Rewriting the history of sex

Amoebae are the poster children for asexual reproduction.  Textbooks show single amoeboid cells like the one above splitting themselves neatly into two daughters — no muss, no fuss.  Theories of why and when sex evolved thus tend to focus on multicellular organisms such as animals and plants.  But the story has never been quite that simple — many unicellular organisms do show evidence for sexual reproduction, though they’ve been dismissed as unimportant exceptions to the rule.  A recent review (Lahr et al. 2011. The chastity of amoebae: re-evaluating evidence for sex in amoeboid organisms.  Proc. R. Soc. B doi:10.1098/rspb.2011.0289) now suggests that we may be looking at the whole situation backwards: among eukaryotes, the unicellular organisms that reproduce sexually may be the rule, not the exception.

Tree of life showing protists as a separate kingdom

Lahr et al. argue that the confusion about unicellular sex has its roots in Victorian-era classifications of single-celled eukaryotes (or protists) as “primitive”, which in the ’60’s led to the view that they were part of a separate biological “kingdom”, and fundamentally different from the multicellular organisms.  In the last few years, however, it’s become clear that this way of thinking simply doesn’t fit reality.  You only get this kind of tree if you define protists as “all eukaryotes that aren’t plants, animals or fungi”.  If you use a more principled classification scheme, single-celled organisms show up all over your evolutionary tree.  For example, the choanoflagellates (single-celled) are much more closely related to both fungi and animals (multicellular) than they are to the entamoebae, the type of amoebae that are responsible for amoebic dysentery.  But both the entamoebae and the choanoflagellates (both single-celled) are closer to the animals than plants (multicellular) are.  Evidently, multicellularity evolved more than once: so it is now impossible to put single-celled eukaryotes in a category by themselves.

So what about sex? With the old tree, you could imagine a common ancestor for plants, animals and fungi that managed to acquire both multicellularity and sex.  With the new tree, you have to imagine many independent inventions of sexuality — one each for plants, animals and fungi, and several more to cover the unicellular organisms that reproduce sexually.  Sexual reproduction minimally requires an organism to have two different states — one with twice as many chromosomes as the other — and to be able to switch between the states by dividing or fusing cell nuclei, so that chromosomes from two different organisms can come together in a single organism.  This is a complicated process to invent once, let alone lots of times.

Lahr et al. make three main arguments.  First, and this is where they spend most of their time in this paper, there is a lot more evidence for sex in single-celled eukaryotes than anyone thought.  Second, most of the evidence for asexuality in single-celled eukaryotes is negative: we assume they’re asexual unless we’ve actually caught them in the act.  But even amoebae may be shy about performing sex acts in public.  Some unicellular eukaryotes are hard to culture in the lab, and others may never get in the mood under lab conditions.  As Lahr et al. point out, “it may not be prudent to rely on the absence of evidence as evidence of the absence of sex”.  And third, all the reasons that evolutionary theorists have come up with for why sex might be useful for multicellular organisms would benefit single-celled organisms just as much.

Fundamentally, the advantage of sexual reproduction is that it allows you to mix DNA from different members of your population, so that the best combinations of genes can arise and outcompete the worst combinations of genes.  Without sex, or another form of DNA mixing, you would expect that unhelpful mutations would accumulate in the population — a theory that goes under the name of Muller’s ratchet — because without DNA recombination there is no way of carving out the unhelpful mutation and getting rid of it.  This is a problem that should affect unicellular organisms just as much as multicellular ones.  It’s possible, of course, that there are special disadvantages to sex in single-celled eukaryotes, but the more examples of sex in protists we find, the less likely this sounds.  Protists that swing both ways, reproducing either sexually or asexually depending on conditions (such as the Dictyostelia) are perhaps the most persuasive argument against that idea: we know for a fact that they can switch into asexual behavior if they want to, and yet there are clearly situations in which they find sexual behavior worthwhile.

Diving deep into the literature, Lahr et al. classify unicellular eukaryotes into four groups: (1) confirmed sexual behavior — these organisms show both meiosis (cell division that reduces the complement of chromosomes to 1/2 of what it was before, converting diploid to haploid) and karyogamy, or nuclear fusion (converting haploid to diploid, with contributions from two individuals); (2) direct evidence for sex, usually either meiosis or karyogamy but not both; (3) indirect evidence for sex, usually either the presence of genes that in other organisms are responsible for meiosis or evidence of an outcome that might result from sex, e.g. the appearance of heterozygotes when you mix two homozygotic populations; and (4) no evidence at all.  Remarkably, given the received wisdom that sex is rare in unicellular eukaryotes, nearly every major lineage in the two largest groups of amoeboid organisms (Amoebozoa and Rhizaria)  shows at least indirect evidence for sex, and over half of them show “direct” evidence or better.

The easiest way to explain these data is to postulate that sex is as old as eukaryotes: if the oldest common ancestor of eukaryotes reproduced in a sexual fashion (dividing meiotically to produce haploid cells, then fusing two haploid cells to produce a diploid cell), then you would expect all eukaryotes to follow suit.  This would mean that the organisms that are peculiar are not the unicellular eukaryotes that do have sex, but the ones that don’t. The evolutionary question is now completely turned on its head: instead of asking why a sexual organism was sufficiently unusual to need sex, we need to ask what it is about the lifestyle of an asexual organism (such as the multicellular bdelloid rotifer) that allows it to dispense with sex.  Lahr et al. suggest that various kinds of lateral gene transfer or periods of polyploidy may substitute for sex in some organisms — which still leaves open the question of why it’s advantageous to choose one strategy rather than another.  Fascinating.

Lahr DJ, Parfrey LW, Mitchell EA, Katz LA, & Lara E (2011). The chastity of amoebae: re-evaluating evidence for sex in amoeboid organisms. Proceedings. Biological sciences / The Royal Society PMID: 21429931