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How and why did Fair Meiosis evolve?

I can hardly think that it provided a fitness advantage to the individual carrying the mutation. Why would it? Or did it evolve through lineage selection? Or was it some kind of pre-existing characteristic of meiosis that have no energy cost and therefore never disappear?

UPDATE:

I call fair meiosis the process of meiosis in which each chromosome has an equal chance of transmission.

I'm trying to make my questions clearer.

Is there any selection pressure in favour of alleles causing a fair meiosis? If yes, why? It doesn't seem to me to provide any advantage to the individual carrying this allele.

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It would be helpful if you defined what you mean by 'Fair Meiosis'. –  MCM Aug 7 '13 at 19:49
    
I do not understand what you mean with the last sentence. –  fileunderwater Aug 7 '13 at 20:09
    
I think you mean 'segment of a chromosome' if a chromosome's missing that's usually fatal in animals! –  shigeta Aug 7 '13 at 22:59
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2 Answers 2

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There's a more meta-level discussion on meiosis, which is that there is an advantage for genes which can get themselves selected in meiosis more often would prosper. This is a prediction of the biologist Robert Trivers, working with Bill Hamilton in the late '60s, known also as the 'selfish gene'. In fact the reason the selfish gene theory was so successful was that selfish genes - individual genes which propagated to offspring more often than 50% of the time. The Dawkins book 'The Selfish Gene' discusses this whole idea and its ramifications in great detail.

So at different times in evolutionary history, its hard to imagine that meiosis was completely 'fair' (50/50% change of any segment of DNA being chosen). In fact its pretty clear from genetic analysis now that some longer segments of DNA tend to be transmitted in one piece, though overall its still felt that the propagation if 50% likely for any given segment.

Over the long run, its been shown, mostly through game theory, that honesty is the best and most profitable policy. The most famous of these experiments was the Prisoner's dilemma competition where all comers have been invited to submit computer programs which can either betray or cooperate. Overall cooperative programs with some safegaurds which punished cheaters win overall. Over time its been shown that systems tend to defend themselves from cheaters and that cooperation and 'fairness' do much better than mobs of cheaters running amok.

Cheaters and unfairness still continue to happen though - systems which are fair tend to invite in a small number of cheaters. Say what you will about the income tax as a system! there is variance over time as to how 'fair' a system can be.

Dawkins has even said he sometimes thinks he should have titled the 'selfish gene' something else instead: 'Nice Guys Finish First'. I doubt that the book would quite have done as well though... we all should be fair, but it doesn't seem to invite book sales.

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Thanks for your answer @shigeta. Now that I think of this question again, I think that something goes wrong in your answer. –  Remi.b Aug 12 '13 at 19:46
    
I think the use of game theory doesn't bring much explaination for the fair meiosis. Whatever the game, altruistic behaviour may evolve thanks to genetic relatedness (Hamilton) or reciprocity (Trivers). For both of them it is important that the behaviour is not expressed toward any random individual/unit (therefore you need population structure, recognition or whatever). But such non-random interaction is not possible for alleles (at least under the assumption of random mating). Moreover, one might argue that the concept of relatedness does not stand when looking at two alleles. Am I right? –  Remi.b Aug 12 '13 at 19:47
    
well the chromosome can be viewed as a highly structured community which plays a game every time it reproduces offspring. that's the formulation that game theory might use look at meiosis. there are other ways, but this is I think a common view now. –  shigeta Aug 13 '13 at 3:40
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I think that Fair meiosis (I assume that you are referring to that chromosomes have an equal chance of transmission) can be seen as a byproduct of recombination at meiosis, which makes every chromosome a mosaic of maternal and paternal chromosomes. Therefore, selection does not act on chromosomes as a single unit, and "unfair" meiosis becomes meaningless. The "value" of "fair meiosis" most likely lies in the adaptive value of recombination.

Addition: To expand on the value of recombination, it has been suggested that the specific value of recombination is to break up linkages and thereby prevent meiotic drive (Haig & Grafen 1991, also see Okasha 2006). Haig & Grafen 1991 also specifically discuss selection for recombination. For an interesting analogy between economy and fair meiosis (veil-of-ignorance vs fair meiosis) see Okasha. 2012. Okasha notes that:

In both, randomization is used to deprive self-interested agents (genes and individuals) of information about their identity, forcing them to adopt an impartial perspective.

In summary he also writes that:

A gene that distorts segregation in its favour can spread despite reducing its host’s fitness. This harms genes at unlinked loci, who are thus under selection to restore fair meiosis if they can. One effect of fair meiosis is to equalize the interests of all the genes, thus ensuring they work for the common good. One way of achieving this is to destroy linkage, given that segregation distortion typically involves linked genes working in concert.

Okasha's paper also has a nice and accessible description of the biological process, and of the selective forces that are operating to counterbalance meiotic drive/segregation disorders.

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Thanks @fileunderwater! I updated my question, hoping to make it more understandable. Does your answer mean that there is no selection in favour of fair meiosis (as fairness is an inveitable consequence of meiosis)? –  Remi.b Aug 7 '13 at 20:30
    
My point is that I think it is likely that the main "target" of selection is recombination, and that fair meiosis is a byproduct. However, I'm not a geneticist and there are maybe experiments showing selection for fair meiosis. Also, you should look into meiotic drive (preferential selection of certain gemetes), e.g. in sex-chromosomes; see plosbiology.org/article/… and annualreviews.org/doi/abs/10.1146/…. –  fileunderwater Aug 8 '13 at 8:24
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