Herbert Gintis vs inclusive fitness theory

Herbert Gintis has an elaborate attack on inclusive fitness theory on his web site. It's titled: Inclusive Fitness and the Sociobiology of the Genome. It says, among other things:

The general point is that if there is a conflict among loci concerning fitness maximization, and if the frequency of alleles at one locus affect the fitness costs and payoffs at other loci, then it is logically impossible that the allele at each locus maximize its inclusive fitness. Rather, the proper setting is evolutionary game theory [...]

I think this is a case of expecting too much from the concept of maximization. The idea of maximization does not imply that all parties reach the maximum they are seeking. It doesn't even imply that they increase the value they are trying to maximize. A hill-climber might be climbing a hill on a mountain that is sinking into the sea. Their elevation may decrease until it reaches zero and they die. This is quite consistent with the idea of maximization.

Gintis apparently claims that frequency-dependence invalidates the idea of maximization of inclusive fitness:

If the genome’s success is based on a pattern of cooperation, promotion, and suppression across loci, which will occur, for instance, if the production of a protein, RNA sequence, or social behavior requires the collaborative activity of many genes (Noble 2011), or if there are frequency dependent social interactions among individuals in a social species (Maynard Smith 1982), then neither genes nor individuals can be characterized as maximizing inclusive fitness. The conditions under which a population genetics model of gene flow implies fitness maximization at the gene or individual level has been carefully explored (Grafen 1999, 2002, 2006; Metz et al. 2008; Gardner and Wild 2011; Gardner West and Wild 2011). With frequency independence, they affirm the maximization hypothesis. With frequency dependence, the hypothesis it is in general false, and no careful researcher has ever claimed otherwise.

Frequency dependence typically means that genes are spending time in environments that differ from the average of the environments they evolved in. It's a case of adaptive lag - where organisms are adapted not to their current environment, but to a weighted average of ancestral environments. This is a classic case where organisms sometimes behave sub-optimally in ways that don't further their own interests.

In such cases, organisms don't always act to maximize their inclusive fitness - but rather act to maximize their inclusive fitness under the hypothesis that they are in an environment that is like the one that their ancestors evolved in. Of course, that hypothesis might be mistaken.

In fact, sufficiently sophisticated creatures might be able to evolve a superior strategy - where they sample the frequency involved and change their behaviour adaptively, based on the observed frequency. So, what frequency dependence often boils down to is that organisms can sometimes fail to maximise their inclusive fitness - because they have cognitive limitations and make mistakes.

In this case, I feel that Gintis is expecting too much from inclusive fitness theory. It doesn't claim that all creatures maximize inclusive fitness perfectly. Creatures have all kinds of imperfections and limitations that prevent them from acting as perfect maximizers.

More fallout from the 2010 Nowak, Tarnita and Wilson kin selection meltdown

Fallout from the 2010 Nowak, Tarnita and Wilson kin selection meltdown continues to rain down. Earlier this year we had this (from Wilson and Nowak):

Inadequacy of Inclusive Fitness and Beyond

The evolution of social insects often is presented as a testing ground for inclusive fitness theory. It has been claimed that inclusive fitness can explain sex allocation, worker policing, conflict resolution, and evolution of eusociality (14), but precise calculations of inclusive fitness do not exist for any of these phenomena. Relatedness-based arguments, such as the monogamy window hypothesis, are not necessarily wrong but rarely provide a complete picture; moreover, one cannot rely on inclusive fitness to determine when they are correct. The failure of inclusive fitness theory to provide exact calculations is not surprising, because a mathematically meaningful approach to inclusive fitness (72) cannot be performed for the majority of evolutionary processes (5), and the linear regression method (73⇓–75) does not provide meaningful insights and cannot make empirical predictions (76). In general it is not possible to study social evolution from the perspective of an individual by evoking the virtual quantity of inclusive fitness. Instead we should focus on how natural selection acts on alleles that modify social behavior. On the level of genes or alleles, there is no inclusive fitness: Mathematical descriptions of the evolutionary dynamics of genetic mutations do not require a partition of fitness effects (which usually is impossible anyway) or any other aspect of inclusive fitness theory.

These folk have a bee in their bonnett. I - and many other scientists - think it is a stupid one. For homework, I think these authors should write an article explaining - at undergraduate level - why kin selection has been as successful as it has been - including when and why it is useful. At the moment, it doesn't look as though they are clear on these topics. The Price equation can't be used to make empirical predictions? It might be funny if it wasn't so silly and sad. If you don't have a sympathetic understanding of a topic, you are often in a poor position to criticise it. You wind up attacking straw men of your own making.

IMO, probably the main lesson here for other scientists is the value of humility in science. If you are overconfident, nail your flag to the mast and then dig in then it is easy to wind up making a fool out of yourself.

Kin or group selection: which is more confusing

The last decade has seen a bit of a shake out in the domain of kin selection and group selection.

Until recently it was possible to argue that the group selection advocates were consistently more confused about social evolution than users of kin selection. However as group selection advocates learned more about their topic some of them gradually started making sense - and some of them now hold fairly reasonable positions.

Also, it has become clear that some of the opponents of group selection are very confused about the whole topic. Steven Pinker wrote a fairly embarrassing article on the topic in 2012 - and some of that article's commentators made similarly embarrassing follow-ups.

Popular blogger Jerry Coyne has written a string of articles about group selection. He doesn't seem to have made much effort to understand what advocates of group selection are saying - and so produces mostly straw man attacks.

Richard Dawkins isn't exactly helping either. For example, he writes:

Is a group a replicator? No. We do not have a 'group pool', a metapopulation in which some groups are more successful than others at making replicas of themselves, replicas that persist through geological time.

This seems like classic replicator rot to me. Try talking about copying and heredity instead, and we do indeed have collections of groups, some of which are better at making copies of themselves than others. Maybe none of them are especially brilliant at making copies of themselves: but so what?

The broad equivalence between kin and group selection makes the issue of which framework causes more confusion into a significant issue. One of the main problems with group selection historically has not been that it's wrong, but that it is confusing and easy to mis-apply.

The confusion by the group selection opponents is unfortunate. It doesn't help to make the case that kin selection is less confusing and less subject to abuse.

However, I think it is still dwarfed by the confusion related to group selection. Martin Nowak and E.O. Wilson are perhaps the most prominent examples - but it seems to me that they represent only the tip of a pretty substantial iceberg.

Kin selection and its critics

Here's an interesting new paper: Kin Selection and Its Critics - Jonathan Birch and Samir Okasha.

Samir Okasha wrote a rather flawed book on group selection some years ago. However, this article shows that he is doing a good job of keeping up with developments in the field - and it isn't so easy to find significant mistakes in this large recent article.

I think one problem is that it takes the work of Nowak and Wilson a bit too seriously.

In one place the authors argue against equivalence, saying:

In one respect, the kin selection approach is arguably more general than the multilevel approach, because the latter requires that individuals be nested into nonoverlapping groups, as in figure 4; this is necessary for the decomposition technique in box 2 to apply (Hamilton 1975, Okasha 2006, Frank 2013). Groups of this sort exist in some taxa (e.g., the colonies of many social insect species). But in other cases, individuals engage in social interactions with their conspecifics, but there are no well-defined, discrete groups. The kin selection approach can handle such cases easily; indicative of this is that in deriving equation 4 above (box 1), we did not make use of the fact that the individuals were nested into nonoverlapping groups. Therfore, the claim that kin and multilevel selection are formally equivalent requires at least this qualification.

This doesn't seem like too much of a stumbling block to me. The modern "group selection" approaches depend critically on defining a "group" to include any collection of organisms - no matter how fleeting or ephemeral. You have to buy into this conception of a "group" for the approach to be worth considering in the first place.

The authors say:

The widespread preference for kin selection may be partly due to multilevel selection's association with the flawed good-of-the-group tradition of the 1950s and 1960s and the associated superorganism concept, of which many biologists remain suspicious. It is undeniable that the careless appeal to group-level advantage as a way of explaining a trait's evolution led to serious errors in the past, so biologists’ wariness of this mode of explanation is understandable.

That's about the size of it. However, this paints group selection's problems as being in the past. I think that this is inaccurate. A fairly cursory look at the evolutionary social sciences shows that misapplication of group selection is still widespread.

The essay closes with a plea for "causal aptness": use kin selection when you have relatives, use group selection when you have interacting groups. This proposal sounds reasonable - but I think it would do little to stem the existing misuse of group selection. The problem is that people see differential group reproduction, reach for group selection, and produce just-so stories about how group traits are the product of differential group extinction or reproduction. This is a systematically bad methodology that use of group selection directly encourages. Using "causal aptness" would probably boost usage of group selection. That seems as though it is likely to cause a range of negative outcomes associated with the misuse of group selection - and so I regard the proposal as suspect.

"Causal aptness" is one proposal. A big health warning relating to the misuses of group selection is another. I think that, if you adopt the first proposal, you should also adopt the second one.

Disagree with Steve Frank

I read Steve Frank's paper A new theory of cooperation recently. Steve Frank is an expert, but I thought that this paper was mostly wrong. The theme of the paper is that suppression of competition within groups represents a new theory of cooperation - that beyond kin selection and reciprocity. He credits the development of the idea to Richard Alexander - in The Biology of Moral Systems.

Many of the examples of suppression of competition within groups Steve gives are due to kin selection. Steve disagrees with this, writing:

[...] the main weakness of the theory was also apparent. Extensive cooperation occurs between nonrelatives. Different genes in genomes are functionally integrated but not related. Larger human societies often have many highly cooperative but distantly related individuals. Some of this cooperation between nonkin can be explained by extensions of reciprocity to a general notion of mutual benefit for interacting partners (West Eberhard 1975).

In the early 1980s, kin selection plus these extended notions of reciprocity were the main conceptual tools. Those limited conceptual tools led to blind spots about unsolved problems. Only rather forced theories of mutualism could work for the nearly complete integration of genes into cooperative genomes. Only a very enthusiastic belief in the scope of reciprocity could explain the broad social integration in larger groups of weakly related human

However, cooperation between groups of "unrelated humans" that is not due to reciprocity has turned out to be largely associated with cultural kin selection. This is kin selection applied to memes - not genes. Many of Steve Frank's examples fit onto the familiar kin selection / group selection axis - though he apparently doesn't fully realise this.

There is indeed another force that produces cooperation besides reciprocity and kin selection - and that is "manipulation". Manipulation is where agents impose their wills on other agents. Teams sometimes cooperate because they are cooerced into doing so by supervisor figures. Manipulation helps to explain suppression of competition in cooperative genomes. The efforts of individual genes to bypass meiosis is thwarted by the "parliament of genes" in the genome. Manipulation isn't the same as kin selection or reciprocity - so Steve Frank's paper is partly correct.

However, I think that there's a good reason to call this "manipulation" and not "suppression of competition". "Suppression of competition" is just another way of saying "cooperation". Explaining cooperation in terms of "suppression of competition" seems pretty circular to me.

Manipulation is responsible for the symbiont hypothesis of eusociality. This was proposed in 1934. The "parliament of genes" phrase comes from Leigh (1971). Since manipulation is such an obvious and well-known phenomenon, there may well be earlier examples of it being involved to explain cooperative behaviour. As a theory of cooperation, the idea is not exactly new - and I'm pretty sure that Richard Alexander wasn't responsible for it.

In The Biology of Moral Systems, Richard Alexander wrote:

It is a common error to suppose that something additional to nepotism and reciprocity is required to account for the structure of society. (p.153)

Here it sounds as though he repudiates this particular revolution.

West and Gardner on kin vs group selection

West and Gardner have not been shy about pointing out the virtues of kin selection over group selection. Here they are with a summary in 2013:

The most frequently used methods are neighbour-modulated and inclusive fitness. In particular, modern neighbour-modulated fitness methods allow the modeller to go from the underlying biology to an expression or fitness, in a way that facilitates the development of relatively general models [8,27,28,35,37]. In contrast, the group selection approach is used relatively little for modelling specific traits partly because as soon as one moves away from the simplest, most abstract models, and wants to add in real world biology, it often becomes analytically intractable — for example, when populations are structured into different classes of individual, according to sex, age, caste or ploidy [38–40].

I know these folk also have plenty of other objections to group selection. Here, forced to pick one, they went for analytic tractablility. It seems like an odd choice to me. As a veteran computer modeller, analytic tractablility comes relatively low on my list of virtues. I would probably list group selection's association with junk science as my number one complaint.

Identity by descent: a confusing concept

There's a lot of discussion of kin selection using the term "identical by descent" and "identical by state". The idea of "identical by descent" is that genes are shared as a result of direct descent from a common ancestor - without recombination or mutation. "Identical by state" just means that the DNA sequence is shared. It is said that 50% of their genes with their daughters "IBD".

I think the "identical by descent" terminology is confusing and not useful. In biology, if genes are identical, they are practically always identical through being copied from one (or more) shared ancestors. Mothers share more than 50% of their genes with their daughters - due to genes that have reached fixation, inbreeding and so on. However they still share these gene sequences due to descent from shared ancestors. As to a gene mutating into another form and then mutating back again. If you do the sums, for a gene of any reasonable size this rapidly becomes ridiculously unlikely. There's too much scope for neutral mutations elsewhere. In practice, when genes are identical, the odds are enormously in favour of this being due to shared ancestry. The idea that recombination with an identical gene makes genes not "identical by descent" is an awful one. They are still "identical by descent" - just descent from various different ancestors.

You can't say that mothers share 50% of their genes with their daughters "IBD". It is confusing and mistaken. If you want to use the 50% figure, you have to find another reason for doing so.