August 30, 2010

E.O. Wilson v. W.D. Hamilton: Round II, 45 Years Later

From the NYT:
Scientists Square Off on Evolutionary Value of Helping Relatives

Why are worker ants sterile? Why do birds sometimes help their parents raise more chicks, instead of having chicks of their own? Why do bacteria explode with toxins to kill rival colonies? In 1964, the British biologist William Hamilton published a landmark paper to answer these kinds of questions. Sometimes, he argued, helping your relatives can spread your genes faster than having children of your own.

For the past 46 years, biologists have used Dr. Hamilton’s theory to make sense of how animal societies evolve. They’ve even applied it to the evolution of our own species. But in the latest issue of the journal Nature, a team of prominent evolutionary biologists at Harvard try to demolish the theory.

The scientists argue that studies on animals since Dr. Hamilton’s day have failed to support it. The scientists write that a close look at the underlying math reveals that Dr. Hamilton’s theory is superfluous. “It’s precisely like an ancient epicycle in the solar system,” said Martin Nowak, a co-author of the paper with Edward O. Wilson and Corina Tarnita. “The world is much simpler without it.”

Other biologists are sharply divided about the paper. Some praise it for challenging a concept that has outlived its usefulness. But others dismiss it as fundamentally wrong.

“Things are just bouncing around right now like a box full of Ping-Pong balls,” said James Hunt, a biologist at North Carolina State University.

Dr. Hamilton, who died in 2000, saw his theory as following logically from what biologists already knew about natural selection. Some individuals have more offspring than others, thanks to the particular versions of genes they carry. But Dr. Hamilton argued that in order to judge the reproductive success of an individual, scientists had to look at the genes it shared with its relatives.

We inherit half of our genetic material from each parent, which means that siblings have, on average, 50 percent [1/2] of the same versions of genes. We share a lower percentage with first cousins [1/8], second cousins [1/32] and so on. If we give enough help to relatives so they can survive and have children, then they can pass on more copies of our own genes. Dr. Hamilton called this new way of tallying reproductive success inclusive fitness.

Each organism faces a trade-off between putting effort into raising its own offspring or helping its relatives. If the benefits of helping a relative outweigh the costs, Dr. Hamilton argued, altruism can evolve.

The idea wasn't exactly wholly new. J.B.S. Haldane liked to joke in the 1950s when he was asked if he'd give up his life for his brother: No, but maybe for 2 brothers or 8 first cousins.
Dr. Hamilton believed that one of the things his theory could explain was the presence of sterile females among ants, wasps, and some other social insects. These species have peculiar genetics that cause females to be more closely related to their sisters than to their brothers, or even to their own offspring. In these situations, a female ant may be able to spread more genes by helping to raise her queen mother’s eggs than trying to lay eggs of her own.

Wilson didn't like Hamilton's theory the first time he heard of it either. In his delightful autobiography Naturalist, Wilson described how he wrestled with Hamilton's epochal papers during an 18-hour train ride in 1965:

"Impossible, I thought, this can't be right. Too simple… By dinnertime, as the train rumbled on into Virginia, I was growing frustrated and angry… And because I modestly thought of myself as the world authority on social insects, I also thought it unlikely that anyone else could explain their origin, certainly not in one clean stroke… By the time we reached Miami, in the early afternoon, I gave up. I was a convert and put myself in Hamilton's hands. I had undergone what historians of science call a paradigm shift."

Zimmer continues:
But as the years passed, Dr. Wilson’s enthusiasm for the theory waned. “It was getting tattered,” he said. Many species with sterile females, for example, do not have the strange genetics of ants and wasps. And many species with the right genetics have not produced sterile females. ...

A number of scientists strongly disagree, though. “This paper, far from showing shortcomings in inclusive fitness theory, shows the shortcomings of the authors,” said Frances Ratnieks of the University of Sussex.

Dr. Ratnieks argues that the Harvard researchers cannot rule out kinship as a driving force in social evolution because their model is flawed. It does not include how closely related animals are.

That would seem to be a big factor. 

Read the rest of the article here

To see some of the more interesting implications of Hamilton's theory, see my 2004 article.



Anonymous said...

This is the "Group Selection" debate that David Sloan Wilson has written a lot about. Personally, I see no reason why Group Selection is reviled so much. The whole point is that network effects can make traits that are hurt in one-on-one interactions beneficial for whole groups. An altruist might lose to a selfish person, but a group of altruists will likely co-exist better than a group of selfish-people, all without any selfish-genes to explain it all.

AmericanGoy said...

"An altruist might lose to a selfish person, but a group of altruists will likely co-exist better than a group of selfish-people, all without any selfish-genes to explain it all."

Don't tell this to the nutty libertarians.

Efficient market theory with a purely selfish individual is the founding block of free market (tm) capitalism don'cha know?

Brent Lane said...

Always like to see EO Wilson mentioned in your stuff, Steve.

Naturalist is one of my favorite autobiographies, for two reasons: the chapter on Wilson's undergraduate career at the University of Alabama-Tuscaloosa (or UA-T as we Auburn grads like to call it) is the most damning indictment of the outrageous inflation in postwar higher education. In his trademark meticulous way, Wilson kept records of every single expenditure on the way to his BS in Biological Science, even including his travel to and from his then-home in Mobile. Grand total for his degree? Somewhere in the neighborhood of $2000. For EVERYTHING. That won't even pay tuition and fees for a single semester nowadays (not to mention the decline in the value of the education itself in the last six decades).

The other is a more personal note: I was delighted to read in Wilson's boyhood accounts of his life in my current hometown of Pensacola that he lived a scant two blocks from where I am now sitting - and in his recollections he recounts how he spent many hours poking around nearby construction sites, one of which was almost certainly my house, which was built during the time he lived here.

Unfortunately I've managed to miss meeting him on his frequent visits to the area - hopefully he'll get back down this way again soon.

Anonymous said...

Steve, either the paper is loco (in a way not evident from reading the abstract), or Zimmer's article is.

Evolution of eusociality is an extremely difficult subject. I'll leave it to Martin Nowak, who I know is a lot smarter than me. Of course it is quite true that many eusocial species do not have the strange haplo-diploid genetic system of ants - and there is no doubt that this does weaken the case for eusociality being a result of Hamilton's rule.

In contrast, why bacteria autolyse to help 'siblings' 99.9% genetically identical to themselves is /extremely simple/. It is virtually 100% certain to be caused by the Haldane-Hamilton phenomena. The way some birds help their parents raise young, when no territory is easily available and they are too young to skillfully contend for it, is also very simple.

Just ask Cochran, he'll tell you the same. Or if he doesn't, kindly forget I said anything.

gcochran said...

E. O Wilson isn't much of an analyst. As far as I can tell, he never was. He's a natural public intellectual.

Obviously eusociality doesn't require the haplodiploid genetic system seen in the hymenoptera, since there are termites, mole-rats, etc that don't work that way. Hamilton thought haplodiploidy might help, by increasing the relatedness coefficient, but he appears to have been mistaken. The relatedness coefficient matters, though: it looks as if the ancestral form of a eusocial species is always monogamous. That means that the relatedness coefficient is 1/2: good enough, evidently. See Hughes, WOH et al, Ancestral monogamy shows kin selection is key to the evolution of eusociality, Science, 320, 1213-1216, 2008

Some eusocial species are non-monogamous, but this seems to happen only when the worker castes are sterile and thus can't
opt out by producing their own more-closely-related offspring anymore.

Kin selection theory has lots and lots of successful predictions. It's in good shape.

dearieme said...

“Things are just bouncing around right now like a box full of Ping-Pong balls,”: but if the box is full, the balls don't bounce around. There oughta be a law against stupid similes.

Chuck said...

"This is the "Group Selection" debate that David Sloan Wilson has written a lot about. Personally, I see no reason why Group Selection is reviled so much."

Two reasons:
1.With humans, groups selection means biocultural evolution. Which means genetic population differences due to culture differences and cultural adaptations modified around genetic differences in the sense of 'norms of reaction.' That is, it's related both to Multilevel selection theory and to gene-culture coevolution.

So, some cultural differences are genetic and some cultural ways are more adapted to certain genotypes; and cultures of the past -- of which there were recent significant differences -- shaped population genetics.

What don't you get about the being reviled? Go read: 'Guns,Germs,and Steel.' And factor in gene-culture co-evolution for the past 10-thousand years and you get a variant of 'The 10,000 Year Explosion: How Civilization Accelerated Human Evolution.'

2. Group selection implies that groups act as a unit of selection. Think Kmac. So, populations represent a meta-organism.

Overall, It's really a toss up as to which is more political incorrect. We have the gene-centered Hamilton world, in which individuals try to maximize their inclusive fitness which leads to kin selection or, alternatively, we have the group centered Sloan world, in which individual evolve collectively and so individual fitness is maximized by group fitness.

Anonymous said...

>"Things are just bouncing around right now like a box full of Ping-Pong balls," said James Hunt, a biologist at North Carolina State University.>

I'd rather watch Ping-Pong balls than read that paper. Funniest ever video: a mall cam captured a kid prankster "accidentally" dropping a box of dozens of golf balls from the top of the escalator. They went absolutely everywhere; the chaos was gorgeous.

>Not all workers ants are sterile.<

Not all humans are sterile. But are the sterile humans particularly adapted to helpfulness? Plenty of homosexuals aren't sterile, and a number of them contribute to society, though it's not clear whether they are a net plus or net drain.

Just throwing out some puzzlers.

Dutch Boy said...

The old-time panhandlers had the right line: "Brother, can you spare a dime?"

TGGP said...

I think Dawkins already discussed termites in "The Selfish Gene". They aren't haplodiploid, but they have not only stable monogamy but repeated generations of incest. That results in a high relatedness coefficient. Don't remember what he said about mole-rats.

MQ said...

Samuel Bowles and his coauthors demonstrated that reasonable estimates of levels of violence among pre-historic hunter gatherers could have triggered group selection in humans.

Group selection makes tremendous intuitive sense when you look at human social and ethical instincts, which are very finely honed to punish cheaters.

FF said...

" Plenty of homosexuals aren't sterile, and a number of them contribute to society, though it's not clear whether they are a net plus or net drain."

Fa'afafine in traditional Samoan society have been valued as helpful in the family unit...with a chosen son undertaking the position of mother's domestic helper.
This role seems to be especially common in larger families with more boys than girls.

TGGP said...

John Hawks is underwhelmed.

Anonymous said...

Many here have missed the terms of this controversy. EO Wilson & co's change of mind was forced by 1999 work by James Hunt who studied multiple origins of sociality in a wasp phylogeny in which all the species had about the same “kin selection potential” and found that sociality evolved when there were strong “ecological” incentives (Hunt JH 1999. Trait mapping and salience in the evolution of eusocial vespid wasps. Evolution 53: 225-237). But since ~2005 Wilson, Hoelldobler, etc, have hijacked the controversy.
People have indeed started realizing that crucial for the existence/persistence –and thus for the evolution– of animal societies is not (or not so much) “kin selection” but rather the very rewarding ecological niches out there in which biomachines that adopt group-approaches to foraging and interference competition are much more effective trophically than are biomachines which adopt “solitary-consumer/fighter/reproducer” strategies.
This means that the evolutionary success of the genetic programs encoding such group behaviors is fully subordinate to the existence of such ecological opportunities!
In other words: people have begun realizing that, e.g., “altruism” is also a winning ecological strategy, rather than just an example of the promotion, or not, of altruism genes and the rejection (or invasion) of cheater genes.
The social-ant colony, e.g., is an ecological machine that out-competes at the foraging- and interference-competition level most other organisms in almost any terrestrial ecological setting, i.e., a social-ant colony in the field cannot be reduced natural-historically and evolutionary-historically to just an example of an ESS immune to “selfishness” mutations that may undermine the genetic encoding of its sociality.
Wilson indeed has always made a big deal of the fact that ant species monopolize nearly 70% of the insect biomass on earth, but he did not realize the implications of this until the wasp guy rubbed it to him and his coterie while they were still happily repeating the empty syllogisms of kin-selection numerologists [who meanwhile have even almost managed to deny Darwin (sic!) the credit for explaining the existence of sterile ants, etc., when he mentioned in the Origin Species that an individual's sacrifice can benefit the reproduction of relatives, i.e., kin selection].
This 70% means that evolution by “natural selection of individuals” delivers niche-occupancy strategies that suffice to claim only ~30 of the trophic energy monopolized by the insect Bauplan (assuming termites and other social insects are insignificant biomass-wise).
The situation among many mammals is the same. Wild-dog packs and hyenas, e.g., beat the hell out of tigers and lions, and biomass wise they dominate.
It is time for gratuitous faux-a-prioristic arguments to be confronted with ultimate natural-historical facts. And it is also time that the applied-math peddlers posturing as evolutionary biologists learn that “natural selection” is not the same as “evolution by natural selection”, that differential fitness is always caused by differential ecological performance (and never by “genes”), and that evolution by natural selection is just something that “may” happen when there is differential ecological performance at some level of biological organization, which however does not “prove” that ecological performance is caused by molecular interactions of genes (or of proteins; genes may suffice but are not necessary for differential performance, but additive genetic variation in performance suffices for evolution driven by differential ecological performance).
In other words, Sober’s 1984 [1984 sic!] book “The Nature of Selection” should be required reading for every evolutionary biologist. Sober showed first that the “kin selection” oxymoron is a muddled verbal construct to refer to that special case of group-level differential ecological performance in which “selected” groups happen to also be kin groups (most of the time but not always... see mutualism, e.g.).