How kin selection pushed group selection into the scientific fringes

Group selection lost out to kin selection in the 1960s and 1970s as an explanation for cooperative behaviour. Group selection went on to lead an underground existence - in which a few remaining proponents sought out ways to find things which group selection explained which kin selection did not.

We now know that modern versions of these theories make the same predictions. So there isn't really anything that group selection can explain that kin selection cannot. However this didn't stop the group selection proponents from trying to find these types of phenomena. Indeed, if they had succeeded, fame and glory would have awaited them.

This quest took group selection to the borderlands of science. Kin selection was uncontroversially used to explain obvious adaptations - such as breast feeding, parental care and nepotism. Group selection picked more controversial targets - senescence, the maintenance of sexual recombination and cultural evolution. The theme of these topics seems to have been avoiding rapid refutation of: "kin selection explains that without invoking group selection".

This quest now seems to be mostly over. Most of the group selection enthusiasts have publicly given up their original quest - and have accepted the equivalence between kin selection and group selection.

However the topics group selection is invoked to explain still seem to be skewed away from those that kin selection is used to explain. As a result, group selection is generally offered as an explanation in areas where the theory doesn't function well. This seems like a hangover which group selection is still recovering from.

The "multi-level" terminology

This article will claim that "multi-level selection" and "group selection" should not be understood as being synonyms.

It does appear that "multi-level selection" is terminology that was invented to give group selection a face lift - and allow it to escape from an unglamorous past.

However, group selection is not more or less "multi-level" than kin selection is. The concepts of "relatedness" and "kin selection" can be applied at multiple levels too. One can meaningfully discuss the relatednes between cells in an ant, the relatedness between an ant and its sisters and the relatedness between entire colonies of ants. This has been understood since the 1970s and it can be seen as a result of the generality of the Price equation.

These days, group selection enthusiasts often prefer to use the "multi-level selection" terminology. This article is my explanation of why I rarely follow them - and why I think it is a confusing gambit. Kin selection is "multi-level" too. Using the term "multi-level selection" fails to distinguish between kin selection and group selection. It is true that kin selection and group selection are equivalent - in the sense that modern versions of these theories make the same predictions. However that doesn't mean that proponents use the same methodologies. These are still topics that are worth distinguishing between. The best way of doing that is, I think to use the terms "kin selection" and "group selection".

Group selection enthusiasm still rampant in the social sciences

Most evolutionary biologists got over group selection back in the 1970s. However, there's one area of biology where it is particularly prominent: the social social sciences. There's particular enthusiasm for cultural group selection - as though cultural evolution plays by different rules in this area.

Cultural kin selection represents an alternative perspective which makes little mention of selection acting on groups. Instead of humans being part of innumerable overlapping groups, their genes and memes are modeled as being related to the genes and memes of others. This perspective has been much more enlightening in the organic realm, and I think it will prove to be much more enlightening in the cultural realm as well. The largely-fictional groups of group selection are just a clumsy and awkward way of viewing the situation - most of the time. The perspective has a long history of producing dud science.

In most of evolutionary biology, 90% of scientists are using kin selection and 10% are using group selection. In the social sciences, it's the other way around. I think that this fairly clearly indicates the existence of a problem.

Why is group selection still so popular among social scientists? For a long time many of them held out hope that it would prove to be a new theory of social behaviour. These hopes now appear to have been crushed by the failure of the theory to make different predictions from the long-established orthodoxy of kin selection.

Social scientists have a long history of not understanding how evolutionary biology applied to their subject areas. As a result there's a large scientific lag afflicting the study of cultural evolution. Group selection enthusiasm seems to be clearly one aspect of that: the numerous social scientists involved are stuck back in the 1960s somewhere, where the virtues of the kin selection perspective were not yet widely appreciated.

Lastly, group selection in the social sciences seems to have found extensive funding from the John Templeton Foundation. In a surreal twist to the final battle between science and religion, group selection enthusiasm has been funded to the tune of millions of dollars. That kind of marketing budget can buy a considerable quantity of confusion.

Obvious types of kin selection

If you ask a student of kin selection about the most obvious aspects of the human phenotype that have been influenced by kin selection and are coded for in human DNA, I think you would generally get back a list looking something like this:

• Genitals;
• Breasts;
• Placenta;
• Umbilical cord;
• Female body fat;
• Maternal love;

If you ask a group selection proponent the corresponding question (what are the most obvious aspects of the human phenotype that have been influenced by group selection and are coded for in human DNA), I think you would get back a very different list. The group selection proponent might be more likely to mention multi-cellularity - but I think they would be highly likely to back a very different list.

What's up here? Kin selection and group selection are basically the same thing.

I don't pretend to have a complete explanation for this - but I think the group selection enthusiasts were led astray by the urge to distinguish themselves from kin selection enthusiasts. If discussing family groups, it was obvious that kin selection applied to it - and explained it. The group selection advocates therefore focused their attention elsewhere - where it seemed as though there was more chance to explain new phenomena that kin selection failed to cover. This hypothesis explains the migration of group selection enthusiasts to cultural evolution - since that is obviously not down to shared DNA.

Eventually, there was nowhere else to run, and the group selection advocates mostly gave up their claims that group selection was something new and different. Now the rhetoric in the area has mostly shifted to other issues.

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.

A brief history of cultural kin selection

Kin selection applies to cultural variation. This is called cultural kin selection. It is an important topic.

Here's a brief history of the concept:

The observation that social and genetic kinskip were different in humans dates back to Lewis Henry Morgan in 1871.

Boyd and Richerson published one of the first articles on the topic in 1980 - connecting cultural kin selection and cultural group selection.0 An early modern article on the topic was written by Kristen Hawkes in 1983 and titled: "Kin Selection and Culture".

David Schneider's 1984 book "Critique of the Study of Kinship" argued that kinship was a different concept in different cultures, that people treating non-relatives as though they were kin was common - and that this reduced the significance of kin theories from biology when considering humans.

The idea of cultural kin selection appears in David Hull's (1988) book. David wrote:

Increasing one's conceptual inclusive fitness in science means increasing the number of replicates of one's contribution in the work of successive generations of other scientists.

...and...

science is a function of conceptual inclusive fitness.

Next, Francis Heylighen's (1992) paper: "Selfish Memes and the Evolution of Cooperation" stated:

The mechanism of kin selection can be extended to memes by redefining inclusive fitness as the fitness of a meme taking into account all its carriers. All individuals carrying the same meme can be viewed as relatives or kin insofar as this meme is concerned. Hence, the tendency to be altruistic towards offspring or close kin that follows from genetic evolution can be generalized to altruistic tendencies towards members of the same memetic or cultural group. The explanation for ultrasociality in the social insects on the basis of genetic inclusive fitness can be readily transposed to the emergence of ultrasociality in humans on the basis of memetic inclusive fitness.

He went on to explain how memes exploited kin-altruism towards relatives to redirect benefits towards cultural relatives:

many ethical systems explicitly refer to the ideal of "fraternity", and sometimes members of the same cultural group (e.g. monks or Freemasons) are supposed to call each other "brother". Though these are not brothers in the biological sense, the meme attempts to harness the innate tendency to behave altruistically towards kin and to use it for purposes different from the increase of genetic inclusive fitness.

Around the same time, Paul Allison published a series of papers on the topic - most notably "The Cultural Evolution of Beneficent Norms".

Heylighen revisited the idea of cultural kin in 1997, writing:

The genetic argument for altruism towards individuals carrying the same genes (kin selection) generalizes to altruism towards carriers of the same memes.

In 1997, David Hales wrote in "Memetic Evolution & Suboptimisation":

I now want to propose that two previously described extensions to basic natural selection can be applied subtlety within a meme framework: kin altruism and group selection.

There's a paper by John Evers (1998) called "A justification of societal altruism according to the memetic application of Hamilton's Rule", which attempts to directly adapt Hamilton's Rule to memetics - based on the idea of the "fraction of shared memes". John doesn't really go into the difficulties associated with this idea, though.

Also in 1998, "Cultural Software" by J. M. Balkin came out. Balkin clearly understood cultural kin selection, writing:

We often see people energetically promulgating their memes in the forms of beliefs, behaviors, artifacts, and customs while struggling with others who resist or disagree. Just as competition between biological kin groups can lead to strife, so can competition between cultural kin groups.

...and...

Just as individuals have varying degrees of genetic kinship, they also have varying degrees of memetic kinship. The two forms of kinship are cross-cutting: people can have many of the same memes even if they are completely unrelated. If the analogy to evolutionary arguments about kin-based altruism holds, then we would predict considerable altruistic behavior between people with lots of similar cultural software-for example, people of the same religion or culture, teachers and students, members of the same fraternity or club.

In 2000, David Hull showed that he understood the idea that kin selection extended into the cultural realm, writing: "One final example of similar processes operating in biological and memetic change is kin selection". He went on to give an example:

In science, scientists also distinguish between kin and non-kin, but the relevant genealogy is conceptual. The issue is not who holds similar ideas but who is conceptually connected to whom. The best way to increase the likelihood that you will be a successful scientist is to work under a successful scientist (Hull 1988).

Momme Von Sydow in a 2000 thesis wrote:

Corresponding to kin selection on the biological level, memes might ‘egoistically’ support their relatives in the same brain or in different brains, if they were identical (or similar enough). One might formulate a mathematical inequality analogous to Hamilton’s, where memes would replace genes.

In 2001, an important paper on tag-based cooperation came out - by Riolo, Cohen and Axelrod. It was followed by a large number of other papers on the topic. Riolo had come up with the idea much earlier - and had performed computer simulations of tag-based cooperation in 1992.

In 2001, Karl Sigmund and Martin Nowak, pointed out that cultural tag-based cooperation was a form of cultural kin selection.

Gordon Rakita (2003) rechristened cultural kin selection "kith selection". The term "kith selection" is kind-of cute - but it seems as though it is unnecessary jargon - and it doesn't fit in very well with "cultural group selection".

The idea of "cultural kin selection" appears again in Francis Heylighen's (2008) article: "Cultural Evolution and Memetics" - where he says:

Horizontal transmission of cooperation norms solves this problem, since the members of a cultural group are all memetically related to each other, sharing their memes rather than their genes. Therefore, cultural kin selection will extend to all members of the group (Evers, 1998). This entails a selective pressure for memes to support the fitness of the whole group of their carriers, e.g. by promoting cooperation.

In 2009, Gordon Rakita spelled out some of the implications of the idea of "kith selection" in detail. He started out by introducing a class of behaviours that kin selection acting on genes appears to explain poorly:

Kin selection does not seem to offer a suitable explanation for instances in which soldiers give their lives for their comrades. The conditions necessary for the model are not met, for example, soldiers are rarely genetically related. Given this, how are such acts to be explained?

He then offered a fine explanation - involving selection acting on memes:

A meme that encourages a soldier to throw himself on a grenade to save his comrades will negatively impact its future prospects of being transmitted to others. (This behavior is similar to that of the worker ant who forgoes reproduction in favour of the reproductive potential of the queen.) However, if the soldier’s comrades also carry the meme for grenade smothering, then the soldier’s behavior will indirectly impact the future replicative success of those other copies of the altruistic meme. This mimetic model of kin selection I term kith selection, kith being unrelated but like-minded acquaintances

Recently Mark Pagel's Wired For Culture book offered an explanation of human cooperation in terms of cultural "green beard" effects. In the process, he pointed out that such green beard effects were a kind of kin selection.

For references, see the cultural kin selection bibliography.

Clade selection

"Kin selection" and "group selection" are common terms for the way that organisms help organisms which are similar to themselves. I've proposed the term "similarity selection". Another contender is "clade selection". This term came from George C. Williams (1992).

Dawkins said of this:

Williams efficiently disposed of “group selection,” which never recovered (except as a muddled version of kin selection). But in Natural Selection: Domains, Levels and Changes (1992), where he gathered many threads of thought, he developed the important and superficially similar idea (foreshadowed in Adaptation and Natural Selection) of “clade selection” to explain, not “altruism” but macroevolutionary patterns of diversity and - as I would put it - “the evolution of evolvability.”

"Clade selection" seems like better terminology than "group selection" - in some respects. Like the term "kin selection" it puts an explicit emphasis on relatedness. Group selection only works - in the sense of producing group-level adaptations - when relatedness is involved. So: why not use the term clade selection?

Alas, I think there's a good reason not to use the term "clade selection". A clade consists of an organism and all its descendants. The problem is with the "all". You can still have group selection that works without it being clade selection - by the fitness delta involved not affecting all the descendants.

The "all" in "clade" makes "clade selection" a confusing term. Not worthless, perhaps, but I don't think I can endorse the term.

Tim Tyler: Williams, Plan and Purpose in Nature (review)

Tim Tyler: Williams, Plan and Purpose in Nature (review)

Transcript:

Hi. I'm Tim Tyler, and this is a review of this book:

Plan and Purpose in Nature: The Limits of Darwinian Evolution by George C Williams.

George Williams is an expert in Darwinian evolution, and this book is an attempt to condense his knowledge down into a format which is easily digested by those new to the field. It is very readable and entertaining book.

It covers basic issues in evolutionary biology, particularly adaptationism, the unit of selection, sexual reproduction, senescence and medicine.

Williams embraces the term "The adaptationist program" - saying he almost selected it as the title of his book. This phrase originated with Gould and Lewontin - and was intended as a term of derision. No doubt Williams is making a point by using the term, but I would have preferred that adaptation enthusiasts left it alone - making it harder for critics to point at instances of the alleged phenomenon.

The book was published in 1996 - and I thought it was interesting to see what had changed since then. Williams offered an explanation for sexual reproduction that invokes generating diversity to help adapt to novel environments. For example plants like strawberries reproduce using runners and vegetative reproduction locally, but produce sexual seeds for transmission of offspring to a diverse range of remote environments. That is not a completely unreasonable explanation, but the modern way of putting it invokes parasites. If it wasn't for the need to evade parasites, the environment would often not change fast enough to favour sexual recombination. Williams does mention parasites, but they aren't the main feature. Another area where I noticed there were some oddities were in the chapter on senescence. The disposable soma theory and the antagonistic pleiotropy theory of aging are given without being named - and Williams emphasizes how senescence of living bodies is nothing like senescence of machinery - saying:

In thinking of senescence, the analogy to the wear and tear, or corrosion, or other process that ultimately causes an artificial device to fail is utterly misleading.

I think that the relationship here is close enough to not deserve being described as "utterly misleading". Indeed these days we have new modern theories of senescence - like "reliability theory" - that apply to both machinery and bodies, that highlight the relationship between senescence in both kinds of system.

The section about group selection has stood the test of time reasonably well. Williams says that most animal groups are not functionally organized, and that most groups are "just mobs of self-seeking individuals". That's true - though these days people might take more care to mention the possibility of cooperation with kin - i.e. genetic selfishness, not individual selfishness.

The section about medicine is welcome as well. However, while Darwinian medicine sounds nice, we seem firmly embedded in the era of "drug company" medicine, with little sign of an end in sight.

At the end of the book there's a section on philosophical implications. Williams describes the product of natural selection as immoral. He says "although the biological creation process is evil it is also abysmally stupid". His example of the horrors of natural selection is infanticide by males, which he argues is natural and adaptive - though obviously infanticide by males is certainly not adaptive in many modern societies today - since it is likely to result in extended incarceration. Williams endorses Dawkins' proposed rebellion against the selfish replicators and responds to naturalistic moralities with condemnation. This is a common position these days, but human morality sits firmly in the domain of evolutionary theory, and if your theory of evolution doesn't explain it, you need to rethink it. I figure that evolutionary theory offers reasonable explanations of morality that we don't need to apologize for.

Anyway, this is still a fine book - though perhaps some learned readers might find it too simplistic.

Enjoy,

Tim Tyler: Okasha, Evolution and the Levels of Selection

Transcript:

Hi. I'm Tim Tyler, and this is a review of this book:

Evolution and the Levels of Selection by Samir Okasha

I'd previously read Samir's Very Short Introduction to the Philosophy of Science. I thought that was good - and so I had some idea of what this book would be like.

The book contains an interesting and entertaining romp through the territory of group selection. It's what I call a "firehose presentation". In other words, it's a long stream of technical material that doesn't let up. This is a good match for my own preferences in a science book. Samir goes through practically every controversy in the field, and provides insightful opinions and commentary.

The book contains discussions of the Price equation and its significance, causality, emergence, evolutionary transitions, the gene's eye view, species selection, the group selection controversy and kin selection.

I thought the book was interesting and good. However, there were also quite a few parts of it which I disagreed with - or did not like. This is a reflection of the controversial nature of the subject matter.

The book dates from 2006. Throughout most of the history of the field of group selection, many of its advocates considered it to be a super-set of kin selection - often saying things like: relatedness is only one of many ways in which altruists can form groups which are then selected. However in recent years, the quest to find things that group selection explained - and that kin selection did not - seems to have petered out, with many of the most vocal group selection advocates now proclaiming its equivalence to kin selection. Samir's book predates many of these developments - and I suspect anyone writing a book on the subject today would treat the topic rather differently.

The book discusses kin selection only rather briefly. There's a discussion about it in the chapter relating to the group selection controversy, and another one in the chapter about evolutionary transitions. Samir recognises the possibility that kin and group selection might be equivalent, and cites several sources who claim that it is, sometimes approvingly. However, most of this book makes no mention of kin selection.

These days, I think few would approach group selection this way. Kin selection has a rich and successful history, while group selection has spent most of its existence mired in confusion and controversy. Kin selection has been much better studied. So: an obvious approach to many of the topics in this book would be to just use kin selection. However, it is hard to imagine this whole book being written in the language of kin selection. A good number of the issues just seem less important from that perspective. For example, in group selection there's the issue of what counts as a group. This broadly maps onto the issue of what counts as an individual in kin selection - yet this issue seems less controversial. Group selection faces of issue of how to model parly-overlapping groups - since most group selection models feature disjoint groups. Yet the corresponding issue of partly-overlapping families in kin selection seems less contentious. It's hard to escape the impression that the need for this book is partly because group selection is so awkward, difficult to understand and poorly-studied. Since kin selection is much better studied and much more widely used, it seems as though there would be less need for a philosopher to clear up misunderstandings in the field.

Samir offers several digs at the views of Richard Dawkins in the book. He criticises the idea that evolution is based on replicators, offering Hull's comment about them "passing on their structure intact" to claim that the term "replicator" implies high fidelity copying. I think that practically everyone on both sides of this debate agrees that high fidelity copying is not necessary - and it's high fidelity information transfer that matters for cumulative adaptive evolution. No modern users of the term "replicator" in biology use the term in that way - and many of them have objected to this persistent misunderstanding. Of course it's partly Richard Dawkins' fault for assigning an ordinary english word a counter-intuitive technical meaning.

Saimr also criticises the gene's eye view on two grounds. First, he says that it ignores behavioural and environmental inheritance. That isn't true if you adopt an information-theoretic definition of the term "gene" following Williams - since then memes are a type of gene, and the gene's eye view remains valid. Saimr also says that epistasis and "modifier genes" act against the gene's eye view. This is strictly true, but some linearity in the expression of genes is really all that is required to make the gene's eye view useful. Since a linear component in the expression of genes is ubiquitous, this issue seems like a storm in a teacup to me.

Like any complex technical book, there are some mistakes. The most embarrassing one I spotted was where Samir offered an incorrect definition of inclusive fitness - including the "augmenting" but not the "stripping" component - on page 145. Samir's explanations are usually clear - but sometimes the light fades. One such problem comes with the concepts of "MLS1" and "MLS2". Samir introduces these concepts by saying that they represent different focuses of interest on page 56. However on page 59 we hear that "MLS1 and MLS2 are distinct processes" and "whether either occurs in a particular case is a matter of objective fact". At best, this sort of material is very confusing.

Overall, this is a fine book - but I was left wondering if Samir had directed his energies in an appropriate fashion. The book will probably contribute to the modern group selection revival. However that revival seems likely to be accompanied by the usual muddle and confusion that follows group selection around like a black cloud. The problems with group selection at this stage are more sociological than anything else. Yes, groups exhibit reproduction and differential reproductive success, and that affects the course of evolution, but the problem is that practically whenever group selection gets used it results in junk science, or at best, science that is inferior to that which would have been produced by using kin selection. Looking at the mess that group selection has caused in the evolutionary human sciences illustrates this point. Does the world really need more group selection? After reading Samir's book, I was still sceptical. Samir doesn't address sociological questions concerning whether the muddle associated with group selection means that it does more harm than good. Instead, he just wants to clear up the muddle. But in that case: why not use kin selection? It seems much better studied, much less confusing, and has produced much less junk science.

What I think group selection needs most is clearly-articulated reasons to use it in place of kin selection. At the moment, the "why not use kin selection?" question is challenging to answer. Maybe there are reasons - but this book doesn't really provide an answer. It doesn't even ask the question.

Enjoy,

Group selection and kin selection: formally equivalent

These days, there's a scientific consensus about group selection and kin selection.

As Marek Kohn said in 2008:

There is widespread agreement that group selection and kin selection — the post-1960s orthodoxy that identifies shared interests with shared genes — are formally equivalent.

As Michael Wade, 2009 put it:

It is remarkable that kin selection has been widely accepted and group selection widely disparaged when, for simple genetic models, they are actually equivalent mathematically.

As Peter Richerson, 2012 put it:

I think most evolutionists now agree that kin and group selection are the same thing.

Such observations date back to Hamilton (1975). Queller (1992) is another important paper on the topic.

Modern paper titles in the area include: "Group selection and kin selection: two concepts but one process" and "Group selection and kin selection: formally equivalent approaches".

In "Social semantics: how useful has group selection been?", West, Griffin and Gardner (2009) state:

There is no theoretical or empirical example of group selection that cannot be explained with kin selection.

The theoretical equivalence of kin selection models with those of the new group selection seems to be fairly widely recognized. Wilson and Wilson (2007) seem to agree, saying:

The theories that were originally regarded as alternatives, such that one might be right and another wrong, are now seen as equivalent in the sense that they all correctly predict what evolves in the total population. They differ, however, in how they partition selection into component vectors along the way. The frameworks are largely intertranslatable and broadly overlap in the kinds of traits and population structures that they consider.

Formal models of "group selection" and "kin selection" are now widely regarded as producing the same results. Gardner and Grafen (2008) say:

group selection has already been incorporated into social evolution theory, and is found to be exactly equivalent to kin selection: the two approaches are simply different ways of describing the same evolutionary process and both lead to the prediction that individuals should maximize their inclusive fitness

Here's Gardner, West and Wild (2011):

it has long been understood that the kin selection and multilevel (group) selection approaches to social evolution are mathematically equivalent, and merely represent different partitions of the same evolutionary process (i.e. natural selection; Hamilton, 1975; Grafen, 1984, 2006a; Wade, 1985; Frank, 1986, 1995; Queller, 1992b; Rousset, 2004; Gardner et al. , 2007; Lehmann et al., 2007b; Gardner & Grafen, 2009). No model of multilevel selection has ever delivered a (correct) prediction that could not be reformulated in terms of kin selection – despite repeated claims to the contrary.

Kerr and Godfrey-Smith (2002) recommend switching between the two perspectives - saying:

we also argue that each type of model can have heuristic advantages over the other. Indeed, it can be positively useful to engage in a kind of back-and-forth switching between two different perspectives on the evolutionary role of groups. So the position we defend is a “gestalt-switching pluralism.”

Group selection enthusiast Samir Okasha endorsed equivalence in a 2010 editiorial titled Altruism researchers must cooperate writing:

Lastly, 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.

To his credit, group selection enthusiast David Sloane Wilson is now on the correct side in this debate. So is group selection enthusiast Peter Richerson and group selection enthusiast Michael Wade.

For naysayers in this area, see here.

References

• Marshall, J.A. (2011) Group selection and kin selection: formally equivalent approaches.
• Godfrey-Smith, Peter (2002) Gestalt-Switching and the Evolutionary Transitions
• West, Griffin and Gardner (2009) Social semantics: how useful has group selection been?
• West, S.A., Griffin, A.S. & Gardner, A. (2007) Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection.
• Gardner, A. and Grafen, A. (2008) Capturing the superorganism: a formal theory of group adaptation
• Lehmann, L (2007) Group selection and kin selection: Two concepts but one process
• Kohn, Marek (2008) Darwin 200: The needs of the many
• Traulsen, A. (2010) Mathematics of kin- and group-selection: formally equivalent?
• Leigh, E.G. Jr. (2010) The group selection controversy.
• Queller, David C. (2012) Two languages, one reality
• Queller, David C. (1992) Quantitative genetics, inclusive fitness, and group selection.
• Hamilton, W. D. (1975) Innate Social Aptitudes of Man: an Approach from Evolutionary Genetics
• David Sloane Wilson and E. O Wilson (2007) Rethinking the theoretical foundation of sociobiology.
• Grafen, Alan (2007) Natural Selection, Kin Selection and Group Selection.
• Johnson, Eric Michael (2012) The Good Fight.
• Wilson, David Sloan (2012) Clash of Paradigms: Why Proponents of Multilevel Selection Theory and Inclusive Fitness Theory Sometimes (But Not Always) Misunderstand Each Other
• Wilson, David Sloan (2012) Richard Dawkins, Edward O. Wilson, and the Consensus of the Many
• Wade, Michael J., Wilson, David Sloane, Goodnight, Charles, Taylor, Doug, Bar-Yam, Yaneer, de Aguiar, Marcus A. M., Stacey, Blake, Werfel, Justin, Hoelzer, Guy A., Brodie, Edmund D. III, Fields, Peter, Breden, Felix, Linksvayer, Timothy A., Fletcher, Jeffrey A., Richerson, Peter J., Bever, James D., Van Dyken, J. David and Zee, Peter (2009) Multilevel and kin selection in a connected world
• Bijma, P. and Aanen, D. K. (2009) Assortment, Hamilton's rule and multilevel selection.
• Breden, F. (1990) Partitioning of covariance as a method for studying kin selection.
• Wade, M. J. (1980) Kin selection: its components.
• Frank, S. A. (1994) Genetics of mutualism: the evolution of altruism between species
• Okasha, Samir (2010) Altruism researchers must cooperate

Group selection turns out to be kin selection

It was observed early on that most of the evidence that was cited as favouring group selection seemed to be explained rather well by kin selection.

Slime mold aggregation typically consisted of identical clones - the highest level of relatedness it is possible to get. The ant and termite families that group selection enthusiasts loved got a long list of nice quantitative predictions from kin selection theory. The evolution of chickens that supposedly counted as evidence for group selection was explained neatly by kin selection: the chickens were couped up with their close relatives.

It was argued that group selection was needed to explain cooperation between strangers who were not genetically related. However, this line of argument ignored cultural kin selection - much cooperation between strangers could be explained neatly in terms of shared memes - rather than shared genes.

There were other factors that explained cooperation too: including reciprocity, reputations, virtue signalling and the Allee effect. It seemed as though group selection was trying to take credit for the moves of other theories which were already well-established.

Was there anything group selection was needed for? Fortunately, this question now seems to have been answered...

The evolution of group selection

Group selection enthusiasts were dissatisfied with the consensus that group selection couldn't compete with individual-level selection. They counter-attacked in a number of ways, saying that:

• The insistence by critics on groups being disjoint was mistaken - groups could still be targets of selection even if they overlapped.

• Kin selection was actually a type of group selection - acting on family groups.
• Reciprocal altruism was actually a type of group selection - involving small groups of reciprocators.
• Some major evolutionary transitions showed group selection in action - today's organisms were once yesterday's groups.
• Group selection had firm mathematical foundations - in the form of the Price equation.
• Laboratory experiments on group selection showed that it was potentially a powerful force.

• There are circumstances where between-group migration was very low - for example with parasites and symbiotes that spent most of their time inside other organisms.

• Group selection explained altruism, religion, senescence, sexual recombination - etc.

They also pointed out that a number of criticisms that had been leveled at group selection were wrong:

• The idea that between-group variation would be destroyed by migration and/or within-group selection was wrong - since substantial between group variation could be observed empirically - for example in a species such as our own.

• The idea that groups are not replicators - and so aren't a valid "level of selection" - was bunk.
• The widespread 50:50 sex ratio was not an argument against group selection for that trait - group selection could easily favour a 50:50 sex ratio.

A number of these points seemed quite reasonable - however...

Enter George Price

One of the more significant developments in the early history of kin selection was the contribution of George Price. Price had read Hamilton's papers, and contributed a mathematical model of kin selection that proved superior to Hamilton. Hamilton had worked with the concept of shared genes. Price developed a largely-equivalent formulation based on correlations. Price's maths was better than Hamilton's - and it raised the possibility of spiteful behaviour.

Hamilton had predicted that close relatives would cooperate - since helping relatives helps copies of your genes inside them. Price pointed out that another way of helping your genes was killing off the least-closely related individuals in the population - that kin selection had an dark side: spite.

Spite was an interesting idea - but not a terribly practical one. The effort and risk involved in harming large numbers of non-relatives seemed highly unlikely to result in a payoff to the actor.

Price's equation allowed for a fairly simple derivation of Hamilton's rule. It was rather like the relationship between Newton's model and Einstein's. Price had a more general model that made almost all the same predictions as Hamilton's model - but handled a few extreme cases better.

However, Price's equation was to have other effects - besides its predictions about spite. Essentially Price modeled the effect of natural selection and persistence on the frequency of a trait in a population. It had two terms, one representing the persistence of the trait and the other representing the change caused by selection. It more-or-less ignored drift by dealing with expected values: stochastic forces would average out. Price had provided the logic of Universal Darwinism - and showed how the mathematics of selection could be applied to practically anything. Its generality reinforced the idea that blood relatedness was only one factor that could be responsible for trait correlations between generations. Many interpreted this to mean that the idea of "kin" was out - and that we needed a more general theory.

One of the things that the Price equation could be applied to was entire groups. You could split a population into groups (however you liked) and apply the Price equation to those groups. You could also apply the equation to individuals within those groups. That quickly led to a model of group selection. The change in frequency of a trait could be modeled as being divided into a component due to natural selection within groups, and a component due to natural selection between groups.

Price's maths could have led to a rapid reconciliation between kin selection and group selection proponents. However, that isn't quite what happened, as we will see.

References

• Gardner, A. (2008) The Price equation.
• Jones, James Holland (2008) Notes on the Price Equation
• Frank, Steven A. (2012) The Price Equation.
• Frank, Steven A. (1995) George Price's contributions to Evolutionary Genetics.
• Grafen, A. (2000) Developments of the Price equation and natural selection under uncertainty.

Kin selection and group selection: early rivals

The dust-up between kin selection and group selection began in 1964 with a paper by John Maynard Smith titled "Group Selection and Kin Selection". Maynard Smith wrote this after reading Hamilton's 1964 paper on the topic and delaying its publication. That caused some sour grapes - but we won't go into that story further here. The paper introduced and christened kin selection - and contrasted kin and group selection. Kin selection offered a promising explanation for altruism, while group selection seemed to have demanding prerequisites, and was probably not very significant. The paper established a pattern of thought on the topic that Maynard Smith would perpetuate throughout his career.

Hamilton wrote mostly about kin selection. Williams (1966) came out against group selection. Wilson (1975) promoted kin selection, and Dawkins (1976) was critical of group selection. Kin selection become popular, group selection became neglected and was believed to be an insignificant force.

Frank's 1998 book "Foundations of social evolution" barely mentions group selection. Alexander's "Darwinism and Human Affairs" (1979) says:

We can now say with conviction that Williams' argument against group selection was right.

Group selection was theoretically dubious, biologists seemed to rarely need to invoke it - and there wasn't any evidence for adaptations for the good of the group.

However, group selection refused to die quietly. Over the years its advocates became increasingly vocal in its defense. The "levels of selection" issue became one of the longest-running battles in evolutionary biology. The issue still seems to be alive and kicking in 2012.

An introduction

The term "kin selection" refers to a type of selection in which heritable elements increase in frequency by causing their bearers assist their relatives.

Genes coding for strategies favouring assisting relatives can spread in populations if the benefit to the relatives multiplied by a coefficient of relatedness is greater than the cost to the actor. This idea is formalised in Hamilton's equation: rB > C.

The theory of kin selection successfully models much of the apparently-altruistic behaviour in the world. It explains the love of mothers for their children. It shows that an individual-centric perspective on the natural world is incorrect - organisms are built to care about others besides themselves.

The theory of kin selection has roots dating back to Darwin, but it was first formalised by Hamilton in 1964. George Price contributed a slightly improved formalisation in the 1970s - which showed how kin selection could favour spite - as well as altruistic behavior.

Kin selection has been a tremendously productive theory. However in modern times much mud slinging against kin selection has taken place by advocates of a supposedly alternative theory of the evolution of social behaviour: group selection. Here we will attempt to set the record straight on the topic.