Can diploidy evolve in absence of sexual reproduction?

Question

Theoretical question

• Can diploidy (or polyploidy) evolve from a haploid lineage in the absence of sexual reproduction ?
• For what theoretical reason? How can such evolution take place?

Empirical evidence

Beside theoretical answers I'd like to also ask for empirical examples:

• Are there any examples of diploid (or polyploid) species that reproduce exclusively asexually, and for which sexual reproduction never occurred in the evolutionary lineage of this species?

Or in other words,

• Does diploidy (or polyploidy) exist in lineages that has never underwent sexual reproduction?

Is my assumption correct?

I am assuming that in eukaryotes haploidy appeared before diploidy. Is this assumption correct?

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By sexual reproduction I mean that the genome of the offspring is a combination (with or without recombination/crossover) of two parent individuals. I don't mean reproduction with sexes (or with mating types). I welcome the discussion of self-fertilization if needed.

Answer 1

I can only offer a partial answer on the theoretical aspects. I don't know if you are familiar with the mid-90s papers by Otto et al. (Otto & Goldstein,1992, Otto & Marks, 1996), but these are definitely relevant to your question. They deal with the "masking hypothesis" of diploidy, i.e. that deleterious mutations can be masked by "healthy" alleles, and the trade-offs between diploidy (ploidy level), recombination rate, and purging of deleterious alleles. Otto & Goldstein (1992) shows that recombination is essential for the evolution of diploidy, and without recombination, haploids will "win" over diploids.

Otto & Marks (1996) is a fairly comprehensive paper that builds on the previous one, and looks at how different mating systems interact with recombination and purging to influence the evolution of ploidy levels. As a general result, they predict a correlation between mating system and ploidy level, with sexual reproduction favoring diploidy, while asexual reproduction favors haploidy. However, from what I can see after a quick re-read, there is nothing that prohibits asexually reproducing species to be diploid (and vice versa) - see e.g. page 206 - and the paper includes a condition that must hold for diploids to invade in asexually reproducing or selfing populations. I have not followed this literature closely, though, and I imagine that tracing recent papers that cite Otto & Marks (1996) can be useful to find further relevant studies.

You should also consider that ploidy levels can differ between sexes (e.g. bees), which can lead to antagonistic selection, which can influence ploidy evolution (see e.g. Immler & Otto, 2014).

As for the empirical evidence part, I do not have any good examples. However, I imagine that it can be extremely difficult to prove that a lineage has only reproduced asexually (or never asexually), since these things are hard to track in fossils. Also consider that it is common to have both sexual and asexual stages, and many species can have a long asexual diploid stage followed by a shorter sexual haploid stage. From what I know, this is the norm in e.g. algae (arguably a group of fairly "basal" taxa). However, I don't know what the ancestral state of algae was (i.e. if they became diploid before having a sexual stage).

As for the ancestral state of eukaryotes, there seems to be evidence that the ancestral state was in fact facultatively sexual (Dacks & Roger, 1999), which would invalidate your assumption. However, this is only based on a couple of quick literature searches on my part, and I am in no way an expert in this area. There are probably more recent studies on this topic as well. However, it is clear that you cannot blindly assume that eukaryotic haploid is ancestral.

Answer 2

This is not on theoretical grounds, but here is an existence proof: a number of bacteria, which reproduce asexually, are polyploid. Here is a blog I really like informally discussing the concept of ploidy in bacteria. The example I am familiar with is cyanobacteria, which can have 3-4 all the way up to 142 copies of its genome, according to this paper (1). There are other examples as well, such as Epulopisculum, a sturgeonfish symbiont (2). This paper even reports a diploid bacteria (3). Searching in Pubmed should reveal other interesting cases of this.

A more borderline example would be even the most typical bug E. coli. When E. coli grows rapidly, it is well known that it has more than one copy of its genome per cell; this allows the organism to be creating the genome for the granddaughters of the current cell, allowing the time between divisions to be shorter than the time it takes to replicate DNA (4). Here is an intuitive explanation of this. Depending on your definition of polyploidy this might not count, but the bacteria presumably are able to make use of this copy number effect.

(1) Greise M et al. (2011). Ploidy in cyanobacteria. FEMS Microbiol. Lett. 323(2):124-31

(2) Mendell JE et al (2008). Extreme polyploidy in a large bacterium. PNAS 105(18): 6730-34

(3) Michelsen O et al (2010). J. Bacteriol. 192(4): 1058-65

(4) Helmstetter CE (1968). DNA synthesis during the division cycle of rapidly growing Escherichia coli B/r. J. Mol. Biol. 31(3) 507-518 ---non-free, unfortunately, but see also Nielsen HJ et al (2007). J. Bacteriol. 189(23):8660-6