Inclusive fitness works

I can't believe the amount of attention the paper by Martin Nowak, Corina Tarnita and Edward O. Wilson Nowak:eusociality:2010 has gotten. It was in last week's Nature. The basic idea was that the evolution of eusociality in insects could be explained in a different way that the usual explanation, which involves calculating the relatedness of worker insects to their reproductive siblings. Eusociality has been one of the most visible applications of inclusive fitness theory -- that is, the observation that the fitness of a gene that alters behavior may be calculated in terms of its effects on the reproduction and survival of relatives. The paper notes that some aspects of eusociality are not well explained in terms of relatedness, and derives an alternative explanation.

The weird part of the paper is the way it describes inclusive fitness as some kind of theoretical afterthought, useful only as an ad hoc explanation for eusocial insects. It contrasts the inclusive fitness concept with "standard natural selection" as if it were possible for organisms to erase the fact that they're related to each other! And the authors imply that they have fatally damaged the concept of kin selection.

It's so contrary to evolutionary theory, that I thought maybe I was missing something. But I've been spending time on another problem this week and haven't had time to follow it up.

Fortunately, Jerry Coyne and Richard Dawkins have both given the paper some attention, and written notes and reactions to it. First Coyne ("A misguided attack on kin selection") reminds us of why kin selection has been such a successful part of "standard" evolutionary theory for the past fifty years.

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 altruismsuicidal 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 mothers genetic welfare and that of her offspring?

Im 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 its not: its simply a natural extension of population genetics to the situation in which ones behavior affects related individuals.

Richard Dawkins has also posted notes about the paper:

Kin selection is not a subset of group selection, it is a logical consequence of gene selection. And gene selection is (everything that Nowak et al ought to mean by) 'standard natural selection' theory: has been ever since the neo-Darwinian synthesis of the 1930s. Inclusive fitness theory is not some kind of supernumerary excrescence, to be 'resorted to' only if 'standard natural selection theory' is found wanting (Misunderstanding One). On the contrary, inclusive fitness theory is one way of expressing what was logically inherent in the synthesis ever since Fisher and Haldane, but had been largely overlooked because people (with the exception of those two geniuses) didn't think about collateral kin.

Yes, unless they're going to repeal the Price equation, they'll have to rely on relatedness to explain those phenotypes that never occur in reproductive individuals. As Dawkins puts it, "You have to talk about shared genes in individuals, with conditional phenotypic expression."