Eukaryote sex is ancestral and widespread

[lpetrich]

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

Here is the overall eukaryote cell cycle. () = cell, X = chromosome.

Haploid: (X) -- asexual reproduction: (X) -> (XX) -> (X) + (X) -- haploid
Cell Fusion: (X) + (X) -> (XX) -- diploid
Diploid: (XX) -- asexual reproduction: (XX) -> (XXXX) -> (XX) + (XX) -- haploid
Meiosis: (XX) -> (XXXX) -> (XX) + (XX) -> (X) + (X) + (X) + (X) -- haploid

The haploid phase, the diploid phase, or both phases can be multicellular.

Previous work had found genes for meiosis-involved proteins in a variety of organisms, including some with no known sexual phase: PLOS ONE: An Expanded Inventory of Conserved Meiotic Genes Provides Evidence for Sex in Trichomonas vaginalis

The current study looked for genes for two proteins,
HAP2 -- for fusing cells
GEX1 -- for fusing cell nuclei
Thus completing the cycle.

This paper's authors found some cell-fusion genes in organisms with no known sexual phase, parallel to that earlier work involving meiosis genes. They failed to find homologs of HAP2 and GEX1 in some organisms, though one or both are absent from some sexually-reproducing ones.

One of their section titles is "Sex in Eukaryotic Microorganisms: More Voyeurs Needed", a section that includes

The sexual cycle of the ascomycete fungus Aspergillus fumigatus was described only in 2009, i.e., nearly 150 y after the species was originally described, despite the fact that this ubiquitous causative agent of life-threatening invasive aspergillosis and important allergen causing severe asthma and sinusitis had been extensively studied for years.

Also,

The taxonomic history of algae and fungi is full of examples of organisms, originally considered as completely different taxa, turning out to be different sexual life cycle stages.

Also, some parasitic organisms are asexual inside their hosts, but have been found to be sexual outside of them. That may also be true of symbionts like the symbiotic dinoflagellate Symbiodinium.

The authors quote an estimate for how much sexuality the tiny marine green alga Ostreococcus tauri has: meiosis / mitosis (asexual division) ~ 10^(-6). A million ordinary divisions for each sexual division.

So we get a picture of many one-celled and simple multicelled eukaryotes reproducing asexually nearly all of the time.

As to why ancestral eukaryotes evolved a sexual phase, the authors speculate that one reason is protection against Reactive Oxygen Species, a side effect of allowing oxygen to be present so that the mitochondria can use it. This would be alongside various other things that may have provoked the evolution of a sexual phase: bring beneficial mutations together, more efficient purging of deleterious ones (Muller's ratchet), and speeding up evolution to outrun parasites (the Red Queen hypothesis).

But it is evident from this work that the ancestral eukaryote had a full-scale sexual cycle, and that most of its descendants had inherited it. Long-lived purely asexual lineages appear to be rare.

 

[Valjean]

Shameless trollops!

 

[lpetrich]

Box 1. of the previously-mentioned paper: Eukaryote phylogenetic diversity: Reshuffling supergroups, microkingdoms, and an elusive root

LECA = Latest Eukaryote Common Ancestor

Recent rooting hypotheses predict that the LECA was a full-scale eukaryote, complete with mitochondria and an endomembrane system, though not with chloroplasts. This work means that it had a complete haploid-diploid cycle, sex and all. The Opimoda-Diphoda rooting suggests that the LECA was an excavate-like organism that had two flagella and a complicated cytoskeleton associated with them. Also that it ate bacteria.

That makes its evolution all the more mysterious, since it's a big jump from prokaryotes to the LECA.

The authors endorse Romain Derelle's results for the eukaryotes' root location, from
Rooting the Eukaryotic Tree with Mitochondrial and Bacterial Proteins
Bacterial proteins pinpoint a single eukaryotic root

Derelle finds that Excavata must be split up, and he finds:

• Opimoda X
  • Amorphea X
    • Opisthokonta - animals, fungi X
    • Amoebozoa X
  • Malawimonas (in "Excavata")
• Diphoda X
  • Discoba (in "Excavata")
  • Diaphoretickes X
• Metamonada (uncertain position) (in "Excavata") X

Opimoda = OPIsthokonta + aMOebozoa
Diphoda = DIscoba + diaPHOretickes

Diaphoretickes X

• Archaeplastida X
  • Glaucophytes
  • - X
    • Chloroplastida - green algae, land plants X
    • Rhodophyta - red algae X
• SAR X
  • Stramenopiles X
  • Alveolata X
  • Rhizaria X
• (Various others)

I've added an X for evidence of meiosis, either observation of it or discovery of meiosis-related genes

 

[bilby]

For those of you outside Australia, a 'rooting hypothesis' is a slang term, meaning an 'hypothesis relating to sexual intercourse'.

 

[Angry Floof]

That is some complex and kinky sexytime going on there.