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Sunday, November 06, 2011

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The Selfish Chromosome: Why Sex Evolved
By Julian David O’Dea, PhD, Department of Health and Ageing, Canberra, ACT, Australia

The problem of why sex evolved in the first place and why it has been maintained in most higher organisms continues to puzzle biologists. Theories have tended to focus on the advantage of sex to the individual or to the population. Popular explanations focus on the advantage of genetic recombination (for example, in providing variation in an evolutionary contest with parasites) or on the usefulness of sex in removing deleterious mutations from the population.

This note proposes that sex evolved because it was (and is) to the advantage of genetic material (chromosomes, for example) to recombine with other genetic material, that is by way of amphimixis (sex). It is assumed that defective or low-quality genetic material (chromosomes, genes) has always been and still is a besetting problem. From the perspective of the “interests” of the bulk of the genetic material, it is desirable to be in an organism with as good quality a genome as possible. That is, as free of deleterious mutations and defective DNA as possible. Obviously such genetic material, in such an organism, will proliferate best.

An organism is likely to possess some lower quality genetic material. If it possessed a lot, it would not be viable. But even a viable organism is likely to have or acquire some substandard genetic material, either by inheritance or mutation or because a changing environment renders some of the genes ineffective or redundant.

What sex does is allow the genetic material in an organism to combine with new material. In most cases, there will be no net benefit, because the amount of deleterious genetic material in the new genome is likely to be, on average, the same as before sex. So, there is no net advantage to most of the genetic material from sex. However, in a substantial proportion of cases (25% in a typical example), the genetic material improves its situation after sex because the deleterious material is lost. The effect of this is to improve the quality of the genome and the organism will therefore proliferate, and the genetic material along with it.

This advantage is multiplied as sexual generations pass. There is a continual improvement, at least relative to asexual organisms which are less able to shed deleterious mutations.

In a single celled organism which proliferates primarily by mitosis, with intermittent meiotic events attendant on sex, any genetic material lost to the ill effects of sex causing the accumulation of deleterious mutations in some individuals will be more than offset by the advantages to the genetic material in cases where all the deleterious material is removed. In the latter cases, the selective advantage will accrue strongly as the organisms proliferate mitotically. In the case of multicellular organisms, there are typically abundant progeny to allow the advantages of really good combinations to accrue to the genetic material which is coding for amphimixis. Some progeny will be lost due to unfortunate genetic combinations, but this will likely be more than offset by the very good combinations produced, which will survive and proliferate exceptionally well (thereby favouring the genetic material itself).

An earlier version of this theory (O’Dea, 2006) was cited in Glansdorff et al. (2009) in the context of their proposal that sex evolved to remove exogenous DNA, in particular from horizontal gene transfer.

As an example, consider two cells, each of which is diploid. If one assumes that one of a (different) chromosome pair in each organism is defective in some way, sexual reproduction will result in no net change in 50% of cases. That is, the new organism which results from amphimixis will have the same number of defective chromosomes (one). In 25% of cases, it will have two, because it acquires both the defective chromosomes from the parental cells. But in 25% of cases, it will have no deleterious material. Such an organism (and its constituent genetic material) will be expected to proliferate exceptionally well, better than asexual organisms unable to readily expunge deleterious DNA from the genome. A similar calculation was provided in O’Dea (2006).

In conclusion, this proposal places the emphasis on the advantage of sex to the genetic material coding for sex, rather than to the individual organism or the population. The level of selection is at the genetic material itself; for example, the chromosomes will be the units of selection, a concept reflected in the title of this note.

References:

Glansdorff et al. (2009). The Conflict Between Horizontal Gene Transfer and the Safeguard of Identity: Origin of Meiotic Sexuality. Journal of Molecular Evolution 69: 470-480.

O’Dea (2006). Did Conflict Between Chromosomes Drive the Evolution of Sex? Calodema (Sydney, Australia) 8: 33-34.


More recent thoughts on the evolution of sex are here:

http://julianodea.blogspot.com.au/2012/10/more-thoughts-on-why-sex-evolved.html

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