Temporal changes in genetic variation during the invasion of Lygodium japonicum in North America

Abstract

Premise of the study. Invasive species are now widespread and have detrimental ecological and economic impacts. They also offer opportunities to investigate rapid evolution in colonizing populations. Here, we leverage nuclear DNA from herbarium specimens of Lygodium japonicum, an invasive fern to 1) identify the putative source(s) of its invasion, 2) test for climate adaptation in its invaded range, and 3) characterize the effects of genetic bottlenecks on adaptive and neutral variation during its establishment. Methods. We use low-coverage genome skimming data from specimens spanning 1905 through 2017 to identify the source region(s) of the L. japonicum invasion of North America. We use a genotype-environment analysis of invaded range samples to identify genomic regions associated with local adaptation to variation in five bioclimatic variables. Finally, we compare heterozygosity between native and invasive individuals and their changes through time in non-coding, coding, and putatively adaptive loci. Key results. We identify mainland Asia as the most likely source region for this invasion. Our genotype-environment analysis found 144 candidate SNPs significantly associated with climatic variation in the invaded range, with precipitation of the driest month associated with the greatest number of SNPs, suggesting rapid genomic adaptation in the invaded range. Finally, we found conflicting trends in individual-level heterozygosity over time when analyzing different types of genetic variation: in non-coding loci, there was a small, yet significant decrease in genetic diversity, but in putatively adaptive loci we did not find evidence of a genetic bottleneck. Conclusions. Natural history collections provide exceptional opportunities to explore evolutionary processes, by capturing genomic sequences across time. Here, herbarium specimens reveal rapid evolution, maintenance of adaptative variation, and accumulation of noncoding diversity in the Lygodium japonicum invasion, highlighting the potential for adaptative variation to fuel the success of invasive species.