I don’t know what’s gotten into E. O. Wilson. He’s certainly the world’s most famous evolutionary biologist, and has gone from strength to strength over the years, winning two Pulitzer Prizes, writing great general books on not only ants but conservation and social behavior. And he’s kept his hands in the ant work, producing any number of technical papers and monographs. He’s even written a novel! Frankly, I don’t know how he does it. I haven’t always agreed with what he says—I think he overreached with the sociobiology stuff, for instance—but you have to admire the guy’s knowledge, breadth, dedication to conservation, and sheer workaholism.
But now Wilson, along with some collaborators like David Sloan Wilson and Martin Nowak, is definitely heading off on the wrong track. They’re attacking kin selection, maintaining not only that it has nothing to do with the evolution of social insects, but that’s it’s also a bad way to look at evolution in general. And they’re wrong—dead wrong.
Their latest attack on kin selection is a big paper in the new Nature by Wilson, Martin Nowak and Corina Tarnita, all from Harvard. They begin by arguing that the classical argument for insect eusociality (cooperatively breeding societies in which “castes” of individuals, like the workers in bees, are sterile and help the queen produce offspring)—an argument based on asymmetrical relatedness—is wrong. This failure to explain eusociality, they claim, is a severe blow to kin-selection theory.
They’re right about the biology. The “textbook” explanation, based on a higher relatedness of workers to their sisters than to their own potential offspring, no longer seems feasible. It posits that queens mate only once, but in reality they often mate many times, which destroys the asymmetry of relatedness that supposedly selects for cooperative breeding. Further, other species, like aphids, termites and mole rats, are eusocial but don’t show asymmetrical relatedness. Finally, lots of haplodiploid species (those in which males come from unfertilized eggs, females from fertilized ones) have asymmetrical relatedness but aren’t eusocial.
But we’ve known all this for years! Check out the papers by Gardner & West and Strassmann & Queller cited below—they point out the same problems that Nowak et al. present as novel, but as far back as 1998. There’s nothing new here.
The main problem with the Nowak et al. paper is this: they see the failure of asymmetrical relatedness to explain social insects as a general failure of kin selection to help us explain those groups—or anything at all. That’s just wrong. There are alternative explanations for how relatedness explains the evolution of social insects (see the two papers by Strassman and Queller), including the phenomenon of sterile castes. And, although Nowak et al. claim that “the production of inclusive fitness theory must be considered meagre,” there are many aspects of eusociality that have been profitably investigated, and explained, by inclusive fitness theory. Here are just a few: why worker bees commit suicide when they sting; why, when a honeybee colony divides, the remaining queen goes around stinging to death all the other future queens in their cells; why workers prefer to raise rear queens in colonies where their mothers have mated only once, but rear males in colonies where their mothers have mated multiply; and why workers in singly-mated colonies kill male larvae. And there are many others.
Sex ratio theory, in which mothers produce different proportions of males and females, has been a particularly fruitful area for applying inclusive fitness theory. So has “altruism”—suicidal honeybees are just one example. And so are parental care and aspects thereof, especially parent-offspring conflict, a field brought to life by Bob Trivers using inclusive fitness theory. How else can you explain weaning conflict except by a conflict between the mother’s genetic welfare and that of her offspring?
I’m baffled not only by Nowak et al.’s apparent and willful ignorance of the literature, but by statements that are just wrong. They flatly assert, for instance, that “inclusive fitness theory” is something different from “standard natural selection theory.” But it’s not: it’s simply a natural extension of population genetics to the situation in which one’s behavior affects related individuals. I could go on, but a little bird has told me that the big guns in the field will, soon and en masse, answer Nowak et al.’s arguments about both theory and data.
I can’t fathom any motive, either psychological or scientific, for Wilson and Company to repeatedly denigrate the importance of inclusive-fitness theory. It’s just a shame that, this late in his career, Wilson has chosen to fight the wrong battle. In the meantime, contrast his attacks on the value of kin selection with the summary paragraphs of Strassman and Queller (2007), who, after reviewing the bearing of inclusive-fitness theory on understanding social insects, conclude:
Any scientific theory purporting to account for biological complexity ought to account for this special nature of social insects. Why do their colonies show a degree of apparent purpose lacking in other aggregations, herds, and flocks? The kin selection extension of natural selection theory does explain this; cooperation results from the opportunity to give sufficiently large benefits to kin.
More importantly, kin selection theory has successfully predicted new findings. Although social insect colonies have clocklike design in many respects, kin selection theory predicts who is throwing sand into the clockworks, as well as which gears might be slipped and which springs sprung. Many of the predicted findings, such as sex ratio conflict and policing, were otherwise completely unexpected. The success of this approach shows that the Darwinian paradigm is capable of explaining not just the adaptations of organisms but also how new kinds of organismal entities come into being.
Finally, a big raspberry to the folks at Nature who decided to publish such a strange paper in the interest of stirring up controversy. If they’d gotten decent reviewers, and followed their advice, it never would have seen print.
UPDATE: Over at his website, Richard Dawkins has added his own notes on the Nowak et al. paper. He doesn’t like it either, and for many of the same reasons.
Nowak, M. A., C. E. Tarnita and E. O. Wilson. 2010. The evolution of eusociality. Nature 466: 1057-1062.
Queller, D. C., and J. E. Strassmann. 1998. Kin selection and social insects. Bioscience 48:165-175.
Strassmann, J. E., and D. C. Queller. 2007. Insect societies as divided organisms: The complexities of purpose and cross-purpose. Proc. Nat. Acad. Sci. USA 104:8619-8626.
West, S. A. and A. Gardner. 2010. Altruism, spite, and greenbeards. Science 327:1341-1344.