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The living rainbow: A fatal flaw in a classic study of sexual selection

The living rainbow: A fatal flaw in a classic study of sexual selection

06 Drosophila melanogater Mating

A key component of classical sexual selection theory is the idea that males maximize their evolutionary fitness—the number of children they ultimately have—by mating with lots of females, while females maximize their fitness by selecting only one or a few high-quality partners. It’s pretty clear that this model works well for some species (like ducks), but also that there are many it doesn’t fit so well. Now it looks like one of the “classic” experimental examples of sexual selection may actually fall into the latter category.

Sexual selection was first proposed by Charles Darwin, in his 1871 follow-up to The Origin of Species, The Descent of Man, and Selection in Relation to Sex; but one of the earliest experimental tests of the model wasn’t published until 1948 [PDF]. The biologist A.J. Bateman allowed small groups of fruit flies—good old Drosophila melanogaster—containing equal numbers of males and females to mate at random, then reared the resulting eggs and reconstructed the parentage of the offspring to determine (1) the number of offspring each of the male and female parent flies had produced and (2) how many parters each parent fly had had.

How did Bateman reconstruct parentage decades before the advent of modern genetic testing? He used mutations with known, visible phenotypic effects as “markers”:

The fertility of individual flies of both sexes was measured by means of dominant marker genes. Several flies of each sex were mated together in one bottle, each fly carrying a different dominant marker gene. In this way, assuming the complete viability of all the marker genes, half the progeny of each fly could be identified.

That’s a pretty clever design given the technological limitations of the time. But it also turns out to be the fatal flaw in Bateman’s experiment.

Using this approach, Bateman reconstructed parentage for his offspring flies, and found that the reproductive success of males varied more than that of females; and that males were more likely than females to finish the experiment without producing any offspring—both suggestive of stronger competition for mates among the males.

Examining the number of mates for each of the parent flies, Bateman found that the number of mates also varied more in males than in females. In fact, his data showed that males with more mates tended to have more offspring—while for females, having a larger number of partners didn’t do much to improve offpsring production.

The results Bateman described are the epitome of the sexual selection model, with males competing to inseminate as many females as possible, while females instead try to select only one or a few very fit males to father their children. But those results hang on the assumption that Bateman’s marker mutations didn’t create any bias in his parentage reconstructions—and some of the marker mutations were pretty wild: gene variants that distorted the flies’ wings or eyes, many of which were lethal when a fly carried two copies.

Drosophila melanogater Bar One of Bateman’s marker mutations, “Bar,” results in dramatically distorted eyes. Photo via FlyIU.
In a paper that’s just been released online at PNAS, Patricia Gowaty, Yong-Kyu Kim, and Wyatt W. Anderson present the results of the first attempt to replicate Bateman’s experiment since he first performed it in 1948. To the best of their ability, they collected the same laboratory lines of Drosophila, with the same marker mutations, and conducted the same controlled matings.

Gowaty and her collaborators replicated Bateman’s discovery that different parental marker mutations were represented in the offspring with varying frequency—but they also discovered some substantial biases in the results. One of the most glaring was that, using Bateman’s approach to reconstruct parentage, they found that mothers were less often identifiable as parents than fathers were—which, as they note, is “a biological impossibility.”

Gowaty et al. also found that the fraction offspring carrying two mutant marker genes substantially deviated from 25%, which is the frequency expected if the marker genes truly have no impact on mating success and offspring survival.

In short, Bateman’s key assumption, “the complete viability of all the marker genes,” proved to be incorrect, and incorrect in a way that seems to have systematically biased his results so that his data can’t actually tell us anything about whether or not his fruit flies were experiencing sexual selection. Fortunately, we have methods available to us nowadays that Bateman didn’t, and I’m sure we can look forward to a new test of his hypothesis using DNA fingerprinting and behavioral observations of mating frequency in the near future.◼

Thanks to Daniel Decanini for pointing me to the Gowaty et al. paper on Twitter.


Bateman AJ (1948). Intra-sexual selection in Drosophila. Heredity, 2 (Pt. 3), 349-68 PMID: 18103134

Gowaty, P.A., Kim, Y.-K., & Anderson, W.W. (2012). No evidence of sexual selection in a repetition of Bateman’s classic study of Drosophila melanogaster. Proc. Nat. Acad. Sci. USA. : 10.1073/pnas.1207851109

Evolutionary psychology: A dialogue

Evolutionary psychology: A dialogue

A Biologist went down to the coffee shop one day, because the walk out to the edge of the University campus provided some brief respite from the laboratory. Along the way the Biologist encountered an Evolutionary Psychologist, who was also going to the coffee shop, and they fell to walking together.

As they entered the coffee shop, they found it crowded with undergraduates, for it was almost Finals Week. Accordingly, they joined the long queue of prospective customers waiting to place an order. Said the Evolutionary Psychologist to the Biologist, “My dear colleague, do you not see this crowd of fertile young people as I do, engaged in a dance of mate selection and competiton that predates our ancestors’ descent from the trees?”

And the Biologist replied, “I don’t believe that our ancestors had access to steamed milk and espresso. Or free wi-fi.”

“You are being amusingly obtuse!” chortled the Evolutionary Psychologist. “The environment may have changed somewhat since the days of our Darwinian origins, I will allow, but ova remain much dearer than sperm cells.”

“That much is certainly true,” said the Biologist. “But I am not sure how much it matters to the coffee-shop flirtations of undergraduates, almost none of which will result in procreative intercourse.”

“Ah,” said the Evolutionary Psychologist, “Perhaps this is a subject wherein my own field has surpassed the expertise of yours, my dear colleague. For instance, we have recently discovered [PDF] that men are more attracted to unintelligent, inattentive women—precisely what one would expect if men have been naturally selected to seek out easy opportunities for impregnation. And this search is doubtless underway all around us at this very moment.”

“That is a remarkable and possibly misogynistic hypothesis,” said the Biologist. “I am most curious to know how it was tested.”

“O! It was most elegantly done,” said the Evolutionary Psychologist. “Some of my colleagues simply asked a small class of undergraduate psychology students—males, of course—to examine photographs of women which were previously selected for their various appearances of vulnerability, and tell whether the photographs indicated vulnerability to sexual exploitation, suitability for a one-night stand, and suitability for a long-term relationship.”

“I see,” said the Biologist.

“Most surprisingly,” continued the Evolutionary Psychologist, “My colleagues discovered that the young collegiate males felt that women who looked drunk, or were standing in compromising postures, or indicating vulnerability in any of a dozen different ways, were both more vulnerable to sexual assault and more suitable for a brief sexual dalliance—but not more suitable for matrimony.

“So you see, my dear Biologist, it is not we Evolutionary Psychologists, who proposed the hypothesis of sexual exploitability, that are misogynists—the only misogynist here is Natural Selection itself, which confirmed our hypothesis.”

“I must beg your pardon, dear colleague,” said the Biologist, “but I am afraid I do not understand the basis for your conclusion. In order for this discovery to have any bearing on reproductive success, is it not the case that most human reproduction would need to occur via coerced intercourse?”

“I must confess that this seems to be what the data indicate,” replied the Evolutionary Psychologist. “But we must not conclude therefrom that all men are rapists! By no means, dear colleague. I think it is quite plain that this result demonstrates no more then that all men are potential rapists.”

“But I remain perplexed!” said the Biologist. “Surely rape is an inefficient way to reproduce, since babies traditionally require a good deal of care after impregnation, and women have long known how to un-plant unwanted seeds.”

“That,” said the Evolutionary Psychologist, “is an important question to be resolved by additional study! But of course it need only be the case that the occasional coercive impregnation could increase a man’s reproductive success, however slightly, for Natural Selection to grab hold.”

“I suspect,” said the Biologist, “that you attribute greater efficiency to Natural Selection than this evolutionary force truly possesses, my dear colleague. But even if drunken collegiate hook-ups were a viable avenue for procreation, you must concede that there would needs be some genetic basis for the tendency to reproduce in this fashion, if Natural Selection is to act upon it. Do you truly believe this to be the case?”

“What a peculiar question!” exclaimed the Evolutionary Psychologist. “I thought that you Biologists were well aware that, in the absence of evidence to the contrary, it is quite safe to assume that any and all aspects of human nature have a heritable genetic basis. Would you truly require the demonstration of heritability in order to conclude that an observed trait or behavior is adapted by Natural Selection?”

“Indeed we would,” said the Biologist. “Such a demonstration, in the case of a tendency to sexual coercion, would be considered most remarkable in its own right, in the scholarly journals of my discipline.”

“What a boring and backward discipline you practice!” said the Evolutionary Psychologist. “Truly, it is no wonder that your field has seen no great advance this last half-century, even as we Evolutionary Psychologists dissect the very nature of humanity.”

“Your ambitions,” said the Biologist, “are indeed remarkable.”

At this juncture, the two colleagues found that they had reached the front of the queue, placed their orders, and went their separate ways.◼


Goetz, C., Easton, J., Lewis, D., & Buss, D. (2012). Sexual exploitability: Observable cues and their link to sexual attraction. Evolution and Human Behavior DOI: 10.1016/j.evolhumbehav.2011.12.004

Science online, socially un-contagious edition

Science online, socially un-contagious edition

You probably won’t catch bad eating habits at that cocktail party. As long as you go easy on the canapés. Photo by rocketlass.

Big blogging news this week: Bora Zivkovic and the team at Scientific American have launched a big new network of science blogs, sweeping up a large chunk of my RSS subscriptions, including Kate Clancy, Eric Michael Johnson, Christie Wilcox, Krystal D’Costa, Kevin Zelnio, Jason Goldman, and SciCurious. And just like that, SciAm is the center of the science blogosphere. Congrats to everyone involved!

  • When the press release precedes peer review, check your wallet. A whole series of studies proposing that behaviors from divorce to overeating are “contagious” via social ties may be bunk.
  • Hoisted on their own statistical petard. A study of dinosaur morphology data using statistical methods invented by Creationists ends up confirming descent with modification.
  • Solution: either more funding, or fewer deaths. US Federal funding for research into solutions to infection by drug-resistant Staphylococcuscomes to less than $600 per MRSA death.
  • Darwin was polite even in pencil. Robert Krulwich examines Charles Darwin’s marginalia.
  • They’re elephants with wings! Why you should never piss off a crow.
Diversity in Science Carnival: Pride Month 2011

Diversity in Science Carnival: Pride Month 2011

Even though the queer nerd is a long-established phenomenon, and a pretty common one these days, we’re not necessarily very visible in science, technology, engineering, or mathematics disciplines. Even cutting-edge fields can be surprisingly conservative, and a lot of us end up in industries or academic departments where people are still not asking or telling. And on the other hand, science often has a lower profile within the queer community than it deserves—how many queer scientist types have you seen on TV lately? Yeah, me neither.

(Maybe Willow Rosenberg? But she ditched computer science for magic, and she’s been off the air since 2003!)

As just one example of this, when Alberto Roca and I went looking for science-related videos on the “It Gets Better” project website, where queer adults can post their stories to encourage queer kids who are dealing with bullying, neither of us found much. Big tech companies like Microsoft, Pixar, Bayer, and Eli Lilly are well represented, but search for individuals’ videos labeled “science” and you get … not a lot.

So where are the examples of queer scientists for today’s nerdy gay, lesbian, bi, and trans kids to look toward?

Well, actually, we’re all over the place. For last October’s National Coming Out Day, Steve Silberman and Maggie Koerth-Baker put together a wonderful double feature at BoingBoing, compiling the personal stories of LGBT scientists, and presenting an in-depth interview with endocrinologist Neena Schwartz. Now, for the Pride edition of the Diversity in Science blog carnival, we have another array of voices from across the science blogosphere: queer and allied scientists and science fans, discussing everything from gay history to the science of sexuality to their personal experiences as sexual minorities in scientific workplaces.

The carnival commences after the jump!

Our stories

We’re nerds, so I think we tend to be fairly accepting of variance.
—A respondent to Rick MacPherson’s survey of LGBT folks in ocean science

To kick things off, here’s one notable exception to the lack of science-y personal “It Gets Better” vidoes, and it’s a queer nerdy delight: Borja’s even wearing my favorite xkcd shirt.

Carnival contributor AstroDyke also suggests the IGBP video by Apple employees.

David Kroll highlights an in-depth report on LGBT folks in the chemical sciences, many of whom don’t feel safe to be out at work—as well as recent findings from the Center for Work-Life Policy that making a workplace LGBT-friendly benefits employers as well as employees. Rick MacPherson reports the results of his survey of LGBT folks in the oceanic sciences, covering broad trends and individual responses. Marcelo Vinces—who started a blog just to contribute to this carnival—says that early neurological and genetic studies of same-sex attraction helped him come out.

It gets better in the sciences for a lot of us, but it also gets complicated. EcoPhysioMichelle finds she must “write her own history” as a bisexual and a scientist. Gerty-z explains how coming out at work doesn’t happen just once—it happens over and over again.

For your enjoyment, here is a representative conversation:
person: So, what does your husband do?
me: there is no husband. But, my wife is a [redacted]
person: …
person: OH. *looks awkward*

Sarcozona wonders where the other queer ecologists are, and suggests we should, er, recruit:

I think science should be doing more to recruit young queer students. So many queer students major in gender studies or queer theory because those subjects help us understand ourselves better, validate our experiences, and focus on making the world a better place. But science can do that, too!

Finally, Alberto Roca of Minority Postdoc covers (with coauthor David G. Taylor) the first career summit organized by the National Organization of Gay and Lesbian Scientists and Technical Professionals—an event that both recognized how far we’ve come and how far we have to go.

Our history

Gay history is intertwined with the history of science, sometimes quite closely. Romeo Vitelli recounts the story of Alan Turing, who helped defeat Nazi Germany with groundbreaking innovations in machine calculation, only to find himself sentenced to hormonal “castration” for being gay.

Sculpture of Alan Turing by Stephen Kettle, at Bletchley Park National Codes Centre, UK. Photo by Leo Reynolds.
Several of Turing’s colleagues from his Bletchley Park days also supported him. His mentor, Max Newman, and fellow cryptanalyst Hugh Alexander acted as character witnesses during his trial. This was a courageous stand for them considering the “guilt by association” mentality that often tarred anyone who supported convicted sex criminals. Many of Turing’s friends, homosexuals themselves, felt obliged to distance themselves out of fear that they would be suspected as well.

Astrodyke wonders when groundbreaking gay rights activist Frank Kameny will be recognized by his fellow astronomers. And last but not least, in a post with strong contemporary relevance, David Kroll discusses the sometimes uneasy relationship between the Civil Rights movement and the later gay rights movement.

Our science

One of the major challenges of dealing with sexual minorities in a scientific context is that human sexuality means very different things in different cultural contexts. Eric Michael Johnson describes how a 5,000-year-old, possibly-male skeleton buried laying on its left side turned into a “gay caveman” in the retelling—even though he certainly wasn’t a caveman, and probably wasn’t gay.

By all accounts it seems that the UK Telegraph had the dubious honor of being first in this case, and in so doing committed two wrongs in just as many words: “Gay Caveman.” First off, a person living during the Chalcolithic (a period previously referred to as the “Bronze Age”) was not a caveman. This highly inaccurate term is usually used for Neandertals or Cro-Magnon humans, both of whom lived about 35,000 years ago.

In an incisive piece for the magazine Orion this March, Alex Johnson proposed queering ecology to better understand on humans’ relationship with nature. Earlier this year, I discussed the diversity of sexuality Joan Roughgarden found across the animal kingdom, and last week I delved into how natural selection might—or might not—act on human same-sex sexuality. Meanwhile Luke Swenson, a doctoral candidate in virology at the University of British Columbia, has been steadily producing great posts about the latest HIV research at his blog Going Viral since it launched back in February.

And that’s it for the Pride 2011 Diversity in Science carnival. Look for new editions of DiS in the near future!

Thanks to the contributors who sent in all these great posts, and many, many thanks to Alberto Roca at Minority Postdoc, who chose to relaunch Diversity in Science with this Pride Month carnival, and relentlessly rounded up a host, contributors, and a long list of cool resources to include in the Carnival.

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