Rapid repeatable phenotypic and genomic adaptation following multiple introductions

Abstract

Uncovering the genomic basis of repeated adaption can provide important insights into the constraints and biases that limit the diversity of genetic responses. Demographic processes such as admixture or bottlenecks affect genetic variation underlying traits experiencing selection. The impact of these processes on the genetic basis of adaptation remains, however, largely unexamined empirically. We here test repeatability in phenotypes and genotypes along parallel climatic clines within the native North American and introduced European and Australian Ambrosia artemisiifolia ranges. To do this, we combined multiple lines of evidence from phenotype-environment associations, F_ST -like outlier tests, genotype-environment associations and genotype-phenotype associations. We used 853 individuals grown in common garden from 84 sampling locations, targeting 19 phenotypes, >83 k SNPs and 22 environmental variables. We found that 17%-26% of loci with adaptive signatures were repeated among ranges, despite alternative demographic histories shaping genetic variation and genetic associations. Our results suggest major adaptive changes can occur on short timescales, with seemingly minimum impacts due to demographic changes linked to introduction. These patterns reveal some predictability of evolutionary change during range expansion, key in a world facing ongoing climate change, and rapid invasive spread.

Keywords: Ambrosia artemisiifolia; climate adaptation; genotype-environment associations; genotype-phenotype associations; multiple introductions; rapid repeated adaptation.