Does inclusive fitness theory miss part of the picture?

I originally titled this post “The Less Wrong wiki is wrong about group selection”, because it seemed wildly overconfident about its assertion that group selection is nonsense. The wiki entry on “group selection” currently reads:

People who are unfamiliar with evolutionary theory sometimes propose that a feature of the organism is there for the good of the group—for example, that human religion is an adaptation to make human groups more cohesive, since religious groups outfight nonreligious groups.

Postulating group selection is guaranteed to make professional evolutionary biologists roll up their eyes and sigh.

However, it appears that the real problem is not that the wiki is overconfident (that’s a problem, but it’s only a symptom of the next problem) but that the traditional dogma on the viability of group selection is wrong, or at least overconfident. I make this assertion after stumbling across a paper by Martin Nowak, Corina Tarnita, and E. O. Wilson titled “The evolution of eusociality”, which appeared in Nature in August of this year. I found a PDF of this paper through Google scholar, click here. A blog entry discussing the paper can be found here (bias alert: it is written by a postdoc working in Martin Nowak’s Evolutionary Dynamics program at Harvard).

Here’s some quotes (bolding is mine):

It has further turned out that selection forces exist in groups that diminish the advantage of close collateral kinship. They include the favouring of raised genetic variability by colony-level selection in the ants Pogonomyrmex occidentalisand Acromyrmex echinatior—due, at least in the latter, to disease resistance. The contribution of genetic diversity to disease resistance at the colony level has moreover been established definitively in honeybees. Countervailing forces also include variability in predisposition to worker sub-castes in Pogonomyrmex badius, which may sharpen division of labour and improve colony fitness—although that hypothesis is yet to be tested. Further, an increase in stability of nest temperature with genetic diversity has been found within nests of honeybees and Formica ants. Other selection forces working against the binding role of close pedigree kinship are the disruptive impact of nepotism within colonies, and the overall negative effects associated with inbreeding. Most of these countervailing forces act through group selection or, for eusocial insects in particular, through between-colony selection.

Yet, considering its position for four decades as the dominant paradigm in the theoretical study of eusociality, the production of inclusive fitness theory must be considered meagre. During the same period, in contrast, empirical research on eusocial organisms has flourished, revealing the rich details of caste, communication, colony life cycles, and other phenomena at both the individual- and colony-selection levels. In some cases social behaviour has been causally linked through all the levels of biological organization from molecule to ecosystem. Almost none of this progress has been stimulated or advanced by inclusive fitness theory, which has evolved into an abstract enterprise largely on its own

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The question arises: if we have a theory that works for all cases (standard natural selection theory) and a theory that works only for a small subset of cases (inclusive fitness theory), and if for this subset the two theories lead to identical conditions, then why not stay with the general theory? The question is pressing, because inclusive fitness theory is provably correct only for a small (non-generic) subset of evolutionary models, but the intuition it provides is mistakenly embraced as generally correct.

Check out the paper for more details. Also look at the Supplementary Information if you have access to it. They perform an evolutionary game theoretic analysis, which I am still reading.

Apparently this theory is not that new. In this 2007 paper by David Sloan Wilson and E. O. Wilson, they argue (I’m just pasting the abstract):

The current foundation of sociobiology is based upon the rejection of group selection in the 1960s and the acceptance thereafter of alternative theories to explain the evolution of cooperative and altruistic behaviors. These events need to be reconsidered in the light of subsequent research. Group selection has become both theoretically plausible and empirically well supported. Moreover, the so-called alternative theories include the logic of multilevel selection within their own frameworks. We review the history and conceptual basis of sociobiology to show why a new consensus regarding group selection is needed and how multilevel selection theory can provide a more solid foundation for sociobiology in the future.

From the other camp, this seems to be a fairly highly-cited paper from 2008. They concluded:

(a) the arguments about group selection are only continued by a limited number of theoreticians, on the basis of simpliﬁed models that can be difﬁcult to apply to real organisms (see Error 3); (b) theoretical models which make testable predictions tend to be made with kin selection theory (Tables 1 and 2); (c) empirical biologists interested in social evolution measure the kin selection coefﬁcient of relatedness rather than the corresponding group selection parameters (Queller & Goodnight, 1989). It is best to think of group selection as a potentially useful, albeit informal, way of conceptualizing some issues, rather than a general evolutionary approach in its own right.

I know (as of yet) very little biology, so I leave the conclusion for readers to discuss. Does anyone have detailed knowledge of the issues here?