The dominant evolutionary theory for Earth's most successful creatures, and a proposed influence on human altruism, is under attack.

For decades, selflessness – as exhibited in eusocial insect colonies where workers sacrifice themselves for the greater good – has been explained in terms of genetic relatedness. Called kin selection, it was a neat solution to the conundrum of selflessness in what was supposedly an every-animal-for-itself evolutionary battle.

One early proponent was now-legendary Harvard biologist E.O. Wilson, a founder of modern sociobiology. Now Wilson is leading the counterattack.

"For the past four decades kin selection theory … has been the major theoretical attempt to explain the evolution of eusociality," writes Wilson and Harvard theoretical biologists Martin Nowak and Corina Tarnita in an Aug. 25 *Nature *paper. "Here we show the limitations of its approach."

According to the standard metric of reproductive fitness, insects that altruistically contribute to their community's welfare but don't themselves reproduce score a zero. They shouldn't exist, except as aberrations – but they're common, and their colonies are fabulously successful. Just 2 percent of insects are eusocial, but they account for two-thirds of all insect biomass.

Kin selection made sense of this by targeting evolution at shared genes, and portraying individuals and groups as mere vessels for those genes. Before long, kin selection was a cornerstone of evolutionary biology. It was invoked to help explain social and cooperative behavior across the animal kingdom, even in humans.

But according to Wilson, Nowak and Tarnita, the great limitation of kin selection is that it simply doesn't fit the data.

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At first, eusociality was seen only in insect species whose reproductive biology makes fertilized eggs grow into females, and unfertilized eggs into males. As a result, sisters share more genes with each other than their offspring. Through a kin selection lens, eusociality makes sense in these species: Sisters are driven to work for each other, not their less-related offspring.

But then eusociality was found in other insect species – termites and aphids – along with snapping shrimp and naked mole rats, in which siblings were no more related to each other than to their offspring. The correlation between high genetic relatedness – "inclusive fitness," in the kin selection argot – and eusociality no longer held.

The new study isn't the first to point these flaws out, but it exhaustively models the mathematics of the gap.

"Inclusive fitness theory is almost like a shortcut. It only applies to a small subset of all possible models," said Tarnita. "Outside of that subset, it doesn't work."

The researchers offer their own alternative theory, based on standard natural selection, but with a twist: After starting with a focus on a single founder, selection moves to the level of colony. From this perspective, a worker ant is something like a cell – part of a larger evolutionary unit, not a unit unto itself.

"Our model proves that looking at a worker ant and asking why it is altruistic is the wrong level of analysis," said Tarnita. "The important unit is the colony."

The researchers propose a theoretical narrative that begins with a primordial, solitary ant – perhaps something like the ancient Martialis heureka – that lived near a food source and developed genetic mutations that caused it to feed its offspring, rather than letting them fend for themselves. Called progressive provisioning, such nurture is widespread in insects.

Another mutation could result in offspring that stayed near the nest, rather than leaving. They would "instinctively recognize that certain things need to be done, and do them," said Nowak, describing real-world examples. "Put two normally solitary wasps together, and if one builds a hole, the other puts an egg in it. The other sees the egg, and feeds it."

That would be enough to form a small but real colony – and from there, eusociality could emerge from an accumulation of mutations that led to a hyper-specialization of tasks, limited reproduction to queens alone and favored the colony's success above all else. Within this colony, a queen would be analogous to a human egg or sperm cell – a unit that embodies the whole. Worker self-sacrifice is no more nonsensical than that of a white blood cell.

The researchers called this series of steps a "labyrinth," one that isn't easily navigated. Hence the rareness of eusociality, which is believed to have arisen just 10 to 20 times in history. But their theory explains everything that kin selection does, plus what it doesn't.

"There is no need whatsoever to invoke kin selection or inclusive fitness," said Corina – not in eusociality, not in any cooperative behavior.

The study provoked varying reactions among evolutionary biologists. An article in Cosmos quoted Oxford University's Stuart West describing the paper as "obviously incorrect," and Rice University's David Queller saying the new model "involves, and I suspect requires, close kinship."

Other researchers were more supportive. University of British Columbia mathematical zoologist Michael Doebeli said the new theory is better than kin selection at explaining eusociality, and stressed that kin selection is just an idea. "It's not a biological mechanism, it's an accounting technique," and one that misses a lot, he said.

According to David Sloan Wilson, an evolutionary biologist at Binghamton University, the paper is a culmination of research that "knocks kin selection theory off its perch" – something that should have happened long ago. "Kin selection theory has become so general that it's used to explain anything that evolves by social behavior," ignoring evolution's complexity, he said. "To the average animal researcher studying social behavior, it seems the only thing they need to know is relatedness. That's not unhelpful, but it's not the only factor."

Especially troubling to David Sloan Wilson is how kin selection, with its intuitive appeal to our preference for family over strangers, has been applied to human social life. "The idea that everything nice about human behavior is based on interactions among genetic relatives during the Stone Age, and is now being incorrectly expressed, is pathetic as an explanatory framework," he said.

Tarnita said the new theory of eusociality may be useful in describing how single-celled organisms gave rise to multicellular organisms. Human selflessness and cooperation, however, is of a different sort, also involving the interaction of culture and sentience, not just genetics and environment.

"There are certain things we can learn from ants, but I wouldn't try to draw a parallel," said Tarnita. "It's easier to think about ants, but people are complicated."

Update: The lede originally read, "and a proposed explanation for human altruism." I've since changed to, "a proposed influence." Thanks to commenters for pointing out the oversimplification.

Images: 1) Steve Jurvetson/Flickr. 2) Progressive provisioning in a solitary Synagris cornuta wasp, and a colony of the primitive eusocial wasp Polistes crinitus./Science.

See Also:

Citation: "The evolution of eusociality." By Martin A. Nowak, Corina E. Tarnita & Edward O. Wilson. Nature, Vol. 466, No. 7310, August 26, 2010.

Brandon Keim's Twitter stream and reportorial outtakes; Wired Science on Twitter. Brandon is currently working on a book about ecological tipping points.