Post-invasion selection acts on standing genetic variation despite a severe founding bottleneck

Invasive populations often have lower genetic diversity relative to the native-range populations from which they derive. 1 Dlugosch K.M. Parker I.M. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol. Ecol. 2008; 17: 431-449 Crossref PubMed Scopus (1378) Google Scholar ,2 Uller T. Leimu R. Founder events predict changes in genetic diversity during human-mediated range expansions. Glob. Change Biol. 2011; 17: 3478-3485 Crossref Scopus (105) Google Scholar Despite this, many biological invaders succeed in their new environments, in part due to rapid adaptation. 3 Yin X. Martinez A.S. Sepúlveda M.S. Christie M.R. Rapid genetic adaptation to recently colonized environments is driven by genes underlying life history traits. BMC Genomics. 2021; 22: 269 Crossref PubMed Scopus (8) Google Scholar ,4 Prentis P.J. Wilson J.R. Dormontt E.E. Richardson D.M. Lowe A.J. Adaptive evolution in invasive species. Trends Plant Sci. 2008; 13: 288-294 Abstract Full Text Full Text PDF PubMed Scopus (656) Google Scholar ,5 Szűcs M. Vahsen M.L. Melbourne B.A. Hoover C. Weiss-Lehman C. Hufbauer R.A. Rapid adaptive evolution in novel environments acts as an architect of population range expansion. Proc. Natl. Acad. Sci. USA. 2017; 114: 13501-13506 Crossref PubMed Scopus (95) Google Scholar ,6 Vandepitte K. De Meyer T. Helsen K. Van Acker K. Roldán-Ruiz I. Mergeay J. Honnay O. Rapid genetic adaptation precedes the spread of an exotic plant species. Mol. Ecol. 2014; 23: 2157-2164 Crossref PubMed Scopus (92) Google Scholar Therefore, the role of genetic bottlenecks in constraining the adaptation of invaders is debated. 7 Estoup A. Ravigné V. Hufbauer R. Vitalis R. Gautier M. Facon B. Is there a genetic paradox of biological invasion?. Annu. Rev. Ecol. Evol. Syst. 2016; 47: 51-72 Crossref Scopus (216) Google Scholar ,8 Schrieber K. Lachmuth S. The genetic paradox of invasions revisited: the potential role of inbreeding × environment interactions in invasion success. Biol. Rev. Camb. Philos. Soc. 2017; 92: 939-952 Crossref PubMed Scopus (102) Google Scholar ,9 Rollins L.A. Moles A.T. Lam S. Buitenwerf R. Buswell J.M. Brandenburger C.R. Flores-Moreno H. Nielsen K.B. Couchman E. Brown G.S. et al. High genetic diversity is not essential for successful introduction. Ecol. Evol. 2013; 3: 4501-4517 Crossref PubMed Scopus (58) Google Scholar ,10 Roman J. Darling J.A. Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol. Evol. 2007; 22: 454-464 Abstract Full Text Full Text PDF PubMed Scopus (662) Google Scholar Here, we use whole-genome resequencing of samples from a 10-year time-series dataset, representing the natural invasion of the Asian honey bee (Apis cerana) in Australia, to investigate natural selection occurring in the aftermath of a founding event. We find that Australia's A. cerana population was founded by as few as one colony, whose arrival was followed by a period of rapid population expansion associated with an increase of rare variants. 11 North H.L. McGaughran A. Jiggins C.D. Insights into invasive species from whole-genome resequencing. Mol. Ecol. 2021; 30: 6289-6308 Crossref PubMed Scopus (44) Google Scholar The bottleneck resulted in a steep loss of overall genetic diversity, yet we nevertheless detected loci with signatures of positive selection during the first years post-invasion. When we investigated the origin of alleles under selection, we found that selection acted primarily on the variation introduced by founders and not on the variants that arose post-invasion by mutation. In all, our data highlight that selection on standing genetic variation can occur in the early years post-invasion, even where founding bottlenecks are severe.