A combinational theory for maintenance of sex

Abstract

Sexual reproduction implies high costs, but it is difficult to give evidence for evolutionary advantages that would explain the predominance of meiotic sex in eukaryotes. A combinational theory discussing evolution, maintenance and loss of sex may resolve the problem. The main function of sex is the restoration of DNA and consequently a higher quality of offspring. Recombination at meiosis evolved, perhaps, as a repair mechanism of DNA strand damages. This mechanism is most efficient for DNA restoration in multicellular eukaryotes, because the initial cell starts with a re-optimized genome, which is passed to all the daughter cells. Meiosis acts also as creator of variation in haploid stages, in which selection can purge most efficiently deleterious mutations. A prolonged diploid phase buffers the effects of deleterious recessive alleles as well as epigenetic defects and is thus optimal for prolonged growth periods. For complex multicellular organisms, the main advantage of sexuality is thus the alternation of diploid and haploid stages, combining advantages of both. A loss of sex is constrained by several, partly group-specific, developmental features. Hybridization may trigger shifts from sexual to asexual reproduction, but crossing barriers of the parental sexual species limit this process. For the concerted break-up of meiosis-outcrossing cycles plus silencing of secondary features, various group-specific changes in the regulatory system may be required. An establishment of asexuals requires special functional modifications and environmental opportunities. Costs for maintenance of meiotic sex are consequently lower than a shift to asexual reproduction.

Figure 1

Hypothetical outline of evolutionary history of sexual reproduction in eukaryotes. Steps towards obligate sexual reproduction (left column). Functional constraints and selective forces driving evolution from one step to the next (right column).

Figure 2

Scheme of potential advantages of sex in complex multicellular organisms. A haploid restoration phase of the genome alternates with a diploid duration phase, which is optimal for growth and cell differentiation. The advantage of regular sex is, thus, a qualitatively improved genome in the diploid phase, which is important for organisms with a high organic complexity (animals, vascular plants).

Figure 3

Three explanations for the observed phylogenetic distribution that asexuality is rare and scattered in the phylogeny of multicellular eukaryotes. White, sexual lineages; black, asexual lineages; A–G, extant taxa; 1–5, shifts from sexuality to asexuality. (a) Asexuals are short lived because of the accumulation of deleterious mutations and/or lower genetic variation; the model is contradicted by the existence of ancient asexuals (lineage A). (b) Asexuality is unstable because the shift back to obligate sexuality happens frequently (note that this model assumes equal extinction rates of asexuals and sexuals); empirical evidence for this model is scarce. (c) Shifts from sexuality to asexuality are most frequently triggered by interspecific hybridization (unsuccessful shifts marked by ‘†’); shifts to asexuality are rarely successful because of the divergence of sexual parents and functional constraints. Owing to unblocked speciation of sexuals, frequencies of asexuality remain low.