Copy number variation contributes to parallel local adaptation in an invasive plant

Abstract

AbstractAdaptation is a critical determinant of the diversification, persistence, and geographic range limits of species. Yet the genetic basis of adaptation is often unclear and potentially underpinned by a wide range of mutational types – from single nucleotide changes to large-scale alterations of chromosome structure. Copy number variation (CNV) is thought to be an important source of adaptive genetic variation, as indicated by decades of candidate gene studies that point to CNVs underlying rapid adaptation to strong selective pressures. Nevertheless, population genomic studies of CNVs face unique logistical challenges not encountered by other forms of genetic variation. Consequently, few studies have systematically investigated the contributions of CNVs to adaptation at a genome-wide scale. We present a genome-wide analysis of CNV contributions to the adaptation of an invasive weed,Ambrosia artemisiifolia, across its native and invasive ranges in North America and Europe, respectively. CNVs show clear signatures of parallel local adaptation between native and invasive ranges, implying widespread reuse of CNVs during adaptation to shared geographic patterns of selection. Using a local principal component analysis to genotype CNV regions in historic samples that span the last two centuries, we identified 16 large CNV regions of up to 11.85 megabases in length, six of which show signals of rapid evolutionary change, with pronounced frequency shifts between historic and modern populations. Our results provide compelling genome-wide evidence that copy number variation underlies rapid adaptation over contemporary timescales of natural populations.Significance StatementUsing a population genomic approach, we identified copy number variation (CNVs) displaying parallel signatures of local adaptation across the native and introduced ranges of the invasive weedAmbrosia artemisiifolia. We further identified 16 large CNVs associated with ecologically important traits, including sex allocation and height, that show strong signatures of selection over space and time, along with dramatic temporal changes over the past several decades. These results highlight the importance of copy number variation in both local adaptation and rapid adaptation of invasive species.