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.

... 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).

The Anatomy of a Fraud

[update: 12 May 2013] Robert Trivers added a page to his blog called Fraud at Rutgers and released the investigation report of the Research Advisory Board of Rutgers University. Nature published a news articles about the case. (HT to Jeremy Fox at Dynamic Ecology. See also this post by Jon F Wilkins at Lost in Transcription.)

[date: 5 Feb. 2013] Below is a Nature paper that has never been officially retracted, AFAIK, and is still cited. The re-analysis by Trivers et al. matches Fisher's famous re-analysis of Mendel's data. Trivers was one of the co-authors of the original paper, but he got suspicious, when one of his students could not repeat the results of the study given the data.

Just click through and make up your own mind.

Brown WM, Cronk L, Grochow K, Jacobson A, Liu CK, Popovic Z, Trivers R (2005) Dance reveals symmetry especially in young men. Nature 488: 1148-1150.
→ Cited 121 times according to Google Scholar at 05. Feb. 2013 (and counting).

Trivers R, Pallestis BG, Zaatari D (2009) The anatomy of a fraud. TPZ Publishing, Antioch, CA.

Here's an animation of an asymmetrical male dancer.

The Mousetrap Paradox

It might be useful to reformulate Behe's mouse trap ruse as a paradox, in order to reveal the absurdity of his conclusion. Remember, a paradox is an argument that seems to be correct but leads to an absurd conclusion.


1. Premise:
The flat snap mouse trap consists of five parts, each carrying a function that is necessary for the trap to catch mice: platform, striker (hammer), spring, holding bar (holds the striker in set position), catch (arrests the holding bar in set position and carries the bait).

Figure 2-2 from Behe (Darwin's Black Box, p. 46)

2. Premise:

If any of these parts is missing, the trap will not function as a trap (irreducibly complex). So far the argument is correct. 

3. Conclusion (absurd because it contradicts the historical evidence):

Hence the trap cannot have a precursor working with one part less.

4. Contrary evidence:

The direct precursor of current flat snap traps (the patent from which they all derived) had one part less and was working perfectly (catching mice, economic success story etc).

5. Resolution:

Maynard Smith (1958) on the advantage of sexual reproduction

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,

J. Huxley anticipated H.J. Muller by misinterpreting R.A. Fisher

R.A. Fisher (1932, The bearing of genetics on theories of evolution. Science Progress 27:273-287) published an address delivered before the Royal Society of Dublin, 31 January 1932. In it, he explained the inbreeding depression as due to the accumulation of recessive deleterious mutations in out-crossing species, which inbreeding will expose, and the lack of such a depression in naturally inbreeding species as due natural selection preventing such an accumulation. The context is the evolution of dominance and recessiveness and the purpose is explaining why some organisms experience inbreeding depression and others not. Here's the relevant passage:

"It is the habitual cross-pollination of the maize plant, when grown commercially for seed, that has permitted the accumulation of the great swarm of defects which are revealed by self-fertilisation. In species commonly self-fertilised such recessives would be quickly eliminated, and the habitual procedure in scientific maize improvement now lies in the selection of those self-fertilised lines which are most free from serious defects, and which, on crossing, do, in the first or second generation, outyield every commercial variety of maize obtainable.        The injury observed on close inbreeding is thus exposed in an entirely new light. It is not perpetual self-fertilisation, but the first few generations, and especially the first generation, that is dangerous. The inbred lines show no perceptible further deterioration after eight or ten generations. Moreover, it is not the racial potentialities that are injured, but only the individual expression of them. It is not the species, but the individual, which suffers. The various devices which exist in nature to ensure exogamy are not for the benefit of the species, for which, so to speak, Natural Selection cares nothing, but to ensure the well-being of the immediate progeny ; to guard them against the recessive defects, which may lie latent in their parents." Fisher (1932, p. 283)

Julian Huxley (1942, Evolution. The Modern Synthesis. Harper & Brothers Publishers) construed this as a mutation clearance argument for the maintenance of sex similar to Muller's Ratchet:

"In addition, as Fisher (1932) stresses, it [sexual reproduction] has a function to perform in relation to the deleterious nature of most mutations. For, by allowing recombination, it permits mutations to appear in homozygous form, and thus facilitates the elimination of the more deleterious. Elimination will be greater when the frequency of homozygosis is increased by inbreeding or self-fertilization." (Huxley 1942, p. 84)

I cannot help but feel that this is a misinterpretation of Fisher (1932), who wanted to explain why most organisms experience an inbreeding depression, while some did not, and not deploy an argument for the evolutionary maintenance of sex (not here anyway). Nevertheless, the misinterpretation was luckily in line with later reasoning by Muller (1964, The Relation of Recombination to Mutational Advance. Mutation Research 1:2-9).

P.S.: Muller does not cite Huxley, so we do not know whether Huxley's idea/misinterpretation had consequences. However, they knew each other personally. In 1915, Huxley hired Muller, then a student at Thomas Hunt Morgan's fly lab, as his assistant at the Rice Institute in Huston.

How a Kuhnian missed a crisis

According to George C. Williams (1975, Sex and Evolution. Princeton University Press, p. v) there has been a crisis simmering in evolutionary biology ever since the recognition of the paradox (anomaly) that sexual reproduction is the prevalent mode of reproduction in higher animals and plants although, all else equal, asexual mutants should gain an  immediate,  twofold reproductive advantage.
   From my student days,  perusing the primary literature in order to grasp the scientific issues, I only remembered that Michael T. Ghiselin (1974, The Economy of Nature and the Evolution of Sex. Univ. California Press) introduced his book with chapters on the history and philosophy of science showing that he was a dyed-in-the-wool Kuhnian. Therefore, on rereading his book with a historical interest recently, my expectation was that he would also have seen the paradox of sex and perceived a crisis.
   Alas, Ghiselin (1974) marched through the eras with such a wide gait, that he stepped over this major problem of his time.