Origins of Eukaryotic Sexual Reproduction

Sexual reproduction is a nearly universal feature of eukaryotic organisms. Given its ubiquity and shared core features, sex is thought to have arisen once in the last common ancestor to all eukaryotes. Using the perspectives of molecular genetics and cell biology, we consider documented and hypothetical scenarios for the instantiation and evolution of meiosis, fertilization, sex determination, uniparental inheritance of organelle genomes, and speciation.The transition from prokaryote to protoeukaryote to the last eukaryotic common ancestor (LECA) entailed conservation, modification, and reconfiguration of preexisting genetic circuits via mutation, horizontal gene transfer (HGT), endosymbiosis, and selection, as detailed in previous articles of this collection. During the course of this evolutionary trajectory, the LECA became sexual, reassorting and recombining chromosomes in a process that entails regulated fusions of haploid gametes and diploid → haploid reductions via meiosis. That the LECA was sexual is no longer a matter of speculation/debate as evidence of sex, and of genes exclusively involved in meiosis, has been found in all of the major eukaryotic radiations (Brawley and Johnson 1992; Ramesh et al. 2005; Kobiyama et al. 2007; Malik et al. 2008; Phadke and Zufall 2009; Fritz-Laylin et al. 2010; Lahr et al. 2011; Peacock et al. 2011; Vanstechelman et al. 2013).We propose that the transition to a sexual LECA entailed four innovations: (1) alternation of ploidy via cell–cell fusion and meiosis; (2) mating-type regulation of cell–cell fusion via differentiation of complementary haploid gametes (isogametic and then anisogametic), a prelude to species-isolation mechanisms; (3) mating-type-regulated coupling of the diploid/meiotic state to the formation of adaptive diploid resting spores; and (4) mating-type-regulated transmission of organelle genomes. Our working assumption is that the protoeukaryote → LECA era featured numerous sexual experiments, most of which failed but some of which were incorporated, integrated, and modified. Therefore, this list is not intended to suggest a sequence of events; rather, the four innovations most likely coevolved in a parallel and disjointed fashion.Once these core sexual-cycle themes were in place, the evolution of eukaryotic sex has featured countless prezygotic and postzygotic variations, the outcome being the segregation of panmictic populations into distinct species with distinctive adaptations.For additional reviews on the evolution of sex, the interested reader is referred to Goodenough (1985), Dacks and Roger (1999), Schurko et al. (2009), Wilkins and Holliday (2009), Gross and Bhattacharya (2010), Lee et al. (2010), Perrin (2012), and Calo et al. (2013).