Origins of Eukaryotic Sexual Reproduction

Abstract

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 genome of an Encephalitozoon cuniculi type III strain reveals insights into the genetic diversity and mode of reproduction of a ubiquitous vertebrate pathogen

“…One of these could be mitotic recombination, as this known asexual driver of genome homogenization in many microbial eukaryotes, including many pathogens (Butler et al, 2009;Cuomo et al, 2012;Rosenblum et al, 2013), has been shown to increase in frequency in the absence of a functional Spo11 (Lario et al, 2015;Sun and Heitman, 2015). As a sexual alternative, ECIII-L could undergo meiosis without the need for Spo11, a situation that would be analogous to what is seen in the distant microbial lineage Dyctiostelium sp (Goodenough and Heitman, 2014), or perhaps, the SNP we identified is too recent to have impacted the genome of ECIII-L in significant ways (that is, EcIII-L has always been a 'selfer', and the recent Spo11 mutation we found will only affect the mutational patterns of ECIII-L down the road). Indeed, besides the one SNP we report, and the rest of Spo11 in ECIII-L is completely identical to other isolates, suggesting that this frameshift is recent.…”

What can we infer about the origin of sex in early eukaryotes?

“…However, recent insights make it more and more likely that the basic meiotic cycle appeared upon the formation of the first eukaryote [1]. A highly insightful hypothetical reconstruction of the origins of eukaryotic sexual reproduction from humble (archaeal) beginnings is given by Goodenough and Heitman [2]. Complete meiotic sex is characterized by four separate, but interlocking, mechanisms that, as such, are already rather complex.…”

“…For a lot of pertinent mechanisms, we can readily envisage how they probably evolved from prokaryotic forerunners [2]. A hyperthermophilic archaeon species displays cell-cell fusion [8].…”

“…But, in every case, some prokaryotic factors and/or processes can be identified as evolutionary precursors. The processes involved are as follows: (i) Ploidy alterations: increases via cellular fusion processes and reductions via meiosis; (ii) cell -cell fusion regulation, which started out with the fusion of similar cell types (isogamous fusion) and later became anisogamous; (iii and iv) coupling mating-type allele regulation to (differential) organelle transmission and to (adaptive) spore formation [2]. In (archezoan) theories that postulated eukaryotic evolution prior to endosymbiont entry, organelle transmission was seen as a later addition to a fully operational meiotic mechanism, but nowadays meiotic sex is seen as one of the set of processes that probably arose in reaction to endosymbiont entry [3].…”

Understanding diversity in telomere dynamics

“…The factors driving the evolution of linear chromosomes are not fully understood, but they are probably tied to the evolution of sexual reproduction. Sexual reproduction, which is nearly universal in eukaryotes [6], allows organisms to produce much more genetically diverse offspring [7]. Linear chromosomes and meiotic cell division mean that the genetic material can be shuffled across the homologous chromosomes, and that homologous chromosomes can independently segregate into the four haploid daughter cells.…”