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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?


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 genders (or with mating types). I welcome the discussion of self-fertilization if needed.

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2 Answers

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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 definately 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 interacts with recombination and purging to influence the evolution of ploidy levels. As a general results they predict a correlation between mating system and poidy 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 litterature 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 have 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 litterature 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.

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Thanks a lot for this literature. It is very interesting indeed. And thanks for the Dacks and Roger's article too! –  Remi.b Feb 7 at 15:18
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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

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Nice examples, but I suspect that the original poster is looking for eukaryotic examples (based on the Is my assuption correct? part) –  fileunderwater Feb 6 at 22:22
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From a theoretical viewpoint, why should it matter? If you are looking only at whether an asexually reproducing species can evolve polyploidy, then I feel that asexual eukaryotes and asexual prokaryotes are reproducing the same way, and so will provide viable models for this process. Furthermore, are there any uniformly haploid eukaryotes? If not current, do we have evidence of any in the fossil record? –  A. Kennard Feb 6 at 22:42
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All the mechanisms that I know influencing heredity (and thus evolution) that differ between eukaryotes and prokaryotes (e.g. homologous recombination) have to do with sexual reproduction or are intrinsically features of a polyploid organism. They couldn't factor into the evolution of polyploidy in a haploid organism, prokaryote or eukaryote. The only difference would be if there is an effect of having multiple, different chromosomes; most bacteria only have one type of chromosome, and I'm not sure how polyploid the few examples of bacteria with multiple chromosomes are. –  A. Kennard Feb 6 at 22:46
    
I mostly agree, and just pointed out what the Q seemed to ask for. However, I guess horizontal transfer could make a difference in bacteria, but I cannot really say if this should be important specifically for the evolution of diploidy. Overall, I agree that they should face the same problems going from haploid->diploid. Does "masking" of deleterious alleles work the same way in diploid bacteria as in eukaryotes? –  fileunderwater Feb 6 at 22:55
    
+1 Thanks for these empirical observations. They are meaningful to my question and impressive. –  Remi.b Feb 7 at 15:19
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