Why I don't work on sex in eukaryotes

I just got back from the SMBE meeting and the final meeting of the CIfAR (formerly CIAR) Evolutionary Biology program. I made a point of going to most of the sessions on deep phylogeny, and they reminded me of why I decided not to work on the evolutionary origins of sexual reproduction in Eukaryotes.

John Logsdon's talk reminded me of why and how I originally was planning to work on this. "The Evolution of Sex" is still one of the biggest unsolved problems in evolutionary biology; we don't know how or why eukaryotic sexual reproduction (by meiosis and gamete fusion) originated and we don't know why it's been so evolutionarily successful. Most research into this is theoretical, or involves comparing populations that reproduce with and without sex.

My plan (10 or 15 years ago) was to instead investigate the origin of sexual reproduction by first identifying the deepest-branching evolutionary lineage that has sexual reproduction or homologs of meiosis-specific genes, and then determining the functions of these homologs and/or of sexual reproduction in the present-day members of this lineage.

When I first made this plan, the field of deep phylogeny was full of optimism that we would soon have a reliable phylogenetic tree showing the true relationships of all eukaryotes. The figure to the left shows the state of the tree then. The groups called Diplomonads, Trichomonads and Microsporidia were thought to be the first to have branched from the line that eventually led to plants and animals. Microsporidians were known to have (various weird forms of) sexual reproduction, while sex was unknown in Trichomonads and Diplomonads, consistent with an origin between the times of these divergences. The precise branching order wasn't yet firm, but most researchers felt that all we needed was a few more sequences of a few key taxa, and maybe a few refinements to the analytical methods used to infer relationships from sequences.

But the adjacent figure shows the present state of this phylogeny. It's from a recent review by a collaboration of CIfAR researchers, all but one of whom were at last week's meetings (Keeling et al. Trends in Ecology & Evolution 20:670-676). There's a pdf here; I think it's open access.

The new tree organizes the eukaryotes into five main lineages, with no real information about the order in which these groups originated (the 'root' (the center of the figure) is shown as what's called a 'star' phylogeny). The division into five groups is itself very speculative, as there are very deep divergences within each group. Bottom line? we don't know which eukaryote lineages arose first, and few researchers are now confident that we will ever know.

And where is sexual reproduction in this tree? Just about everywhere; the apparently asexual groups are dispersed with the sexual groups. So I don't regret my decision 7 years ago to abandon my goal of placing the origin of sex on the eukaryote tree.

And what about the goal of identifying the genes specific to meiosis, and characterizing their distribution in eukaryotes? A number of genes have been described as 'meiosis-specific', and in his SMBE talk John reported on their distribution and relationships to other genes, especially in those unicellular eukaryotes that might be representatives of early branches. Most of these genes are present in most of the species he's looked at, and in most cases they appear to have arisen by gene duplication.

One of the biggest challenges with this work is being sure that a gene is indeed meiosis-specific in all of the species it's found in - a gene that is meiosis-specific in yeast could have a related but not meiosis-specific role in a distant relative. This is very difficult to determine, especially because sex has never been observed in some of these species (if they are sexual, they're also very secretive). I'm glad that John Logsdon has been working on this, rather than me.