Despite the homogenizing effect of strong gene flow between two populations, adaptation under symmetric divergent selection pressures results in partial reproductive isolation: adaptive substitutions act as local barriers to gene flow, and if divergent selection continues unimpeded, this will result in complete reproductive isolation of the two populations, i.e. speciation. However, a key issue in framing the process of speciation as a tension between local adaptation and the homogenizing force of gene flow is that the mutation process is blind to changes in the environment and therefore tends to limit adaptation. Here we investigate how globally beneficial mutations (GBMs) affect divergent local adaptation and reproductive isolation. When phenotypic divergence is finite, we show that the presence of GBMs limits local adaptation, generating a persistent genetic load at the loci that contribute to the trait under divergent selection and reducing genome-wide divergence. Furthermore, we show that while GBMs cannot prohibit the process of continuous differentiation, they induce a substantial delay in the genome-wide shutdown of gene flow. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Department of Marine Sciences Centre for Marine Evolutionary Biology University of Gothenburg Gothenburg Sweden

Institute of Evolutionary Biology University of Edinburgh Edinburgh UK

Institute of Vertebrate Biology Academy of Sciences of the Czech Republic Brno Czech Republic

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Felsenstein J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals?. Evolution 35, 124–138. (10.1111/j.1558-5646.1981.tb04864.x) PubMed DOI

Flaxman SM, Feder JL, Nosil P. 2013. Genetic hitchhiking and the dynamic buildup of genomic divergence during speciation with gene flow. Evolution 67, 2577–2591. (10.1111/evo.12055) PubMed DOI

Rafajlović M, Emanuelsson A, Johannesson K, Butlin RK, Mehlig B. 2016. A universal mechanism generating clusters of differentiated loci during divergence-with-migration. Evolution 70, 1609–1621. (10.1111/evo.12957) PubMed DOI PMC

Wu CI. 2001. The genic view of the process of speciation. J. Evol. Biol. 14, 851–865. (10.1046/j.1420-9101.2001.00335.x) DOI

Yeaman S, Whitlock MC. 2011. The genetic architecture of adaptation under migration-selection balance. Evolution 65, 1897–1911. (10.1111/j.1558-5646.2011.01269.x) PubMed DOI

Barton NH. 1983. Multilocus clines. Evolution 37, 454–471. (10.1111/j.1558-5646.1983.tb05563.x) PubMed DOI

Barton NH, Partridge L. 2000. Limits to natural selection. BioEssays 22, 1075–1084. (10.1002/1521-1878(200012)22:12<1075::AID-BIES5>3.0.CO;2-M) PubMed DOI

Piálek J, Barton NH. 1997. The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes. Genetics 145, 493–504. PubMed PMC

Hartfield M, Otto SP. 2011. Recombination and hitchhiking of deleterious alleles. Evolution 65, 2421–2434. (10.1111/j.1558-5646.2011.01311.x) PubMed DOI

Uecker H, Setter D, Hermisson J. 2015. Adaptive gene introgression after secondary contact. J. Math. Biol. 70, 1523–1580. (10.1007/s00285-014-0802-y) PubMed DOI PMC

Stapley J, Feulner PG, Johnston SE, Santure AW, Smadja CM. 2017. Variation in recombination frequency and distribution across eukaryotes: patterns and processes. Phil. Trans. R. Soc. B 372, 20160455 (10.1098/rstb.2016.0455) PubMed DOI PMC

Hill WG, Robertson A. 1966. The effects of linkage and the limits to artificial selection. Genet. Res. 8, 269–294. (10.1017/S0016672300010156) PubMed DOI

Haller BC, Messer PW. 2019. SLiM 3: forward genetic simulations beyond the Wright–Fisher model. Mol. Biol. Evol. 36, 632–637. (10.1093/molbev/msy228) PubMed DOI PMC

Kelleher J, Thornton KR, Ashander J, Ralph PL. 2018. Efficient pedigree recording for fast population genetics simulation. PLoS Comput. Biol. 14, e1006581 (10.1371/journal.pcbi.1006581) PubMed DOI PMC

Messer PW, Ellner SP, Hairston NG. 2016. Can population genetics adapt to rapid evolution? Trends Genet. 32, 408–418. (10.1016/j.tig.2016.04.005) PubMed DOI

Schneider A, Charlesworth B, Eyre-Walker A, Keightley PD. 2011. A method for inferring the rate of occurrence and fitness effects of advantageous mutations. Genetics 189, 1427–1437. (10.1534/genetics.111.131730) PubMed DOI PMC

Campos JL, Zhao L, Charlesworth B. 2017. Estimating the parameters of background selection and selective sweeps in Drosophila in the presence of gene conversion. Proc. Natl Acad. Sci. USA 114, E4762–E4771. (10.1073/pnas.1619434114) PubMed DOI PMC

Keightley PD, Trivedi U, Thomson M, Oliver F, Kumar S, Blaxter ML. 2009. Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines. Genome Res. 19, 1195–1201. (10.1101/gr.091231.109) PubMed DOI PMC

2002. Gene flow and the limits to natural selection. Trends Ecol. Evol. 17, 183–189. (10.1016/S0169-5347(02)02497-7) DOI

Orr H. 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52, 935–949. (10.1111/j.1558-5646.1998.tb01823.x) PubMed DOI

Barton NH, Bengtsson BO. 1986. The barrier to genetic exchange between hybridising populations. Heredity 57, 357–376. (10.1038/hdy.1986.135) PubMed DOI

Aeschbacher S, Selby JP, Willis JH, Coop G. 2017. Population-genomic inference of the strength and timing of selection against gene flow. Proc. Natl Acad. Sci. USA 114, 7061–7066. (10.1073/pnas.1616755114) PubMed DOI PMC

Lohse K, Chmelik M, Martin SH, Barton NH. 2016. Efficient strategies for calculating blockwise likelihoods under the coalescent. Genetics 202, 775–786. (10.1534/genetics.115.183814) PubMed DOI PMC

Booker TR, Yeaman S, Whitlock MC. 2019. Global adaptation confounds the search for local adaptation. bioRxiv 742247 (10.1101/742247) DOI

Charlesworth B. 1998. Measures of divergence between populations and the effect of forces that reduce variability. Mol. Biol. Evol. 15, 538–543. (10.1093/oxfordjournals.molbev.a025953) PubMed DOI

Cruickshank TE, Hahn MW. 2014. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol. Ecol. 23, 3133–3157. (10.1111/mec.12796) PubMed DOI

Setter D, Mousset S, Cheng X, Nielsen R, DeGiorgio M, Hermisson J. 2019. VolcanoFinder: genomic scans for adaptive introgression. bioRxiv 697987 (10.1101/697987) PubMed DOI PMC

Navarro A, Barton NH. 2003. Chromosomal speciation and molecular divergence–accelerated evolution in rearranged chromosomes. Science 300, 321–324. (10.1126/science.1080600) PubMed DOI

Mallet J. 1995. A species definition for the modern synthesis. Trends Ecol. Evol. 10, 294–299. (10.1016/0169-5347(95)90031-4) PubMed DOI

Edelman NB. et al. 2019. Genomic architecture and introgression shape a butterfly radiation. Science 366, 594–599. (10.1126/science.aaw2090) PubMed DOI PMC

Racimo F, Sankararaman S, Nielsen R, Huerta-Sánchez E. 2015. Evidence for archaic adaptive introgression in humans. Nat. Rev. Genet. 16, 359–371. (10.1038/nrg3936) PubMed DOI PMC

Servedio MR, Hermisson J. 2019. The evolution of partial reproductive isolation as an adaptive optimum. Evolution 74, 4–14. (10.1111/evo.13880) PubMed DOI

Seehausen O, Takimoto G, Roy D, Jokela J. 2008. Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol. Ecol. 17, 30–44. (10.1111/j.1365-294X.2007.03529.x) PubMed DOI

Fraïsse C, Gunnarsson PA, Roze D, Bierne N, Welch JJ. 2016. The genetics of speciation: insights from Fisher’s geometric model. Evol. Int. J. Org. Evol. 70, 1450–1464. (10.1111/evo.12968) PubMed DOI

Barton NH. 2017. How does epistasis influence the response to selection? Heredity 118, 96–109. (10.1038/hdy.2016.109) PubMed DOI PMC

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