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

Abstract

Adaptation is a critical determinant of the diversification, persistence, and geographic range limits of species. Yet the genetic basis of adaptation is often unknown 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 contributing to the adaptation of an invasive weed, Ambrosia artemisiifolia - the first such study in an invasive pest. CNVs show clear signatures of parallel local adaptation between North American (native) and European (invaded) ranges, implying widespread reuse of CNVs during adaptation to shared heterogeneous patterns of selection. We used a local principal component analysis to genotype CNV regions in whole-genome sequences of samples collected over 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 variants - stretches of DNA that can be either present, absent, or in multiple copies - displaying parallel signatures of local adaptation across the native and introduced ranges of the invasive weed Ambrosia artemisiifolia. We further identified 16 large copy number variants, some associated with ecologically important traits including sex allocation and height, that show strong signatures of selection over space, along with dramatic temporal changes over the past several decades. These results highlight the importance of an often-overlooked form of genomic variation in both local adaptation and rapid adaptation of invasive species.