’ territories whenever they get the chance. As they grow larger, though, these now-medium-sized males change strategies—they join in the large males’ courtship of females, and fertilize some of the eggs laid in the large males’ territory. Medium males’ coloration resembles that of female bluegills, and their strategy has been described as deceptive, mimicking females to “cuckold” large males [PDF]. Roughgarden favors another explanation: that medium males are collaborating with large males [$a], helping to attract females in return for a chance to reproduce.

Finally, in several species of whiptail lizards, females have evolved that don’t need males to reproduce—their eggs are fertile without sperm. Yet these parthenogenetic females copulate with each other, and this same-sex activity helps to stimulate egg-laying. Parthenogenetic females form longer-term associations and share burrows [$a], which is much less common in related, sexually-reproducing species. Roughgarden suggests that for parthenogenetic whiptails, sex has an important role in social interaction even though its reproductive function is diminished.

Females of some whiptail lizard species don’t need a male to reproduce—but copulating with another female helps. (Pictured: a male little striped whiptail, who may be feeling a mite left out.) Photo by jerryoldenettel.This survey of the animal kingdom showcases instances where sexual selection doesn’t seem to fit very well. It also provides a broader evolutionary context for human sexual minorities. The point is not to show that same-sex sexual activity is “natural”—Roughgarden explicitly and scrupulously avoids the “naturalistic fallacy”—but to seek the evolutionary roots of human sexuality. Just as we can learn about the history of human cognition from the problem-solving skills of our closest evolutionary relatives, chimpanzees and bonobos, the fact that bonobo social interactions are structured by sexual relationships between females tells us something about the history of human sexuality.

Social, not sexual, selection?

Roughgarden argues that the diversity of sexual behavior in nature cannot be explained by sexual selection as Darwin originally conceived it. Instead, she proposes that sexual behavior is shaped by social selection, in which individuals cultivate social relationships to obtain resources or reproductive opportunities. She has since developed the verbal model presented in Evolution’s Rainbow as formal game theory models, showing how individuals might cooperate to raise offspring [PDF], including in coalitions more complicated than male-female pairs. Under Roughgarden’s view, sexual interactions, including homosexual ones, can be part of the social interaction that binds together such coalitions.

Roughgarden’s ideas are still under considerable debate. The 2006 game theory paper mentioned in the previous paragraph attracted no fewer than 10 written responses objecting to its rejection of sexual selection theory with varying degrees of vehemence. Tim Clutton-Brock explicitly responded to Roughgarden in a 2007 review arguing that sexual selection remains a useful framework [PDF] for describing most animal mating systems. In his review of Evolution’s Rainbow for the journal Evolution, Douglas Futuyma praised the book’s survey of diversity in animal mating systems. However, Futuyma cautioned against throwing out the idea of sexual selection altogether, quoting Hamlet’s exhortation to his mother: “O throw away the worser part of it/ And live the purer with the other half.”

The debate is outside my immediate expertise, but I would not be surprised if we eventually come to understand sexual selection and social selection as related models with differing degrees of specificity. In forming scientific theories, there is an inherent tension between the goal of explaining as wide a range of observations as possible, and doing so with the simplest possible model. Sexual selection is a simple model that may explain the majority of animal mating systems. Social selection, on the other hand, is potentially much more complicated, proposing a different reproductive game for every animal species—but this also means that a social selection model can be found to fit mating behaviors that cannot be explained by sexual selection.

However the debate over explanatory models is resolved, Roughgarden’s work to broaden the evolutionary perspective on sex has been truly important. Evolutionary biology aims to explain the entire scope of the living world. Evolution’s Rainbow reminds us how endless, and how beautiful, the forms of life truly are.

Joan Roughgarden has since written a second book, The Genial Gene, which elaborates key themes from Evolution’s Rainbow, such as the idea that cooperation may be a better model for the evolution of social interactions than competition and selfishness. For more background on Roughgarden and her work, see the New York Times profile and this piece by Jonah Lehrer for SEED Magazine, as well as Roughgarden’s lab website, all linked in the text above.


Clutton-Brock, T. (2007). Sexual selection in males and females. Science, 318 (5858), 1882-5 DOI: 10.1126/science.1133311

Crews D., Grassman M., & Lindzey J. (1986). Behavioral facilitation of reproduction in sexual and unisexual whiptail lizards. Proc. Nat. Acad. Sci. USA, 83 (24), 9547-50 PMID: 3467325

Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex. John Murray, London. Google Books.

Dominey, W. (1981). Maintenance of female mimicry as a reproductive strategy in bluegill sunfish (Lepomis macrochirus). Environmental Biology of Fishes, 6 (1), 59-64 DOI: 10.1007/BF00001800

Futuyma, D. (2005). Celebrating diversity in sexuality and gender. Evolution, 59 (5), 1156-9 DOI: 10.1554/BR05-4

Kopachena, J., & Falls, J. (1993). Aggressive performance as a behavioral correlate of plumage polymorphism in the white-throated sparrow (Zonotrichia albicollis). Behaviour, 124 (3), 249-66 DOI: 10.1163/156853993X00605

Leuck, B. (1982). Comparative burrow use and activity patterns of parthenogenetic and bisexual whiptail lizards (Cnemidophorus: Teiidae). Copeia, 1982 (2), 416-24 DOI: 10.2307/1444623

Roughgarden, J. (1972). Evolution of niche width. The American Naturalist, 106 (952), 683-718 DOI: 10.1086/282807

Roughgarden, J. (2004). Evolution’s Rainbow. University of California Press, Berkeley. Google Books.

Roughgarden, J., Oishi, M., & Akçay, E. (2006). Reproductive social behavior: Cooperative games to replace sexual selection. Science, 311 (5763), 965-9 DOI: 10.1126/science.1110105

Rummel, J., & Roughgarden, J. (1985). Effects of reduced perch-height separation on competition between two Anolis lizards. Ecology, 66 (2), 430-44 DOI: 10.2307/1940392

New cooperation theory has major Mommy issues

New cooperation theory has major Mommy issues

The cover article for last week’s issue of Nature promised to be the last word in a long-running scientific argument over the evolution of cooperation—but it really just rejiggers the terms of the debate. Instead of solving the problem of how cooperative behavior can evolve, the new paper presents a model of maternal enslavement [$a]. These are not, it turns out, quite the same thing.

Group selection versus kin selection

Let’s start with some background. Unselfish, cooperative behavior has long been a puzzle in evolutionary biology, because natural selection should never favor individuals who make significant sacrifices for the benefit of others. Sure, an unselfish individual might expect those she helps to reciprocate later; but a population of the unselfish would be easily overrun by those who don’t reciprocate.

There have historically been two answers to the problem of the selfish out-competing the unselfish. The first case is basically an extension of logic we all learned in kindergarten: cooperative groups can do things that uncooperative groups can’t. Like, for instance, start a neighborhood garden.

Under this model, neighborhoods of cooperative, garden-making people are nicer places to live, and their inhabitants can collectively out-compete other neighborhoods that can’t get it together to start a community garden. In evolutionary terms, this is group selection—even if individuals sacrifice to build the garden, the group as a whole benefits. Unfortunately, this breaks down if the new garden attracts selfish people to move to the neighborhood, buy up all the cheap real estate, and open Urban Outfitters franchises.

There’s another possibility, though. What if unselfish behavior isn’t always truly unselfish? For instance, if you help your relatives, you’re actually helping some of your own genes. You share half your genes with your siblings, a quarter of your genes with half-siblings, an eighth of your genes with first cousins, and so on. This means that Michael Bluth might be on to something.

Evolutionarily speaking, it doesn’t matter if Michael spends all his time helping his feckless family, as long those efforts help someone in the family (G.O.B., most likely) reproduce and perpetuate some of the genes that Michael shares with him or her. This idea was advanced by W.D. Hamilton in two 1964 papers, one mathematical [PDF], and one more focused on real-world examples [PDF]; we now know it as kin selection. It doesn’t hold up so well for maintaining the kind of complex society humans have today, where we interact with lots of completely unrelated people—but it might have got the ball rolling toward the wheel, war, New York and so forth by selecting for cooperative behaviors within small tribes back at the dawn of history.

The group selection versus kin selection debate has gone back and forth for decades, and the new paper is a shot across the bow of kin selection. The authors, Martin Nowak, Corina Tarnita, and E.O. Wilson, aim to do two things: first, prove that kin selection is wrong; and second, describe an alternative explanation. For the first, they argue that kin selection only applies in narrow circumstances, that those circumstances never show up in nature, and that empirical studies just don’t support the model. Johnny Humphreys makes some reasonable objections to these arguments, and so do several folks interviewed by Carl Zimmer, and I’ll refer you there rather than try to improve on them.* I’m more interested in the second part: the alternative explanation.

Enslaved by Mom
No individual fitness for you—you’re cogs in the Superorganism. Photo by jby.Nowak et al. propose to explain the evolution of unselfishness as it applies to eusociality—organisms like ants or bees or naked mole rats, in which colonies of (closely related) individuals defer most or all of their opportunities to reproduce, in order to support one or a few individuals that reproduce a lot. As Johnny points out in his critique, it’s not clear that eusociality is the same thing as unselfishness at all, even though it’s historically cited as an example of unselfishness [$a]. The new model that Nowak et al. develop actually makes the difference between eusociality and unselfishness even clearer. Under their model, it’s not that worker ants give up reproductive opportunities to help their mother, the Queen, reproduce—it’s that the Queen takes away their reproductive opportunities.

The key insight of the new model is that, in evolving from a non-social insect to a eusocial one, the natural selection that matters affects not the individuals evolving into workers, but the individual who would be Queen. Consider an insect similar to the probable ancestor of ants: females build nests, provision them with food, and lay eggs inside. Nowak et al. propose that a female who evolved the ability to lay “worker” eggs—females that grow up not to found their own nest, but to help in their mother’s—would have greater fitness than females without such helpful offspring.

Aside from the probability of evolving “worker” eggs (which is not a small issue, I think), this shift in perspective from the fitness of the worker to the fitness of the Queen makes all sorts of sense to me. I’ve often wondered why myrmecologists don’t treat ant colonies as single organisms, rather than collections of cooperating individuals.

But this approach also seems to sidestep the key question biologists hope to answer with kin selection and group selection models—these models aim to explain how individuals can come together to cooperate, but Nowak et al. have built a model that looks more like enslavement. I can’t learn anything about how unselfish behavior can spontaneously evolve in a population by looking at a population that has had unselfishness imposed upon it. To indulge in one last especially geeky pop culture reference, it’d be like trying to learn about market economics by studying The Borg.

Nowak, Tarnita, and Wilson might have come up with a very good model for the evolution of eusociality; but if so, it means that eusociality is a bad model for the evolution of cooperation as we usually conceive it.

* I will, however, note that Nowak et al. do something I’ve never seen in a scholarly paper before—in dismissing empirical studies of kin selection, they defer substantive discussion to the Supplementary Information. There are, in fact, 43 pages of SI for this 6-page paper, including two major mathematical models and the discussion of empirical kin selection studies. This is a problem, but one that is beyond the scope of this already-long post.


Axelrod, R., & Hamilton, W. (1981). The evolution of cooperation. Science, 211 (4489), 1390-1396 DOI: 10.1126/science.7466396

Hamilton, W.D. (1964). The genetical evolution of social behaviour. I. Journal of Theoretical Biology, 7 (1), 1-16 DOI: 10.1016/0022-5193(64)90038-4

Hamilton, W.D. (1964). The genetical evolution of social behaviour. II. Journal of Theoretical Biology, 7 (1), 17-52 DOI: 10.1016/0022-5193(64)90039-6

Nowak, M., Tarnita, C., & Wilson, E. (2010). The evolution of eusociality. Nature, 466 (7310), 1057-62 DOI: 10.1038/nature09205