Inclusive fitness applies to genes too

Recently Martin Nowak - in one of his attacks on the concept of inclusive fitness claimed that:

On the level of genes there is no inclusive fitness

I think this is a fairly straightforwardly mistaken idea. The basic logic of Hamilton's 1964 paper applies to genes too. Hamilton claimed that organisms are not just be driven by self interest, and concern for their offspring, but can be expected be interested in the welfare of their other relatives too (brothers, cousins, parents, etc). Similarly, genes aren't just out for themselves. They also act as though they are concerned about their relatives.

With genes the situation is simpler to analyze. To a first approximation, most other genes are related to them by either being identical clones - or by being completely unrelated. These situations correspond to r=1 and r=0 - in the standard inclusive fitness mathematical formalism. If you plug these numbers into Hamilton's rule, you get sensible results. Genes often act as though they do care about the welfare of identical copies of themselves.

The inclusive fitness of a gene can be calculated in the same way as the inclusive fitness of an organism - by adding and subtracting fitness components due to self and relatives - as described by Hamilton.

West, Gardner and I are all in agreement on this issue. In 2013, they said:

Even at the level of the gene, we would still want to know what the maximand is, and the answer is ‘the inclusive fitness of the gene’

So: what was Martin Nowak thinking about? Perhaps he meant to write that inclusive fitness was not a necessary concept at the level of the gene. For example, if you think of genes as being informational, then it is conventional to refer to all the copies of a particular physical nucleotide sequence as representing the same "gene" (or "allele", as some people prefer to say). In which case, talk of "inclusive fitness" is unnecessary.

However, the concept of inclusive fitness is applicable on the level of the genes. I think to claim otherwise is just to invite confusion and misunderstanding.

Why the kin vs group selection arguments persist

There have been a few attempts to explain the persistence of the clash between kin selection and group selection enthusiasts, beyond the recognition of the broad equivalence of the approaches.

D. S. Wilson wrote Clash of Paradigms: Why Proponents of Multilevel Selection Theory and Inclusive Fitness Theory Sometimes (But Not Always) Misunderstand Each Other.

Recently Herbert Gintis has offered his perspective in a review of the book Evolutionary Restraints: The Contentious History of Group Selection.

It seems to me that much of the apparent disagreement comes from those on the outskirts of the debate, who don't properly understand it. The last couple of years has seen a number of confused articles - from Steven Pinker, Edward Wilson, Martin Nowak and others - who just don't know what they are talking about.

Part of the disagreement comes from inertia. People get taught one technique and then get attached to it - and are reluctant to use the other 'unnecessary' approach.

I also think this is partly a conservative vs revolutionary issue. Kin selection is the establishment, group selection is the rebel. Kin selection is tried and trusted, group selection is new and disruptive. Theories with these traits appear to different personality types.

There's also the issue of 'selfishness'. Group selection pictures groups that nurture cooperation flourishing at the expense of groups of selfish individuals. Kin selection seems to be promoting a picture of gene level selfishness. This picture is factually false (the reality doesn't change depending on how you look at it) but the connotations are there. Some like to publicly signal their unselfishness via their beliefs. To others, such cheap signalling seems more like tasteless self-promotion.

Lastly there's confusion over cultural evolution. Most of the group selection enthusiasts come from the social sciences. I've repeatedly heard them argue that kin selection only applies to genetic relatives, and that human cooperation extends beyond blood kin - so there must be something else going on. This argument ignores the important topic of cultural kin selection. The "something else" that is going on turns out to be kin selection after all.

Since kin vs group selection seems closely tied to political and moral issues, perhaps we won't see much more agreement on the topic anytime soon.

Kin selection's 50th birthday

There were prior murmurings, but 1964 marked kin selection's initial publication in a number of respects. Now it's 2014 - it's kin selection's 50th birthday.

Academics have noticed this and are celebrating. One of the celebrations is the Philosophical Transactions of The Royal Society B's theme issue:

‘Inclusive fitness: 50 years on’ compiled and edited by Andy Gardner and Stuart A. West

The introduction says:

In order to better assess the health of inclusive fitness theory on its 50th anniversary, here we showcase research showing the research programme in action, from the extremely pure, mathematical realm, through basic empirical science, to bold applications in a variety of disciplines.

I disapprove of the Claidière / Scott-Phillips / Sperber contribution. They doubt the applicability of kin selection to cultural variation, writing:

Darwinian selection leads to the maximization of inclusive fitness, and this explains the appearance of design in the natural world. Is there an analogous result for cultural attraction? As selection is a special case of attraction, design is possible and in some cases explicable in standard Darwinian terms. Having said that, such explanations will not apply generally, and may not even apply commonly.

From my perspective, this seems like ignorant nonsense. Kin selection is about as applicable and useful to cultural evolution as it is to understanding organic evolution.

Nowak nominates inclusive fitness for retirement

The 2014 annual question at The Edge is: What scientific idea is ready for retirement?

Martin Nowak nominated inclusive fitness. He writes:

Contrary to what is often claimed there exists no empirical test of inclusive fitness theory; nobody has ever performed an actual inclusive fitness calculation for a real population. Inclusive fitness was originally understood as a crude heuristic that can guide intuition in some cases, but not in general. It is only in recent years that inclusive fitness has been elevated—mostly by mediocre theoreticians — to a religious belief, which is universal, unconstrained and always true. Understanding the limitations of inclusive fitness gives us now the opportunity to develop mathematical descriptions of key phenomena in social evolution. It is time to abandon inclusive fitness and focus on a meaningful interaction between theory and experiment in sociobiology.

This seems like unsubstantiated scientific FUD to me.

Nowak claims that the:

dominant and unfortunate impact has been the suppression of meaningful mathematical theories in wide areas of sociobiology.

He means group selection? I think this is unreferenced and unsupported nonsense.

From the 1970s onwards we actually understood that evolution does not permit a single quantity that is always maximized. This fact still has to sink in with many in the inclusive fitness community.

I think that the first sentence here is technically mistaken. You can in fact, model the evolution of any dynamical system using the concept of maximisation of a utility function. Take, for example, the utility function that assigns world events that happen utility 1 and world events that do not happen utility 0. In this case, the evolution of the system can be modeled by "a single quantity that is always maximized". This is the fact of the matter. Nowak's proposed 'fact' is a simple falsehood. We didn't understand this 'from the 1970s onward' - it is simply not true in the first place.

Nowak writes:

On the level of genes there is no inclusive fitness.

Really? Most pairs of genes are either copies of each other (r=1) or not (r=0). Plug these numbers into Hamilton's rule and it works fine. This illustrates the meaning of "The Selfish Gene": genes only care about themselves - or copies of themselves. Nowak doesn't explain what the perceived problem is.

More relating to Nowak's article:

• Marczyk, Jesse (2014) Which Ideas Are Ready to Go to Florida?

• Reuell, Peter (2014) Harvard Gazette press release

Why can't we all just get along?

After the 2010 Nowak, Tarnita, & Wilson affair, Samir Okasha weighed in with a comment in Nature, effectively asking: why can't we all just get along?

The paper was titled: Altruism researchers must cooperate. It is indeed ironic that the science of cooperation has led to so much scientific acrimony.

In the paper, Samir embraces equivalence, writing:

kin and multi-level selection are not alternative theories; they simply offer different takes on the question of how social behaviour evolved. Proponents of kin selection, for example, explain sterile workers in insect colonies by saying that the workers are helping the queen to reproduce, and thus boosting their own inclusive fitness. Proponents of multi-level selection argue that the workers are providing a benefit to the colony as a whole, thus making the colony fitter than other colonies. These explanations may seem different, but mathematical models show that they are in fact equivalent

He says the persistent rival camps are a puzzle since:

The existence of equivalent formulations of a theory, or of alternative modelling approaches, does not usually lead to rival camps in science. The Lagrangian and Hamiltonian formulations of classical mechanics, for example, or the wave and matrix formulations of quantum mechanics, tend to be useful for tackling different problems, and physicists switch freely between them.

His explanation:

History shows that, despite its enormous empirical success, evolutionary biology is peculiarly susceptible to controversy and infighting. This is particularly true of social evolution theory, in part because of its potential applications to human behaviour.

I think this is essentially correct. People fight over application of evolutionary theory to humans for many reasons, but among them are: "it's complicated", and "it's important to get it right".

Group selection doesn't score well in the latter category. It isn't so much that it is wrong, it's more that it has led to decades of muddle, confusion and poor-quality science. If kin selection and group selection are feeling different parts of the same elephant, kin selection has hold of the trunk, while group selection is groping the left thigh.

It is certainly frustrating to have all the biology papers using kin selection, while all the humanities papers seem to use group selection.

A big part of the problem is misunderstandings surrounding cultural evolution. Cultural evolution has historically lagged by decades behind conventional evolutionary theory. There was a revolution in the 1970s in which group selection fell out of fashion, and kin selection became much more popular. A parsimonious explanation of the penchant for group selection in the social sciences is that the field of cultural evolution has yet to go through this transition. The significance of relatedness between memes and memeplexes has yet to be fully appreciated.

Nowak and Wilson are at it again!

You might think Nowak and Wilson would have had their fingers burned in the reaction to their 2010 Nature paper.

However, it seems as though they are at it again. They have a PNAS paper titled: Limitations of inclusive fitness by Benjamin Allen, Martin A. Nowak, Edward O. Wilson.

They deny that evolution can be usefully viewed as an optimization process, saying:

Thus, evolution does not, in general, lead to the maximization of inclusive fitness or any other quantity.

That's complete nonsense: Allen, Nowak, and Wilson don't know what they are talking about. Optimization models are perfectly general - and can model any dynamical system.

The guts of their paper is a criticism of the application of Price's equation to inclusive fitness.

Their main beef is linearity. They are concerned that the 'adding' and 'subtracting' that goes on in the definition of inclusive fitness limits its generality. They write:

Inclusive fitness assumes that personal fitness is the sum of additive components caused by individual actions. This assumption does not hold for the majority of evolutionary processes or scenarios.

However, this linearity doesn't really cause problems - since you can approximate non-linear curves using a series of line segments.

Inclusive fitness is mostly concerned with the issue of whether some helping behaviour will evolve. It calculates whether the net selective effect of a behaviour on the frequency of a gene responsible for it (some of which may be copies in relatives of the actor) is positive or negative (relative to a set of alternatives) in the current environment. The math of inclusive fitness tells you whether the gene is selectively favoured. That's not quite the same thing as whether the behaviour will evolve (maybe it will drift into extinction) - but it's a good start. Nobody ever thought that the behaviours and genes involved had to not interact. Nobody thought that the rate of change of the frequency of the gene would be fixed over time. Maybe the environment will change in crazy non-linear ways in the future - and you'll have to redo your sums.

Basically, it isn't true that inclusive fitness theories assume that personal fitness is a linear sum of action fitness deltas. An action can change the environment (or the actor) in ways that affect the costs and benefits of future actions - and this is perfectly compatible with Hamilton's rule. It means that you may have to apply the rule more than once, is all.

Allen, Nowak, and Wilson's paper is like saying: I've got this crazy non-linear function, there's no way your linear approximation can match it. Except that: yes, there is - a series of linear functions can approximate any other function arbitrarily closely.

If you think that making this sort of objection is childish, I think that you're right - it is childish.

The paper says it was: "supported by a grant from the John Templeton Foundation". It seems like even more fuel for those who think that the Templeton Foundation is systematically distorting science.

Commentary

• Nowak and colleagues skewer Inclusive Fitness
• Now I know I am “El Lobo Solitario”: I don’t even agree with Allen, Nowak, and Wilson
• Inclusive fitness, models, and religious evolution

References

• Allen B, Nowak MA, & Wilson EO (2013) Limitations of inclusive fitness. Proceedings of the National Academy of Sciences of the United States of America
• Nowak MA, Tarnita CE, & Wilson EO (2010) The evolution of eusociality. Nature, 466 (7310), 1057-62

Kin selection is very general

Kin selection theory can only be applied when organisms are influenced by their kin. However this happens at least once in every organisms' lifetime - when they are born.

Kin selection applies to calculations of parental investment and cases where there is parent-offspring conflict. Since all multicellular creatures have a parent-offspring asymmetry and provide some kind of resource bolus to their offspring, that means that kin selection applies to all multicellular organisms.

In other organisms, kin selection is also often relevant. Many microscopic organisms exhibit limited dispersal - and so are surrounded by their kin. If your kin are nearby, you should typically curb your pollution, share your food, and commit suicide if you are compromised by pathogens. Many parasites spend much of their time inside their hosts - where they are often surrounded by their kin.

Kin selection also applies to cultural variation - in the form of cultural kin selection - where it is similarly ubiquitous.