The molecular basis of the evolution of sex

Traditionally, sexual reproduction has been explained as an adaptation for producing genetic variation through allelic recombination. Serious difficulties with this explanation have led many workers to conclude that the benefit of sex is a major unsolved problem in evolutionary biology. A recent informational approach to this problem has led to the view that the two fundamental aspects of sex, recombination and outcrossing, are adaptive responses to the two major sources of noise in transmitting genetic information, DNA damage and replication errors. We refer to this view as the repair hypothesis, to distinguish it from the traditional variation hypothesis. On the repair hypothesis, recombination is a process for repairing damaged DNA. In dealing with damage, recombination produces a form of informational noise, allelic recombination, as a by-product. Recombinational repair is the only repair process known which can overcome double-strand damages in DNA, and such damages are common in nature. Recombinational repair is prevalent from the simplest to the most complex organisms. It is effective against many different types of DNA-damaging agents, and, in particular, is highly efficient in overcoming double-strand damages. Current understanding of the mechanisms of recombination during meiosis suggests that meiosis is designed for repairing DNA. These considerations form the basis for the first part of the repair hypothesis, that recombination is an adaptation for dealing with DNA damage. The evolution of sex can be viewed as a continuum on the repair hypothesis. Sex is presumed to have arisen in primitive RNA-containing protocells whose sexual process was similar to that of recombinational repair in extent segmented, single-stranded RNA viruses, which are among the simplest known organisms. Although this early form of repair occurred by nonenzymatic reassortment of replicas of undamaged RNA segments, it evolved into enzyme-mediated breakage and exchange between long DNA molecules. As some lines of descent became more complex, their genome information increased, leading to increased vulnerability to mutation. The diploid stage of the sexual cycle, which was at first transient, became the predominant stage in some lines of descent because it allowed complementation, the masking of deleterious recessive mutations. Out-crossing, the second fundamental aspect of sex, is also maintained by the advantage of masking mutations. However, outcrossing can be abandoned in favor of parthenogenesis or selfing under conditions in which the costs of mating are very high.(ABSTRACT TRUNCATED AT 400 WORDS)