The coupling of ecology and evolution during range expansions enables mutations to establish at expanding range margins and reach high frequencies. This phenomenon, called allele surfing, is thought to have caused revolutions in the gene pool of many species, most evidently in microbial communities. It has remained unclear, however, under which conditions allele surfing promotes or hinders adaptation. Here, using microbial experiments and simulations, we show that, starting with standing adaptive variation, range expansions generate a larger increase in mean fitness than spatially uniform population expansions. The adaptation gain results from ‘soft’ selective sweeps emerging from surfing beneficial mutations. The rate of these surfing events is shown to sensitively depend on the strength of genetic drift, which varies among strains and environmental conditions. More generally, allele surfing promotes the rate of adaptation per biomass produced, which could help developing biofilms and other resource-limited populations to cope with environmental challenges.

Author contributions: OH, MG, FS designed study; MG, FS performed experiments. WM contributed new reagents/analytical tools; MG, OH developed theory; MG, OH developed coarsegrained simulations; FF, BW developed individual-based simulations; MG, FF, BW, OH analyzed data; MG, BW, WM, OH wrote the paper. All authors commented on and edited the manuscript. AbstractThe coupling of ecology and evolution during range expansions enables mutations to establish at expanding range margins and reach high frequencies. This phenomenon, called allele surfing, is thought to have caused revolutions in the gene pool of many species, most evidently in microbial communities. It has remained unclear, however, under which conditions allele surfing promotes or hinders adaptation. Here, using microbial experiments and simulations, we show that, starting with standing adaptive variation, range expansions generate a larger increase in mean fitness than spatially uniform population expansions. The adaptation gain results from 'soft' selective sweeps emerging from surfing beneficial mutations. The rate of these surfing events is shown to sensitively depend on the strength of genetic drift, which varies among strains and environmental conditions. More generally, allele surfing promotes the rate of adaptation per biomass produced, which could help developing biofilms and other resource-limited populations to cope with environmental challenges.Strains. We used S. cerevisiae strains with W303 backgrounds, where selective advantages were adjusted using cycloheximide. For experiments with E. coli, we used both DH5α and MG1655 strains, tuning fitness differences using tetracycline and chloramphenicol, respectively. Additionally, pairs of strains differing only in the fluorescent marker allowed us to perform truly neutral competition experiments (S. cerevisiae, S. pombe, E. coli). S. cerevisiae and E. coli strains with constitutively expressed fluorescent proteins were used to study the dynamics of cells at the front.A detailed description of all strains and growth conditions is found in Appendix C. 6Main Experiment: Adaptation from standing variation during two types of population expansions (see Fig. 1a): For each pair of mutant and wild type, a mixed starting population of size i was prepared that contained an initial frequency i of mutants having a selective advantage s, defined as the relative difference between mutant and wild-type growth rate ). The population was then grown to final size f in two ways, through a range expansion and, for comparison, through uniform growth, and the final mutant frequency f was determined. The associated increase in mean fitness ̅ follows as ∆ ̅ = ( f − i ) . Uniform Growth: Mixtures of cells were grown in well-shaken liquid medium to the desired final population size and the final fraction of mutant cells was determined using flow cytometry. Range Expansion: Colony growth was initiated by placing 2µl of the mixtures onto plates (2% w/v agar) and incubated until the desired final population size was reached. T...

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