Weak Epistasis May Drive Adaptation in Recombining Bacteria

Abstract

Abstract:The impact of epistasis on the evolution of multilocus traits depends on recombination. While sexually-reproducing eukaryotes recombine so frequently that epistasis between polymorphisms is not considered to play a large role in short-term adaptation, many bacteria also recombine, some to the degree that their populations are described as 'panmictic' or 'freely recombining'. However, whether this recombination is sufficient to limit the ability of selection to act on epistatic contributions to fitness is unknown. We quantify homologous recombination in five bacterial pathogens and use these parameter estimates in a multilocus model of bacterial evolution with additive and epistatic effects. We find that even for highly recombining species (e.g. Streptococcus pneumoniae or Helicobacter pylori), selection on weak interactions between distant mutations is nearly as efficient as for an asexual species, likely because homologous recombination typically transfers only short segments. However, for strong epistasis, bacterial recombination accelerates selection, with the dynamics dependent on the amount of recombination and the number of loci. Epistasis may thus play an important role in both the short-and long-term adaptive evolution of bacteria and, unlike in eukaryotes, is not limited to strong effect sizes, closely linked loci, or other conditions that limit the impact of recombination.Author Summary: Like sexual eukaryotes, many bacterial species recombine so extensively that mutations are only weakly correlated from being transferred to many genetic backgrounds. Recombination in these species breaks mutation combinations and may limit the ability of selection to act on epistatic interactions between mutations. However, even for bacteria that have been historically described as "fully sexual", we show selection may still act on very weak epistatic effects, such that epistasis may frequently comprise an important genetic component of adaptive phenotypes in this kingdom of life despite large variation in recombination rates among species. Since the rate of adaptation for epistatic multilocus traits depends on the number of loci and the recombination rate, bacteria may differ dramatically in their adaptive solutions to selective pressures. 4

Dynamics of genomic change during evolutionary rescue in the seed beetleCallosobruchus maculatus

“…Second, epistatic interactions could have altered the marginal fitness effects of causal variants as allele frequencies changed. Epistatic interactions have previously been shown to play an important role in adaptation in several species, including mice (Steiner et al ., 2007), yeast (Ono et al ., 2017), and bacteria (Arnold et al ., 2018), and future work mapping the genetic basis of host-specific performance or fecundity traits in adapted/maladapted C. maculatus could test for epistasis in this system. Third, direct selection on causal variants could be constant, but indirect selection on our SNP markers could shift as allele frequencies and LD evolve.…”

Predicting evolution using frequency-dependent selection in bacterial populations

“…However, detailed predictions of how a population will respond to a selective pressure are challenging. Models that specify how mutations with a given fitness change in frequency over time are often hard to apply in practice, as we typically do not know in advance important parameters such as the fitness value of particular alleles or how this is affected by their frequency (frequency-dependent selection) or genetic background (epistasis) (5).…”

“…This finding must be considered in the context of recombination, selection, and the evolutionary timescale impacting the pneumococcal genome, which may impact the varying magnitude of NFDS signal across sets of loci. Despite moderate levels of bacterial recombination among pneumococci, there remains appreciable linkage disequilibrium between loci nearby as well as genome-wide (5), which makes it difficult to discern the relative selective importance of any particular locus. Exactly which genomic elements are responsible for the predictive ability we document here is unknown but is obviously of interest and should be a focus for future work.…”

The landscape of coadaptation in Vibrio parahaemolyticus

“…As a result, mutations that are beneficial only on specific backgrounds have a chance to rise to high frequency on those backgrounds even if they are harmful on others. Epistatic interactions that involve only small selective coefficients s (for example s = 1.0×10 −4 ) can create an imprint on the genome in the form of strong linkage disequilibrium (9). These arguments imply that extensive complex coadaptation can potentially accumulate within a single population.…”