Eukaryotes had to raise their game in the sex department.
Sex is very costly. On a biological level, not only does one have to put up with all the searching, displaying, courting, sharing, commitment, etc., but one gives up the ability to have children alone, by simple division, or parthanogenesis. Sex seems to be a fundamental development in the earliest stages of eukaryotic evolution, along with so many other innovative features that set us apart from bacteria. But sex is one of the oddest innovations, and demands its own explanation.
Sex and other forms of mating confer one enormous genetic benefit, which is to allow good and bad mutations to be mixed up, separated, and redistributed, so that offspring with a high proportion of bad genes die off, and other offspring with a better collection can flourish. Organisms with no form of sex (that are clonal) can not get rid of bad mutations. Whatever mutations they have are passed to offspring, and since most mutations are bad, not good, this leads to a downward spiral of genetic decline, called Muller's ratchet.
It turns out that non-eukaryotes like bacteria do mate and recombine their genomes, and thus escape this fate. But their process is not nearly as organized or comprehesive as the whole-genome re-shuffling and mating that eukaryotes practice. What bacteria do is called lateral gene transfer, (LGT), because it typically involves short regions of their genomes, (a few genes), and can accept DNA from any sort of partner- they do not have to be the same species, though specific surface structures can promote mating within a species. Thus bacteria have frequently picked up genes from other species- the major limitation happens when the DNA arrives into the recipient cell, and needs to find a homologous region of the recipient's DNA. If it is too dissimilar, then no genetic recombination happens. (An exception is for small autonomous DNA elements like plasmids, which can be transferred wholesale without needing an homologous target in the recipient's genome. Antibiotic resistance genes are frequently passed around this way, for emergency selective adaptation!) This practice has a built-in virtue, in that the most populous bacteria locally will be contributing most of the donor DNA, so if a recipient bacterium wants to adapt to local conditions, it can do worse than try out some local DNA. On the other hand, there is also no going back. Once a foreign piece of DNA replaces the recipient's copy, there are no other copies to return to. If that DNA is bad, death ensues.
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| Two bacteria, connected by a sex pilus, which can conduct small amounts of DNA. This method is generally used to transfer autonomous genetic elements like plasmids, whereas environmental DNA is typically taken up during stress. |
A recent paper modeled why this haphazard process was so thoroughly transformed by eukaryotes into the far more involving process we know and love. The authors argue that fundamentally, it was a question of genome size- that as eukaryotes transcended the energetic and size constraints of bacteria, their genomes grew as well- to a size that made the catch-as-catch-can mating strategy unable to keep up with the mutation rate. Greater size had another effect, of making populations smaller. Even with our modern billions, we are nothing in population terms compared to that of any respectable bacterium. This means that the value of positive mutations is higher, and the cost of negative mutations more severe, since each one counts for more of the whole population. Finding a way to reshuffle genes to preserve the best and discard the worst is imperative as populations get smaller.
Sex does several related things. The genes of each partner recombine randomly during meiosis, at a rate of a few recombination events per chromosome, thereby shuffling each haploid chromosome that was received from its parents. Second, each chromosome pair assorts randomly at meiosis, thereby again shuffling the parental genomes. Lastly, mating combines the genomes of two different partners (though inbreeding happens as well). All this results in a moderately thorough mixing of the genetic material at each generation. The resulting offspring are then a sampling of the two parental (and four grand-parental) genomes, succeeding if they get mostly the better genes, and not (frequently dying in utero) if they do not.
Additionally, eukaryotic sex gave rise to the diploid organism, with two copies of each gene, rather than the one copy that bacteria have. While some eukaryotes spend most of their lives in the haploid phase, and only briefly go through a diploid mated state, (yeasts are a good example of this lifestyle), most spend the bulk of their time as diploids, generating hapoid gametes for an extremely brief hapoid existence. The diploid provides the advantage of being able to ignore many deleterious genes, being a "carrier" for all those bad (recessive) mutations that are covered by a good allele. Mutations do not need to be eliminated immediately, taking a substantial load off the mating system to bring in replacements. (Indeed, some bacteria respond to stress by increasing promiscuity, taking in more DNA in case a genetic correction is needed, in addition to increasing their internal mutation rate.) A large fund of defective alleles can even become grist for evolutionary innovation. Still, for the species to persist, truly bad alleles need to be culled eventually- at a rate faster than that with which they appear.
The authors do a series of simulations with different genome sizes, mutation rates and sizes (DNA length) and rates of lateral gene transfer. Unfortunately, their figures are not very informative, but the logic is clear enough. The larger the genome, the higher the mutation load, assuming constant mutation rates. But LGT is a sporadic process, so correcting mutations takes not just a linearly higher rate of LGT, but some exponentially higher rate- a rate that is both insufficient to address all the mutations, but at the same time high enough to be both impractical and call into question what it means to be an individual of such a species. In their models, only when the length of LGT segments is a fair fraction of the whole genome size, (20%), and the rate quite high, like 10% of all individuals experiencing LGT once in their lifetimes, do organisms have a chance of escaping the ratchet of deleterious mutations.
" We considered a recombination length L = 0.2g [genome size], which is equivalent to 500 genes for a species with genome size of 2,500 genes – two orders of magnitude above the average estimated eDNA length in extant bacteria (Croucher et al., 2012). Recombination events of this magnitude are unknown among prokaryotes, possibly because of physical constraints on eDNA [environmental DNA] acquisition. ... In short, we show that LGT as actually practised by bacteria cannot prevent the degeneration of larger genomes. ... We suggest that systematic recombination across the entire bacterial genomes was a necessary development to preserve the integrity of the larger genomes that arose with the emergence of eukaryotes, giving a compelling explanation for the origin of meiotic sex."
But the authors argue that this scale of DNA length and frequency of uptake are quite unrealistic for actual bacteria. Bacterial LGT is constrained by the available DNA in the environment, and typically takes up only a few genes-worth of DNA. So as far as we know, this is not a process that would or could have scaled up to genomes of ten or one hundred fold larger size. Unfortunately, this is pretty much where the authors leave this work, without entering into an analysis of how meiotic recombination and re-assortment would function in these terms of forestalling the accumulation of deleterious mutations. They promise such insights in future work! But it is obvious that eukaryotic sex is in these terms an entirely different affair from bacterial LGT. Quite apart from featuring exchange and recombination across the entire length of the expanded genomes, it also ensures that only viable partners engage in genetic exchange, and simultaneously insulates them from any damage to their own genomes, instead placing the risk on their (presumably profuse) offspring. It buffers the effect of mutations by establishing a diploid state, and most importantly shuffles loci all over these recombined genomes so that deleterious mutations can be concentrated and eliminated in some offspring while others benefit from more fortunate combinations.
