Genetic and genomic evolution of sexual reproduction: echoes from LECA to the fungal kingdom

Abstract

Sexual reproduction is vastly diverse and yet highly conserved across the eukaryotic domain. This ubiquity suggests that the last eukaryotic common ancestor (LECA) was sexual. It is hypothesized that several critical processes in sexual reproduction, including cell fusion and meiosis, were acquired during the evolution from the first eukaryotic common ancestor (FECA) to the sexual LECA. However, it is challenging to delineate the exact origin and evolution of sexual reproduction given that both FECA and LECA are extinct. Studies of diverse eukaryotes have helped to shed light on this sexual evolutionary trajectory, revealing that a primordial sexual ploidy cycle likely involved endoreplication followed by concerted chromosome loss and that cell-cell fusion, meiosis, and sex determination later arose to shape modern sexual reproduction. Despite the general conservation of sexual reproduction processes throughout eukaryotes, modern sexual cycles are immensely diverse and complex. This diversity and complexity has become readily apparent in the fungal kingdom with the recent rapid expansion of whole-genome sequencing. This abundance of data, the variety of genetic tools available to manipulate and characterize fungi, and the thorough characterization of many fungal sexual cycles make the fungal kingdom an excellent forum, in which to study the conservation and diversification of sexual reproduction.

Figure 1.. Evolution of sexual reproduction.

Evolution of sexual reproduction from the asexual first eukaryotic common ancestor (FECA) to the sexual last eukaryotic common ancestor (LECA) includes three major innovations: cell-cell fusion, meiosis, and sex. Depending on when cell fusion and sex were acquired, LECA can be either sexual (model A) or unisexual (model B). Evolution of fusogens, meiotic cycles, meiotic drivers, karyotypes, genomes, and epigenetic regulations drive the diversification of modern sexual reproduction in eukaryotes.