Bacterial Solutions to the Problem of Sex

Primer " W hy sex? " is a question that has occupied the minds of evolutionary biologists for more than a century. The evolution of organisms that mix their genes during reproduction is considered one of the major transitions in evolution [1], because it fundamentally changed how genes are transmitted to the next generation. In asexual reproduction, offspring inherit a more or less unaltered genome from the parent. In sexual reproduction, genetic material is fi rst reduced in the gametes (sperm or ovaries) and then fused with that of another individual, before new offspring may develop. Sexual reproduction has led to the evolution of males and females with different and sometimes even opposing reproductive interests and behavior. The consequence of sex, which many evolutionary biologists think explains its existence, is the production of genetic variation by mixing genes from different individuals. Nineteenth-century German biologist August Weismann [2] was the fi rst to realize that sex can produce variation and that variation allows organisms to better respond to selection. Three models have since been proposed as general explanations for the advantages of sex by elaborating Weismann's idea: (i) sex facilitates adaptation to a novel environment by combining benefi cial gene variants, or alleles, from different genomes (Fisher-Muller (FM) model [3,4]); (ii) sex helps organisms stay adapted to existing environmental conditions by combining and effi ciently removing deleterious alleles (mutational deterministic (MD) model [5]); or—a combination of these two ideas—(iii) sex helps to liberate benefi cial alleles from linked deleterious alleles in the genome in which they arose (mutational load (ML) model [6,7]). Several recent laboratory evolution experiments have found support for Weismann's proposal that sex facilitates the response to selection [8]. However, distinguishing between the different models remains a challenge. In particular, it has been diffi cult to alter recombination without changing other variables that might confer a sex advantage, such as environmental conditions or non-neutral genetic markers. In one attempt to overcome these problems, Rice and Chippindale [7] smartly used genetic tools to construct synthetic chromosomes of the fruit fl y Drosophila melanogaster that could not recombine and hence evolved asexually. This trick allowed the authors to study the effect of recombination on the fate of an introduced benefi cial mutation without the obscuring effects of differences in initial fi tness or environmental conditions used to induce sex in some populations. In another recent attempt, Goddard et al. [9] constructed …