DNA repair as the primary adaptive function of sex in bacteria and eukaryotes

The essential feature of sex common to both bacteria and eukaryotes is information exchange (recombination) between two genomic DNA molecules derived from different individuals. In bacteria a naturally occurring sexual process termed transformation is characterized by transfer of DNA from one bacterium to another, followed by recombination between the resident DNA and the incoming DNA. In eukaryotes, the sexual cycle involves recombination between paired DNA molecules (chromosomes) in which the two DNA molecules are derived from two different parents. This process occurs in diploid cells during meiosis, and is followed by formation of haploid gametes. The fusion of gametes from different individuals to generate diploid progeny completes the eukaryotic sexual cycle. DNA damage appears to be a fundamental problem for life. Here, we present evidence for the view that the enzymatic machinery for carrying out recombination, during transformation in bacteria and meiosis in eukaryotes, is an adaptation for DNA repair. Both bacterial and eukaryotic cells, generally, contain repair enzymes that are adept at removing DNA damages. However there are limits to the capability of cells during ordinary cell divisions to repair their DNA. Damages causing loss of information in both DNA strands (double-strand damages) are particularly difficult to handle since they require information from a second homologous chromosome. A repair process referred to as homologous recombinational repair (HRR) appears designed to carry out repair of such double-strand damages.Evidence is presented for the hypothesis that sexual processes (i.e. transformation in bacteria and meiosis in eukaryotes) are maintained as evolutionary adaptations to facilitate HRR. In bacteria and microbial eukaryotes the problem of DNA damages is particularly acute during periods of stress, especially oxidative stress. It is during such stressful conditions that sex (which facilitates HRR) tends to occur in these facultatively sexual organisms. In multicellular eukaryotes, meiosis facilitates HRR and appears to be designed to protect against damages to the DNA of gametes, thus minimizing infertility and defective progeny.Another consequence of recombination during sex is increased genetic variation among progeny. Increased variation appears to have significant consequences at the population level over the long-term and is sometimes considered the primary adaptive function of sex. However, we present evidence that the machinery for sexual recombination is maintained primarily by the strong short-term advantage of passing relatively undamaged DNA from one generation to the next. The genetic variation that is generated appears to be a byproduct of HRR.