Inclusive Fitness: Return to the Wrestling Ring

By Carl Zimmer | March 23, 2011 3:31 pm

Last summer I wrote in the New York Times about a controversy over one of the most influential concepts in the recent history of evolutionary biology. Known as inclusive fitness, it basically says that helping relatives can be a good way to pass on your genes, because they’ve got your genes too.

In August, Nature published a lengthy paper by Martin Nowak, E.O. Wilson, and Corina E. Tarnita in which they argued that inclusive fitness was mathematically flawed and basically superfluous. I had no trouble finding other scientists who were ready to say all sorts of scathing things about Nowak et al. I’m no fan of ginning up fake debates, but when somebody says, “This paper, far from showing shortcomings in inclusive fitness theory, shows the shortcomings of the authors,” the story writes itself.

Seven months later, Nature has finally published some “Brief Communication Arising” letters from some of these critics. The first letter alone has 137 co-signers.

Their ranks include plenty of major players in the field of evolution (including John Alcock, Tim Clutton-Brock, Stephen Emlen, Paul Sherman, Mary-Jane West Eberhard, and Richard Wrangham). The tenor of the letters is more dignified than the comments I got for my story, but the message is unchanged:

We believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature.

The authors of the first letter argue that Nowak et al don’t get inclusive fitness. They claim it needs lots of stringent assumptions, when, in fact, it’s a general theory. They also challenge the idea that inclusive fitness doesn’t provide any more insights into biology. They offer a list of such insights, such as why animals cooperate with each other, why they can act spitefully, and why mothers produce different ratios of males and females. Inclusive fitness has proven particularly useful for addressing last question–what’s known as sex allocation. It explains how the ratio of males to females changes with the density of females, the mortality rate, and many other factors–and it does so for species as varied as mammals, birds, spiders, and plants.

Nowak et al respond to all the criticism and don’t budge in their own stand. They claim that their critics have misinterpreted their own argument. And they claim that sex allocation does not require inclusive fitness. Oddly, though, they never explain why it doesn’t, despite the thousands of papers that have been published on inclusive fitness and sex allocation. They don’t even cite a paper that explains why. They conclude by writing,

Inclusive fitness theory is neither useful nor necessary to explain the evolution of eusociality or other phenomena. It is time for the field of social evolution to move beyond the limitations of inclusive fitness theory.

[Image from Alex Wild]

Comments (21)

  1. I got my popcorn in hand and just sitting back, enjoying the show. Although it is a feisty debate, it doesn’t seem like both sides have the evidence (unlike, say the homo floresiensis controversy or the North American Pleistocene extinction controversy).

  2. RossM

    Science isn’t about democracy – it needs evidence. This debate, one hopes, will result in better thinking about the existing evidence and someone conceiving an experiment to demonstrate that one view is more likely. The last thing we need is two groups saying “is” “isn’t” “is” “isn’t”. I do think that Nowak et al need to addrss all the arguments raised.

  3. Benjamin Hardisty

    I felt that this whole flap is over emphasis on different factors in the Price equation. I also get the impression that both sides are just trying to trump up their publications lists in Nature. The fact is, relatedness has to count for something in promoting the evolution of altruism, but just how much it accounts for in various scenarios is debatable. This whole acrimonious debate is pointless I think. To say that kin selection is never an explanation is quite silly, but to say that it’s the only explanation for the evolution of altruism, reciprocal altruism, parceling etc, is also quite silly. Regardless, I think the kin selection and sex allocation literature is vast, and rather convincing.

  4. This is what I call a “methodology war”. These are common in science and usually mask political differences (i.e., scientific politics). They occur in a science usually when progress has stalled on crucial research questions.

    Wilson has previously argued in favour of group selection by claiming that kin selection is a form of group selection, so the group selectionists won (his 2007 paper with David Sloan Wilson in QRB). The obvious response is that kin selection is an outcome of (purely individual level selection) inclusive fitness, and people did respond that way. So denying that inclusive fitness even exists blocks that objection.

    What facts tell for or against this? Basically if the math works, then one can claim inclusive fitness is explanatory, but there can be no experimentum crucis that will show that the working math is true. So wiggle room persists and hence: methodology war.

  5. Christopher Kandrat

    That was a great debate. But some things are questionable

  6. marcel

    Carl: Can you sort out your pronouns? The passage below, especially, is unclear.

    “The authors of the first letter argue that Nowak et al don’t get inclusive fitness. They claim it needs lots of stringent assumptions, when, in fact, it’s a general theory. They also challenge the idea that inclusive fitness doesn’t provide any more insights into biology. They offer a list of such insights, such as why animals cooperate with each other, why they can act spitefully, and why mothers produce different ratios of males and females. ”

    Most of the occurrences of “they” appear to refer to “The authors of the 1st letter”. But the 2nd sentence makes more sense if the “they” at the start refers to Nowak et al., and that casts doubt, in my mind, on the referents of the other occurrences of “they”.

  7. Daniel

    Thanks, Marcel, for pointing that out. So it wasn’t just me. I struggled with that, too.

  8. One problem is that inclusive fitness has often been promoted as the exclusive underpinning of altruism, etc, in humans. Direct linkages between genes and higher-order behavior are highly suspect in complex organisms and humans, in particular, are heavily subject to cultural pressures.

  9. Sven DiMilo

    “inclusive fitness has often been promoted as the exclusive underpinning of altruism, etc, in humans”

    Often? By whom, exactly? What is meant by ‘etc.’? Are fishes, birds, and mammals “complex organisms”? Do you know what you’re talking about?

  10. Monkey

    I think “etc” should be on the list of no-no words, Carl! I second Sven (#12) on that one.

    As a current language teacher in Taiwan, I am always floored when I get – from fluent adults – sentences like “I love you, etc” or ” I will order the chicken and tofu, etc”. It leaves way…way….to much to the imagination and doesnt add to the content. I also think that this leads into proper english contexts, such as science communication. “X drug caused A, B, C, etc”. What the heck does that actually mean?

    Just some thoughts…Im not poking at your use (or non-use, thankfully) of it, just the comments above brought it up in my mind.

  11. “, etc.” translates roughly as “I heard something about this from my best friend’s boyfriend’s sister who is a biology major. We were talking about it at this party, and I remember it because I thought it was weird that she said altruism is genetic. I mean, how can feelings be genetic? After all, not everything is genetic–some things are culturally determined!”

    With nary a word about where culture came from– poofed into existence by faeries, maybe. Or Tomte.

  12. johnk

    I’m not sure who has said that “inclusive fitness” has been applied to higher organisms, but who, among the coiners of the term, has said it doesn’t apply? When scientists borrow terms like “altruism” and “cooperation” and apply formal definitions without much qualification, the implication is that the ‘scientific’ and correct usage of the terms apply universally.

    I’m with Athena. I think the implied boundaries are, at best, vague. And I’m not at all sure that the altruism shown by bees and ants is driven by similar or analogous mechanisms to the altruism that is (occasionally) shown by humans.

    My guess is that human altruism and cooperation are driven by “values” that derive from genetic, cultural and cognitive roots. But the boundaries are not well explored.

  13. Nathan Taylor

    David Sloan Wilson has always struck me as the single person who has paid his dues and understands both the science and the science history of group selection. He did a whole series of blog posts on putting the group selection controversies behind us. And his books are extremely clear and well written, in particular Unto Others. The whole controversy just saddens me as it has once again set back the science for a shouting match. David Sloan Wilson’s blog post on this is well worth reading. One caveat is he does not hide his disdain for Dawkin’s role in this:–.php

  14. johnk

    Exposing my ignorance:

    Do evolutionary biologists believe that evolution of all traits (including the genetic basis of social behavior) is due to natural selection? Or, is evolution through other forms of selection possible?

    Example 1. Are domesticated animals, such as sheep and dogs, entirely the product of natural selection?

    Example 2. If it’s argued that domestication through selective breeding is not natural selection, then it seems that the intelligent agent for domestication (the human mind) can as easily affect the genetic basis of social behavior in our own species. As a species, we have the capacity to select behavioral traits that have values other than survival.

  15. jon osborn

    Some people use “nature” to mean everything, or the most fundamental basis of everything. Others use it to mean “unconscious” or “unintentianal”. If we use it to mean basic fundamental, then breeding, “artificial” selection is a sub-category of natural selection. Just like sexual selection is a sub-category of natural selection. As for culture, it is commonly held that genetics forms the basis for the ability to form/maintain/develop culture, as in humans primates song birds/crows whales. To say that our cultural acheivments are NOT evolutionarily based, or not genetic, is both wrong and correct: We didnt have quantum mechanics or jazz-funk in the ancestral environment, but we did appreciation for music and abstract explanations of the varied phenomena. This basic appreciation combined with time and memory yeilds our current culture.


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The Loom

A blog about life, past and future. Written by DISCOVER contributing editor and columnist Carl Zimmer.

About Carl Zimmer

Carl Zimmer writes about science regularly for The New York Times and magazines such as DISCOVER, which also hosts his blog, The LoomHe is the author of 12 books, the most recent of which is Science Ink: Tattoos of the Science Obsessed.


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