Why panmictic bacteria are rare

Abstract

15Background Bacteria typically have more structured populations than higher eukaryotes, but this 16 difference is surprising given high recombination rates, enormous population sizes and effective 17 geographical dispersal in many bacterial species. 18Results We estimated the recombination scaled effective population size in 21 bacterial species 19 and find that it does not correlate with synonymous nucleotide diversity as would be expected under 20 neutral models of evolution. Only two species have estimates substantially over 100, consistent with 21 approximate panmixia, namely Helicobacter pylori and Vibrio parahaemolyticus. Both species are far 22 from demographic equilibrium, with diversity predicted to increase more than 30 fold in V. 23 parahaemolyticus if the current value of were maintained, to values much higher than found in 24 any species. We propose that panmixia is unstable in bacteria, and that persistent environmental 25 species are likely to evolve barriers to genetic exchange, which act to prevent a continuous increase in 26 diversity by enhancing genetic drift. 27Conclusions Our results highlight the dynamic nature of bacterial population structures and imply 28 that overall diversity levels found within a species are poor indicators of its size. 29 30 Keywords 31 Panmixia, bacterial population structure, effective population size, recombination, genetic diversity 32 33 Background 34 Bacteria are paragons of adaptability and make up more biomass than all organisms other than plants 35 combined [1]. Many bacterial species have enormous population sizes, disperse effectively around the 36 globe [2-5] and exhibit high rates of within-species homologous recombination [6]. Recombination 37 progressively breaks down non-random associations between markers (linkage disequilibrium), so 38 that in large populations, where pairs of individuals distantly related, linkage equilibrium is expected 39between all pairs of genomic sites. However, in most species for which data is available, there is 40 substantial genome-wide linkage disequilibrium, indicating structuring of variation [7]. Here we 41 3 propose a resolution of this paradox, namely that large bacterial populations accumulate diversity 42 progressively until that diversity acts as an effective barrier to genetic exchange between lineages. 43 44We examine the population structure of 21 bacterial species and find that only the Asian population of 45Vibrio parahaemolyticus is close to genome-wide linkage equilibrium. We find that this population 46 has undergone a recent expansion. If the current population size was maintained over evolutionary 47

The landscape of coadaptation in Vibrio parahaemolyticus

“…V. parahaemolyticus is ubiquitous in shellfish in warm coastal waters, within which it occurs at densities of around 1,000 cells per gram, so a back of the envelope calculation suggests there are likely to be substantially more than 10 15 bacteria in the VppAsia population. The species also has a high estimated effective population size (10, 11) and has strong codon bias, which is often argued to be evidence that even tiny selective coefficients can drive adaptation (24). Furthermore, recombination only breaks up linkage disequilibrium between loci slowly.…”

“…Most bacteria have population structure that deviates more markedly from panmixia (10). In some species this is likely due to smaller effective population sizes, lower recombination rates or mechanistic barriers to genetic exchange between strains.…”

“…Totally 1,103 global V. parahaemolyticus genomes were used in this work (Table S1), which also were analyzed in our other studies (8, 10). To reduce clonal signals, we firstly made a “non-redundant” dataset of 469 strains, in which no sequence differed by less than 2,000 SNPs in the core genome.…”

“…Although recombination happens slowly on the timescale of bacterial generations, the Asian population of V. parahaemolyticus has had a large effective population size for at least the last 15,000 years, or approximately 130 million bacterial generations, over which time recombination has been extensive enough to have almost completely scrambled genetic variation (10). As a result, the population is unusual amongst bacteria in that there is approximate linkage equilibrium between most loci greater than 3 kb apart on the chromosome (10).…”

“…Although recombination happens slowly on the timescale of bacterial generations, the Asian population of V. parahaemolyticus has had a large effective population size for at least the last 15,000 years, or approximately 130 million bacterial generations, over which time recombination has been extensive enough to have almost completely scrambled genetic variation (10). As a result, the population is unusual amongst bacteria in that there is approximate linkage equilibrium between most loci greater than 3 kb apart on the chromosome (10). This feature increases the power of tests for interaction based on identifying non-random associations, which relies on identifying the same combination of alleles on independent genetic backgrounds and can therefore be confounded by clonal or population structure unless this is appropriately controlled for.…”