Kin selection dead?

I had blogged about E.O. Wilson's change of mind about group selection recently, in which it was hinted that he no longer thought that Hamilton's kin selection was a major evolutionary force. Now, a new paper has been published in Nature by Nowak, Tarnita, and Wilson which formalizes the argument.

An accompanying story in Nature gives a high-level overview of the paper:

Kin selection is based on 'inclusive fitness', the idea that, for example, sterile workers can accrue reproductive benefits by helping their relatives. In doing so, they help shared genes to survive and get passed on to the next generation. This provides a route for eusociality to evolve.

But Martin Nowak, a mathematical biologist at Harvard University in Cambridge, Massachusetts, and the lead author of the analysis, says, "there is no need for inclusive fitness to explain eusociality".

Nowak and his team provide the first mathematical analysis of inclusive fitness theory. They calculated which of two behaviours, for example defection — such as going off to set up a separate colony — or cooperation would become more prevalent in a population if standard natural selection was at work. They then worked out what assumptions would be needed for inclusive fitness theory to deliver the same result.

The team discovered that inclusive fitness delivers the same result only in a limited set of specific situations that would rarely hold in reality. For example, inclusive fitness worked only if the two behaviours were very similar — so that the pressure to select one over the other is vanishingly small — and if just two individuals were interacting at one time.

And when the inclusive fitness theory worked, the answer that it provided was mathematically equivalent to that derived from standard natural selection.

"We show that inclusive fitness is not a general theory of evolution as its proponents had claimed," says Nowak. "In the limited domain where inclusive fitness theory does work, it is identical to standard natural selection. Hence there is no need for inclusive fitness. It has no explanatory power."

In a second mathematical analysis, the team investigated how eusociality could evolve through standard natural selection. They found that a gene for eusociality could spread readily as long as the advantages it confers — increasing the lifespan and reproductive success of the queen — kick in even for small colonies. So colonies that have as few as two or three workers must provide significant advantages to their queen for the gene and the behaviour to become widespread.

"Whether or not eusociality evolves depends on how colony size affects the mortality and fecundity of the queen," says Nowak. "Our model also shows that eusociality is hard to evolve but is very stable once it is established."

Going against four decades of theory is no joke, so I will have to think about the significance of this new paper.

UPDATE (Aug 26):

From the press release:

Eusociality is rare, but important in evolutionary biology because the few species that adhere to it -- including social insects and, to an extent, humans -- rank among the planet's most dominant. The biomass of ants alone composes more than half that of all insects, exceeding that of all terrestrial nonhuman vertebrates combined. Humans, who are more loosely eusocial, dominate land vertebrates. Eusociality has arisen independently some 10 to 20 times in the course of evolution," says Tarnita, a junior fellow in Harvard's Society of Fellows. "Our model shows that it is difficult to get eusociality in the first place, but that it is very stable once it is established. A colony behaves like a 'superorganism,' reproducing the genome of the queen and the sperm she has stored."

Nowak, Tarnita, and Wilson's proposal on eusocial evolution sketches out three distinct steps species can take to sidestep eusociality's evolutionary cost:

• First, species must form groups within a population, such as when nests or food attract individuals to discrete locations some distance apart, when parents and offspring remain together, or when migrating flocks follow leaders.

• Second, species must accumulate traits, arising through ordinary natural selection, that favor the switch to eusociality. For instance, Ceratina and Lasioglossum bees, which appear perched on the cusp of eusociality, cooperate in foraging, tunneling, and guarding resources. Another such pre-adaptation is progressive provisioning, in which a female builds a nest, lays an egg in it, and then feeds or guards larvae until they mature. Most importantly, the candidate species must build a defensible nest.

• Finally, individuals must develop genes supporting eusociality, whether by mutation or recombination. Crossing the threshold to eusociality essentially requires that a female and her offspring not disperse to start new, individual nests, but rather remain at the old nest. While eusocial genes have yet to be identified, at least two eusocial ant species are known to have genes that quell the urge to roam from the nest.

If these steps are followed and a species becomes eusocial, the evolutionary costs of individuals foregoing reproduction are compensated by the greatly reduced mortality of the queen and her larvae, which are protected by the colony. In some ant species, a queen that might live for only a few months if alone can live for 25 years or more as part of a colony, producing millions of offspring in the process.

Nature 466, 1057-1062 (26 August 2010) | doi:10.1038/nature09205; Received 10 March 2010; Accepted 26 May 2010

The evolution of eusociality

Martin A. Nowak, Corina E. Tarnita & Edward O. Wilson

Abstract

Eusociality, in which some individuals reduce their own lifetime reproductive potential to raise the offspring of others, underlies the most advanced forms of social organization and the ecologically dominant role of social insects and humans. For the past four decades kin selection theory, based on the concept of inclusive fitness, has been the major theoretical attempt to explain the evolution of eusociality. Here we show the limitations of this approach. We argue that standard natural selection theory in the context of precise models of population structure represents a simpler and superior approach, allows the evaluation of multiple competing hypotheses, and provides an exact framework for interpreting empirical observations.

Link