G.C. Williams and J. Maynard Smith conceived the maintenance of sexual reproduction differently

[This blog post was a mere comment on Sandwalk first, because I thought someone there was confused about the different conceptions of the cost of sex. See this thread, particularly towards the end. The following expands the comment, there, into its own blog post, here. But it just explicates the differences between two historically important conceptions of the cost of sex and does not pretend to offer a resolution. There's also an article here, that also does not pretend to offer a resolution of the paradox of sexual reproduction. But it describes how, despite their different conceptions of the issue, Williams and Maynard Smith were able to communicate with each other fruitfully and amicably. In fact, I find that rather amazing. Often, such situations tend to escalate into a useless dispute with both parties at cross-purpose. None of that ever happened. On the contrary, Williams and Maynard SMith were able to understand each other despite their different assumptions and advance the issue in a dialectic way rather than the contrarian fashion.]


George C. Williams
George Williams conceptualized the maintenance of sexual reproduction as a problem of selection within one species or population. He began by considering organisms that include both sexual and asexual modes of reproduction within their complex life-cycles, for example, aphids & rotifers or strawberries & corals. He conceived the cost of sexual reproduction as the cost of meiosis, that is, the cost of reducing the relatedness with the own offspring from r = 1 to r = 0.5, when these organisms meet the time or conditions for switching from asexual to sexual reproduction. With this kin-selection conception he took the maintenance of sexual reproduction as a problem of selection within a population. Herein, he disagreed with Maynard Smith: 

“I think that the primary disadvantage of sexual reproduction in relation to asexual is most fruitfully formulated as a paradox of kin selection—an organism devotes resources to the production and care of a more distant (r = 0.5) rather than a close (r = 1) relative. This formulation provides a number of advantages. In its focus on genes identical by descent, kin selection is genetically explicit and relates directly to evolution. Maynard Smith’s economic argument (resources wasted on males) makes it easy to overlook the fundamental distinction between (1) the evolutionary problem of sexual and asexual reproduction as alternative character states in a population, and (2) the purely ecological question of competition between a clone and a Mendelian population.” (Williams 1978, ‘Mysteries of sex and recombination. A review of The Evolution of Sex by John Maynard Smith.’ Quarterly Review of Biology 53: 287–289. Page 298)

“I believe that understanding has been hampered by failure to distinguish the ecological from the evolutionary problem of sexuality. In important ways, insights gained from conceptual or experimental comparisons of sexual populations and competing clones (the ecological problem) may mislead in relation to sexual and clonal reproduction as alternative processes in a population (the evolutionary question with which I am concerned here).” (Williams 1980, ‘Kin selection and the paradox of sexuality.’ In Sociobiology: Beyond nature/nurture? Ed. by G.W. Barlow and J. Silverberg. Boulder, CO: Westview: 371–384. Page 372)

The fact that William and Maynard Smith cut the cake differently gets obvious from the way in which Williams treated the maintenance of recombination as not the problem he was at all concerned with:

“I assume that observed chromosome numbers and crossover rates reflect the optimum compromise between maximizing whatever benefits there are in recombination, and minimizing recombinational load. Tighter linkage must reduce recombinational load, but it does nothing to alleviate the cost of meiosis.” (Williams 1975, Sex and Evolution, Princeton Univ. Press, p. 108)

That is, reducing replication-rate by fusing gametes is not alleviated by assuming, for example, a species with a genome consisting of one homologous pair of a giant chromosome and no crossing-over between this homologous pair. [Felsenstein and Yokoyama (1976) modelled this problem.] That would exclude recombination through segregating heterologous chromosomes as well as through crossing-over between homologous chromosomes, but it would not pay the cost of reducing r from 1 to 0.5, or the cost of males, or the cost of fusing gametes, or whatever you conceive the cost of sex to be.

John Maynard Smith
John Maynard Smith conceived the maintenance of high recombination rates (not sex) as a problem of within-population selection between alleles that increase and others that decrease recombination rates. [This differs from Williams's within-population problem of a species with a complex life-cycle and both sexual and asexual modes of reproduction within it.] He accepted Williams's criticism of group-selection arguments for this issue (what he called the "balance argument" of Williams). He agreed that this problem requires an immediate individual-level explanation. But he also maintained that the competition between a sexual population and a genetically isolated asexual clone is a case of between-population selection. At this level, he did allow for long-term or group selection to play some (limited) role.

Anyway, his distinction begins in the preface already:

"I am under no illusion that I have solved all the problems which I raise. Indeed, on the most fundamental question - the nature of the forces responsible for the maintenance of sexual reproduction and genetic recombination - my mind is not made up. On sex, the relative importance of group and individual selection is not easy to decide. On recombination, group selection can hardly play a significant role, but it is not clear to me whether the short-term selective forces I discuss are sufficient to account for the facts, or whether models of a qualitatively different kind are needed." (Maynard Smith 1978, The Evolution of Sex, Cambridge Univ. Press, p. ix)

"It may help to classify the various theories; first, according to the time scale on which selection is supposed to act, and then according to the 'unit of selection' - population, individual, or gene." (Maynard Smith 1978, p. 1)

"I do not find it possible to give an unequivocal answer concerning the role of group selection in the maintenance of sexual reproduction. It has played some role, as evidenced by the taxonomic distribution of parthenogens; but it is not the only relevant force, as will be apparent from the review of the balance argument in Chapter 4, section E. But, whatever one may think of the role of group selection in the maintenance of sex, it cannot explain how it started, and it cannot explain the maintenance of high levels of genetic recombination within sexual populations." (Maynard Smith 1978, p. 6)

And so throughout the book. Maynard Smith consistently distinguishes the maintenance of sexual reproduction from that of recombination, the former being an issue of selection between isolated populations and clones, the latter being one of selection between alleles within one population.

Maynard Smith's support for "some role" of long-term or group selection in the maintenance of sex (not recombination) was also defending his earlier publication from 1958 (The Theory of Evolution, Penguin Books, pp. 138-139). It is often forgotten in potted histories about the paradox of sex, that Maynard Smith did already clearly state the cost of males in this early pop-science writing and also embraced the long-term group-selection explanation of the maintenance of sex.

"If the rate of increase of an animal population were limited by the number of eggs which each female could lay, which in turn depended on how much food a female could eat and transform into eggs, then a population consisting entirely of parthenogenetic females would increase twice as fast as would a population of equal numbers of males and females. From the point of view of reproduction, males are a waste of living material. (This argument does not hold for hermaphroditic organisms, or for those animals in which both parents help to feed the young.)      The compensating advantage of the sexual process is that it increases the range of potential variation in a population, and therefore, its evolutionary plasticity." (Maynard Smith 1958, p. 138)

"Thus the sexual process is a means of ensuring evolutionary plasticity at the expense of interfering with reproduction. [...] Now if the advantage of sexual reproduction is that it increases the range of potential variation in a population, then the advantage refers to the population as a whole, and not to any particular individual in it. It follows that sexual reproduction has been established as a rule, both in animals and plants, because selection has favoured some populations at the expense of others. This forms a contrast to the the examples discussed in the last chapter, in which the 'unit' selected was the individual and not the population." (Maynard Smith 1958, p. 139)

By the way, Ghiselin (1988, p. 16, in Michod & Levin (eds): The Evolution of Sex), reminisced an instance of Williams reviewing one of his papers and telling him about the twofold cost of sex and that he [Williams] had found it in a book by Maynard Smith (1966), which must have been the second edition of the above quoted Penguin book by Maynard Smith (see also Dagg 2016, On recognising the paradox of sex. Philosophy, Theory, and Practice in Biology. DOI: 10.3998/ptb.6959004.0008.003).

The fact that John Maynard Smith never changed his mind about his hedged support for some role of group (between-population) selection in the maintenance of sex is clear from an interview of Richard Dawkins with John Maynard Smith in 1997 (deposited at the Web of Stories in 2008).  

The maintenance of sex and group selection

It is often forgotten that John Maynard Smith was not categorically against group or species selection. In fact, he admitted a role of it in the maintenance of sexual reproduction:

"I do think that the maintenance of sex is a context in which group selection, selection between species, has actually been important." Web of Stories, John Maynard Smith 65 - Explaining the maintenance of sex.

Kin selection as correlated selection

Steven Frank ("Natural selection. VII. History and interpretation of kin selection theory." Journal of Evolutionary Biology 26, in press) sorts out kin selection, group selection, inclusive fitness, direct fitness and all that. While he lucidly explains how correlated selection subsumes all the above concepts as special cases, including genetic relation as one cause of correlation, he stops short of calling the general theory correlated selection. That's because he's interested in understanding the underlying processes and not in squabbling about labels.

Of particular interest to those who followed the recent kerfuffle about a paper by Nowak et al. (2010 "The evolution of eusociality." Nature 466: 1057-1062) will be the following comments revealing a position between the quarreling parties:

"In my view, inclusive fitness has become as much a hindrance as an aid to understanding. I am not saying that inclusive fitness is wrong. Inclusive fitness does provide significant insight into a wide variety of problems. But one must know exactly its limitations, otherwise trouble is inevitable. Realistic biological scenarios arise for which inclusive fitness is important but not sufficient. When one does not clearly recognize the boundaries then, when faced with a solution for which inclusive fitness is not sufficient, it becomes too common to conclude that inclusive fitness and all broader approaches to kin selection analysis fail entirely, and one must discard the whole theory." Frank (in press, p. 21) 

Clearly, Frank is not on the side of those defending inclusive fitness as the general theory with kin and group selection as special cases. He even favors the direct fitness approach. At the same time, however, the statement about throwing out the baby with the bath water (last sentence in above quote) is a criticism of Nowak et al. (2010). Here's another quote showing how Frank conceives the relation between direct and inclusive fitness:

"Direct fitness typically provides a clear and complete analysis, and subsumes inclusive fitness as a special case. Inclusive fitness does have the benefit of an intuitively appealing causal perspective. However, inclusive fitness is more limited and more likely to cause confusion. As understanding of a subject develops, it is natural for yesterday’s general under- standing to become today’s special case." Frank (in press, p. 22)

By the way, Frank sees group selection as equally hindering understanding (p. 23 onwards).

In summary, this could clear up some of the mess around the group/kin selection controversy, but it is confusing that Frank uses the term kin selection as a label for the general theory that comprises all the special cases. After all, kin implies genetic relationship and he clearly does not want to see the theory limited in that way. I'd favor correlated selection as a neutral alternative term.

... the phoenix of the species ...

In a comprehensive review of what was known about the evolution of sex at that time Patrick Geddes and J. Arthur Thomson (1889. The Evolution of Sex. London: Walter Scott) concluded a chapter with this poetic statement:

"Sexual union in those infusorians, dangerous perhaps for the individual life,—a loss of time so far as immediate multiplication is concerned,—is in a new sense necessary for the species. The life runs in cycles of asexual division, which are strictly limited. Conjugation with unrelated forms must occur, else the whole life ebbs. Without it, the Protozoa, which some have called "immortal," die a natural death. Conjugation is the necessary condition of their eternal youth and immortality. Even at this low level, only through the fire of love can the phoenix of the species renew its youth." Geddes, and Thomson (1889, p. 166). 

This is a rejuvenation hypothesis framed in terms of the benefit of the species. The hypothesis is itself being rejuvenated in terms of individual advantages, for example, in Turke (2013. "Making Young from Old: How is Sex Designed to Help?" Evolutionary Biology, in press).

Maynard Smith (1958) on the advantage of sexual reproduction

[Update 15.07.2017: See also this article on the history of the making of the paradox of sex by George C. Williams and John Maynard Smith including evidence from their correspondence: Joachim L. Dagg (2016) On recognising the paradox of sex. Philosophy and Theory in Biology 8: e703.]

Sometime in the late 1950s it dawned on evolutionary biologists that their explanation for the evolutionary advantage of sex implied group selection, but that was not yet seen as an anomaly. One record of this awakening to the implication stems from R. A. Fisher (1958[1999]). Another particularly lucid passage comes from The Theory of Evolution by John Maynard Smith. He first describes the cost of sex as halving the rate of increase of a population and then describes the advantage of sex as more than doubling a population's range of potential variation (Maynard Smith 1958, p. 138f).

"If the rate of increase of an animal population were limited by the number of eggs which each female could lay, which in turn depended on how much food a female could eat and transform into eggs, then a population consisting entirely of parthenogenetic females would increase twice as fast as would a population of equal numbers of males and females. From the point of view of reproduction, males are a waste of living material. (This argument does not hold for hermaphroditic organisms, or for those animals in which both parents help to feed the young.)     The compensating advantage of the sexual process is that it increases the range of potential variation in a population, and therefore its evolutionary plasticity." Maynard Smith (1958, p. 138)

He adds a numerical example showing that 10 mutations would yield only ten variant genotypes in an asexual population but 3^10 in a sexual one, because each mutation will yield three genotypes AA, Aa and aa. Maynard Smith is aware that seeing the advantage of sex in increasing population plasticity implies group selection,

A very short history of evolutionary maintenance problems

The following serves to show that even an abridged history does not need to gloss over differences, here, between what was thought about the relation between sexual reproduction and heritable variation at different times.

1. Darwin's problem
How could heritable variation in fitness relevant traits (which is a prerequisite for natural selection) be maintained, if sexual reproduction halved it every generation because of blending inheritance (Jenkin 1867, 158)? The remedy, here, was the inheritance of acquired variation via Pangenesis, that is, a Lamarckian source of variation in fitness relevant traits.

2. Weismann's solution
[slightly extended because Weismann's is often regarded as identical with later views]
Weismann rejected the inheritance of acquired variation. He saluted Nägeli's idioplasm, a concept of the minute molecular structure of the basis of life, but rejected the internal self-changing force that Nägeli thought this idioplasm must have.

"Nägeli has very ingeniously worked out his conception of idioplasm, and this conception is certainly an important acquisition and one that will last, although without the special meaning given to it by its author. [...] The only proof that idioplasm must necessarily change, in the course of time, as the result of its own structure, is to be found in the fact that Nägeli has so constructed it; and no one will doubt that the structure of idioplasm might have been so conceived as to render any transformation from within itself entirely impossible."  (Weismann 1886; translated in Weismann 1891, p. 264; see also Appendix I, pp. 306-308)

Indeed, Nägeli's idioplasm minus the internal force of change is nothing but Weismann's germ-plasm.

"The germ-plasm or idioplasm of the germ-cell (if this latter term be preferred) certainly possesses an exceedingly complex minute structure, but it is nevertheless a substance of extreme stability, for it absorbs nourishment and grows enormously without the least change in its complex molecular structure." (Weismann 1891, p. 278)

These rejections posed two problems for Weismann. Firstly, heritable variation could not enter the germ-plasm via the inheritance of acquired differences. Secondly, it could neither emerge from an internal self-changing force of the germ-plasm. Therefore the problem of the maintenance of heritable variation in fitness came back to him with a vengeance. Where do heritable variations come from?

"We are clearly compelled to find some other source of hereditary individual differences, or the theory of natural selection would collapse, as it would if hereditary individual variations did not exist." (Weismann 1891, p. 274)

Fortunately, Weismann's non-blending conception of inheritance also pointed a way out. Without blending inheritance he could regarded sexual reproduction as the source of heritable variation in fitness.

"I believe that such a source is to be looked for in the form of reproduction by which the great majority of existing organisms are propagated: viz. in sexual, or, as Häckel calls it, amphigonic reproduction." (Weismann 1891, p. 279)

Sex was no longer the problem but the solution.

3. Fisher's & Muller's theory
Fisher (1930) and Muller (1932) knew that the ultimate source of variation was mutation, and they explicitly rejected Weismann's idea of recombination as the ultimate source. In their theories, sexual recombination accelerates adaptation in an arms race between asexual and sexual populations.

4. Maynard Smith's & Williams's paradox: Fisher's and Muller's theory implies a benefit of sex to species not individuals. Their theory could not be accepted and group selection be rejected at the same time.

• Fisher, Ronald A. [1930] 1999. The genetical theory of natural selection, a complete variorum edition. Edited by Henry Bennett. Oxford: The Claredon Press.
• Jenkin, Fleeming. 1867. “Art. I.—The origin of species.” The North British Review, June, 46:149-171. [http://archive.org/details/northbritishrev24unkngoog]
• Maynard Smith, John. 1978. The evolution of sex. Cambridge: Cambridge University Press.
• Muller, Hermann J. 1932. “Some genetic aspects of sex.” The American Naturalist 66:118-138.
• Weismann, August. 1886. Die Bedeutung der sexuellen Fortfplanzung für die Selektions-Theorie. Jena: G. Fischer. In translation:  Weismann A (1891) The significance of sexual reproduction in the theory of natural selection. Pp. 257-342 in: Poulton EB, Schönland S, and Shipley AE (eds)) Essays upon Heredity and kindered Biological Problems. Authorised translation, second edition. Claredon Press, Oxford.
• Williams, George C. 1975. Sex and evolution. Princeton: Princeton University Press.

Pollock on Wynne-Edwards [updated]

Gregory B. Pollock (1989, p. 205) construed the criticism against Wynne-Edwards as follows:

“Critique of Wynne-Edwards’ view on population regulation and sociality suppose a population of discrete, mutually exclusive groups essential to his thought. Yet both his past and present work focus on continually distributed, philopartric populations; his critics have argued the untenability of a position never his own.”

As I understood the criticism of Maynard Smith (1964), he did not claim that Wynne-Edwards (1962, 1963) assumed strict isolation of breeding groups, but that the sort of group selection he supposed would require such isolation in order to prevent cheats from undermining the group benefit.^* 

Wright (1945) on group selection

According to David Sloan Wilson (1983, p. 163ff) Sewall Wright proposed a group selection model in a review of Simpson's book Tempo and Mode in Evolution. While it is true that Wright proposed a model for the spread of a gene for altruism in a population, it differs from later multilevel selection models in its reliance on drift.

"Thus the socially favorable mutation A₂ tends to be lost or nearly lost in a random breeding population. In a population divided into many small, completely isolated groups, selection becomes reduced in efficiency as drift due to accidents of sampling increases. A₂ may occasionally drift into fixation in a local group but cannot spread in the absence of migration." (Wright 1945, p. 417)

Groups that drifted to fix altruism can provide more migrants to the population pool than other groups of equal size. Nevertheless, within-group selection against altruism is suppressed by within-group drift, and between-group variation can then become significant. In later multilevel selection models, within-group selection is swamped statistically by differences in average fitness between groups and drift does not feature. 

For an example of later multilevel selection theory, the trait-group model of DS Wilson (1975. "A theory of group selection." PNAS 72:143-146) ignores drift within groups, lets the selfish individuals win within-group selection, but has them overwhelmed by variance in the average fitness between groups (given a cycle of groups dissolving in a panmixis and randomly re-forming from that panmictic population).

So I really see a difference between Wright’s model, where within-group drift and between-group migration rates work towards the same end, and MLS models where between-group statistics overwhelm within-group determinism.

• Wilson DS (1983) The group selection controversy: history and current status. Annual Review of Ecology and Systematics 14: 159-187.
• Wright S (1945) Tempo and Mode in Evolution: a critical review. Ecology 26:415-419. [see also the reprint in: Provine WB (ed) Evolution: selected papers. University of Chicago Press, pp. 395-399.]

Price's accommodation

I just finished "The Price of Altruism" by Oren Harman. It is a biography of one of the most important, original, and - er - weird evolutionary biologists of the 20th century, George Price.

I just wanted to remind those who now wage war on accomodationists that Price was - temporarily - a Christian whose fundamentalism even appalled Henry Morris, the Texan founder of the Creation Research Science Center.

Hamilton on group/kin selection

A paper by W.D. Hamilton called "Innate Social Aptitudes of Man: an approach from evolutionary genetics" has been originally published in 1975 by editor Robin Fox (Biosocial Anthropology. London: Malaby Press, pp. 133-153) and has been reprinted in W. D. Hamilton (1996. Narrow Roads of Gene Land. Oxford: W.H. Freeman, pp. 329-351). It has been cited for very different reasons. 

On the one hand, Robert Trivers has called it Hamilton's "fascist paper" thus mocking the shocked reactions of some anthropologists to the paper. These reactions turned against the part of the paper headed "Tribal Facies of Social Behaviour," where Hamilton tried to draw conclusions from his modelling for human behaviour and argued that morally bad streaks from xenophobia to warfare may have a genetic basis that can be positively selected in a group structured species. For example:

"It has been argued that warfare must be a pathological development in humans, continually countered by natural selection, and this claim is sometimes based on a sweeping a priori view that habits of mortal intraspecific fighting must always endanger the survival of a species. [reference to Lorenz 1966. On Aggression.] While endorsing such a view as regards wars between the few frightfully armed superpowers of today, I see no likelihood for it as regards fighting of individuals or of groups up to the level of small nations. Of course, for the species as a whole, and in the short term, war is detrimental from the biological demographic point of view, but, as shown above and elsewhere, detriment to the species does not mean that a genetical proclivity will not spread. Anyway, what is bad at one level may be good at another and the cost to the species may by paid in the long run. The gross inefficiency of warfare may be just what is necessary, or at least an alternative to birth control and infanticide, in order to spare a population's less resilient resources from dangerous exploitation. Maybe if the mammoth-hunters had attacked each other more and the mammoths less they could be mammoth-hunters still." (Hamilton 1975, see also 1996, p. 334f)

Later citations were less shocked about or interested in the stark conclusions at the end of the paper and centered on the earlier parts of the paper, for example, the following passage:

"Returning to the problem of units of selection, Darwin himself, vague about the process of heredity, based most of his arguments on considerations of the fitness of individuals. He made occasional exceptions, as for the social insects where he treated the 'family group' as the unit of selection. I believe even these limited concessions were incautious (Hamilton 1972), and value his judgement more where, discussing the evolution of courage and self-sacrifice in man, he left a difficulty apparent and unresolved. He saw that such traits would naturally be counter-selected within a social group whereas in competition between groups the groups with the most of such qualities would be the ones best fitted to survive and increase. This open problem which Darwin left is really the starting-point of my own argument, but it is historically interesting to note that after some initial wavering between the calls of Spencer, Kropotkin, and others, almost the whole field of biology stampeded in the direction where Darwin had gone circumspectly or not at all." (Hamilton 1975, p. 134f; see also 1996, p. 330f)

[The passages that Hamilton refers to, where Darwin speculated about the good of the insect community or about between-tribe selection, can be found here.] 

In The Extended Phenotype, Richard Dawkins (1983, p. 6) quoted the last sentence with the stampede metaphor to suggest that Hamilton rejected group selection. 

More recently, still, the same paper has been cited as evidence that, with the help of the Price equation, Hamilton reconsidered and eventually accepted group selection as a live possibility (e.g. Sober and Wilson 1998, p. 71ff; Segerstrale 2000, p. 53ff).

IMHO, Hamilton best explained his conception of the relation between group selection, kin selection, and inclusive fitness in the following passage:

"The usefulness of the 'inclusive fitness' approach to social behaviour (i.e. an approach using criteria like (b_ABK - k) > 0) is that it is more general than the 'group selection', 'kin selection', or 'reciprocal altruism' approaches and so provides an overview even where regression coefficients and fitness effects are not easy to estimate or specify. As against 'group selection' it provides a useful conceptual tool where no grouping is apparent—for example, it can deal with an ungrouped viscous population where, owing to restricted migration, an individual's normal neighbours and interactants tend to be his genetical kindred.    

Because of the way it was first explained, the approach using inclusive fitness has often been identified with 'kin selection' and presented strictly as an alternative to 'group selection' as a way of establishing altruistic social behaviour by natural selection (e.g. Maynard Smith 1964; Lewontin 1970). But the foregoing discussion shows that kinship should be considered just one way of getting positive regression of genotype in the recipient, and that it is this positive regression that is vitally necessary for altruism. Thus the inclusive-fitness concept is more general than ‘kin selection’.” (Hamilton 1975, p. 140f; see also 1996, p. 336f)

Hamilton's hierarchy of concepts seems to be:

general theory: inclusive fitness
   special cases: group selection, kin selection, reciprocity, etc.

But it seems to be significant that, in drawing conclusions from his new insight into the real possibility that between-group selection can override within-group selection in structured populations, he emphasized the dark side of between-group xenophobia or warfare rather than the good side of within-group altruism or sacrifice. That emphasis differs strongly from the one of some proponents of group selection, who seem to consider it the cause for moral goodness.

P.S.: Admittedly, I have myself not distinguished between kin selection and inclusive fitness in the post Darwin on kin/group selection. Other possible conceptions of what is the general and what the special case seem to be in the fray. For example, inclusive fitness and multilevel selection are now often regarded as equally general theories and equally legitimate perspectives on the same problem.


References

• Dawkins R (1983) The extended phenotype. Oxford Univ. Press.
• Hamilton WD (1972) Altruism and related phenomena, mainly in social insects. Ann. Rev. Ecol. Syst. 3:193-232.
• Hamilton WD (1975) Innate social aptitudes of man: an approach from evolutionary genetics. In: R. Fox (ed) Biosocial Anthropology. John Wiley & Sons, pp. 133-155.
• Hamilton WD (1996) Narrow roads of gene land, vol. 1. W.H. Freeman, Spektrum.
• Lewontin RC (1970) The units of selection. Ann. Rev. Ecol. Syst. 1: 1-18.
• Maynard Smith J (1964) Group selection and kin selection. NAture 201: 1145-47.
• Segerstrale U (2000) Defenders of the truth. Oxford Univ. Press
• Sober E, Wilson DS (1998) Unto others. Harvard Univ. Press.

Darwin on group/kin selection

Evolutionary biologists, who regard group selection as one big fallacy, tend to retrospectively (whiggish?) interpret Charles Darwin’s statements touching on the issue as groping towards kin selection and inclusive fitness theory. Other evolutionary biologists, however, think that group selection is multilevel selection applied to one particular tier of the natural hierarchy and therefore a correct proposal. These scholars tend to retrospectively interpret the same statements of Darwin as groping towards multilevel selection theory.

The following gives the major quotes I could find in my copies of Darwin and the contrary interpretations of them: Darwin a staunch individualist vs. Darwin the inventor of multilevel selection theory.

What did Wynne-Edwards (1962) actually propose?

A current distinction
A widespread distinction in multilevel selection theory is between two different scenarios. The scenarios could be conceived as extremes of a continuous range of possible scenarios. The scenarios are commonly referred to as multilevel selection 1 and multilevel selection 2 or MLS1 and MLS2 (Damuth and Heisler 1988; Okasha 2006).
    In MLS1 the particle is the focal level and the collective is part of the environment. That is, the collective gets no component of fitness in its own right but population structure and dynamics influence the fitness of particles in important ways that should not be ignored. In MLS2 the collective gets its own component of fitness. That is, collectives beget collectives and have some heritable variance in collective fitness.
    In the extreme case the particles, for example, cells of a body, lose their component of fitness entirely to the collective, the organism (Michod 2005). At this point the question of evolutionary transitions from the MLS1 to the MLS2 regularly arises, but I am not interested in the transitions question here.

Wynne-Edwards regarded groups as a third level of selection - not second.

What exactly got rejected when group selection got rejected in the 1960s? The abridged history that is now standard suggests that Vero C. Wynne-Edwards (1962) specified a previously amorphous reasoning for the good of species or groups and thereby paved the way to its explicit rejection.

“It was this vague good-for-the-species formulation that Wynne-Edwards tried to put on more solid ground with his 1962 book Animal Dispersion in Relation to Social Behaviour.” (Segerstrale 2000, p. 55)

I recently came across the following statement by Wynne-Edwards, which made me pause and wonder whether something got lost by potting history:

“1.5. Social evolution and group-selection

It is part of our Darwinian heritage to accept the view that natural selection operates largely or entirely at two levels, discriminating on the one hand in favour of individuals that are better adapted and consequently leave more surviving progeny than their fellows; and on the other hand between one species and another where their interests overlap and conflict, and where one proves more efficient in making a living than the other. Selection at the individual level is often designated as intraspecific, and that at the higher level interspecific. The latter covers a broad range of relationships; it is frequently concerned not so much with ecological overlap between closely allied species in the same genus as with the mutually conflicting needs of two independent predators seeking the same prey, or two unrelated contestants for the same micro-habitat.

Neither of these two categories of selection would be at all effective in eliciting the kind of social adaptations that concern us here." (Wynne-Edwards 1962, p. 18).

Apparently, Wynne-Edwards took two levels of selection, individual and species, as well established within Darwinism and thought he introduced a third level in between. In retrospective, of course, that does not matter because all higher levels of selection got degraded in the 1960s.

P.S.: Mark E. Borrello (2010) provides a nuanced account recommended to anybody interested in this history of the group selection controversy.

References

• Borrello ME (2010) Evolutionary Restraints. University of Chicago Press, Chicago
•  Segerstrale U (2000) Defenders of the truth. Oxford University Press, Oxford
•  Wynne-Edwards VC (1962) Animal Dispersion. Oliver and Boyd, Edinbourgh

False dating of Fisher on the 'benefit of species'

The earliest backdating of Fisher’s statement about sexual reproduction being due to group selection I have come across is from James F. Crow and Motoo Kimura:

“Fisher (1930) goes so far as to suggest that sexuality may be the only character that evolved for species rather than for individual advantage.” (Crow & Kimura 1965, p. 448)

John Maynard Smith opens his response to Crow & Kimura (1965) as follows:

“It was argued by Fisher (1930) that sexual reproduction is the only characteristic of living organisms which owes its presence to the fact that it favors the survival of groups rather than of individuals.” (Maynard Smith 1968, p. 469)