Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

Abstract

Sexual reproduction and clonality in eukaryotes are mostly seen as exclusive, the latter being rather exceptional. This view might be biased by focusing almost exclusively on metazoans. We analyze and discuss reproduction in the context of extant eukaryotic diversity, paying special attention to protists. We present results of phylogenetically extended searches for homologs of two proteins functioning in cell and nuclear fusion, respectively (HAP2 and GEX1), providing indirect evidence for these processes in several eukaryotic lineages where sex has not been observed yet. We argue that (i) the debate on the relative significance of sex and clonality in eukaryotes is confounded by not appropriately distinguishing multicellular and unicellular organisms; (ii) eukaryotic sex is extremely widespread and already present in the last eukaryotic common ancestor; and (iii) the general mode of existence of eukaryotes is best described by clonally propagating cell lines with episodic sex triggered by external or internal clues. However, important questions concern the relative longevity of true clonal species (i.e., species not able to return to sexual procreation anymore). Long-lived clonal species seem strikingly rare. We analyze their properties in the light of meiotic sex development from existing prokaryotic repair mechanisms. Based on these considerations, we speculate that eukaryotic sex likely developed as a cellular survival strategy, possibly in the context of internal reactive oxygen species stress generated by a (proto) mitochondrion. Thus, in the context of the symbiogenic model of eukaryotic origin, sex might directly result from the very evolutionary mode by which eukaryotic cells arose.

Keywords: eukaryotes; evolution; protists; reactive oxygen species; sex.

Fig. 1.

Representatives of deep eukaryotic lineages without published evidence for sex thus far. (A) Picomonas judraskeda (Picozoa). (B) Andalucia incarcerata and another, thus far undescribed jakobid (Jakobida). (C) Ancyromonas sigmoides (Ancyromonadida). (D) Roombia truncata (Katablepharida). (E) Breviata anathema (Breviatea). (F) Telonema subtilis (Telonemia). (G) An undescribed malawimonad (Malawimonadida). Images courtesy of Petr Táborský (B), Aaron Heiss (C, E, and G), and Akinori Yabuki (F); A and D were adapted from refs. and . (Scale bars, 5 μm.)

Fig. 2.

Distribution of (meiotic) sex and selected sex-related features in eukaryotes. The schematic phylogeny is a consensus of recent literature (Box 1). Root position according to Derelle et al. (138); root positions suggested by others (–136) indicated by small arrows. The Metamonada position remains unsettled. *Uptake of an α-proteobacterium at the origin of the eukaryotes. For each lineage, previously reported or assumed presence of sex is indicated: black boxes, well-documented sex; gray boxes, limited evidence for sex (rare direct observations, indirect inference from genomic data); no boxes, no published evidence; references used here are given in SI Text. The distribution of homologs of HAP2 and GEX1 proteins (implicated in gamete fusion and karyogamy, respectively; see main text) was obtained searching public and private genome and transcriptome resources (see SI Text for further details of genes identified). Absence of boxes does not directly imply absence in a lineage, especially for those given in gray, with limited (or absent) genome-scale sequence data.

Fig. 3.

Possible symbiogenic effects of internal ROS formation. Adaptations of the mitochondrion (Mi): supercomplex formation, antioxidant mechanisms, uncoupling (proteins), mitochondrial genome reduction, and carnitine shuttles. Adaptations of the cell: peroxisome formation (P), antioxidant mechanisms (Ao), internal membrane (Me) formation (autophagy), nuclear membrane (Nm) formation, size increase, and meiotic sex? See main text and ref. .