One of the most interesting topics in my molecular Evolution class was the discussion over the importance of sex. Most students seem to think the problem is solved. They were taught that sex increases variation in a Population and this gives sexual populations an evolutionary advantage. The fact that sex (recombination) breaks up as many linkages as it creates makes the explanation much less viable. The fact that there's very little evidence to support the claim comes as quite a surprise to my students. Sex is still one of the greatest mysterious in evolutionary biology [What did Joe Felsenstein say about sex?] [Everything you thought you knew about sex is probably wrong].

It is worth noting that Maynard Smith's argument invalidates the earliest genetic argument for the evolution of recombination, that advanced by East (1918). That argument is also the one commonly found in textbooks, which tend to be a bit out of date (in this case, by over 50 years). East argued that recombination creates new genotypes. So it does. An AB/ab parent will have among its gametes not only the two types that formed it, AB and ab, but also Ab and aB if there is recombination between the two loci. But if the population is in linkage equilibrium, then somewhere else an Ab/aB parent will be undergoing recombination, which will remove Ab and aB gametes and replace them by AB and ab. These two processes will exactly cancel each other if the two types of double heterozygote, coupling (AB/ab) and repulsion (Ab/aB) are equally frequent. This will happen precisely when the population is in linkage equilibrium. In that case no new genotypes arise by recombination....

We have that anomalous situation that a detailed population genetic analysis analysis reveals not only that the standard explanation for the evolution of recombination will not work, but also that there is a good evolutionary reason for believing that modifiers will be selected to eliminate recombination. [my emphasis LAM]

                        Joe Felsenstein (1988)

Maddamsetti, R., and Lenski, R. E. (2017) Analysis of bacterial genomes from an evolution experiment with horizontal gene transfer shows that recombination can sometimes overwhelm selection. PLOS Genetics, January 31, 2018. [doi: 10.1371/journal.pgen.1007199]

Abstract

Few experimental studies have examined the role that sexual recombination plays in bacterial evolution, including the effects of horizontal gene transfer on genome structure. To address this limitation, we analyzed genomes from an experiment in which Escherichia coli K-12 Hfr (high frequency recombination) donors were periodically introduced into 12 evolving populations of E. coli B and allowed to conjugate repeatedly over the course of 1000 generations. Previous analyses of the evolved strains from this experiment showed that recombination did not accelerate adaptation, despite increasing genetic variation relative to asexual controls. However, the resolution in that previous work was limited to only a few genetic markers. We sought to clarify and understand these puzzling results by sequencing complete genomes from each population. The effects of recombination were highly variable: one lineage was mostly derived from the donors, while another acquired almost no donor DNA. In most lineages, some regions showed repeated introgression and others almost none. Regions with high introgression tended to be near the donors’ origin of transfer sites. To determine whether introgressed alleles imposed a genetic load, we extended the experiment for 200 generations without recombination and sequenced whole-population samples. Beneficial alleles in the recipient populations were occasionally driven extinct by maladaptive donor-derived alleles. On balance, our analyses indicate that the plasmid-mediated recombination was sufficiently frequent to drive donor alleles to fixation without providing much, if any, selective advantage.

Author summary

Bacteria often transfer genes encoding antibiotic resistance as well as other important traits, but the extent of intergenomic recombination—in effect, sex—is highly variable across bacterial species. Why? A better understanding of how and why bacteria exchange genes would help people combat the spread of infectious disease as well as shed light on the evolutionary origins of sex. Here, we sequenced genomes from an evolution experiment with Escherichia coli in which recombination was extensive but, unexpectedly, did not speed up the rate of adaptation. In this experiment, the effective rate of chromosomal recombination was much higher than previously inferred for natural E. coli populations. In fact, the rate was so high that introduced genes sometimes drove established beneficial alleles to extinction in the experimental populations. In effect, genes that were physically linked to the genes causing recombination had a strong transmission advantage, whether or not they provided any selective advantage to the recipient cells.