Adaptive introgression in subdivided populations leaves distinct genomic footprints under global and local selection: a case study in Ciona intestinalis

Abstract Adaptive introgression, the transfer of beneficial alleles between species through hybridization, is increasingly recognized as an important source of adaptation to novel environments. However, the theory of adaptive introgression has primarily been developed for a single panmictic population, whereas many empirical examples involve spatially subdivided populations. In such systems, a low-frequency adaptive allele may either represent the leading edge of an adaptive travelling wave or occur in a subpopulation where the introgressed allele is locally selected against. We developed a simple prediction based on the relationship between adaptive allele frequency and introgressed tract length. Simulations predict a positive correlation during an ongoing sweep of an unconditionally beneficial allele, but no correlation under local adaptation. Tract erosion provides a recombination clock for time since introgression, which also determines the distance travelled by the adaptive wave and hence allele frequency in the former, whereas allele frequency is determined by local selection in the latter. We tested this prediction in a well-characterized case of adaptive introgression, in the sea squirt Ciona intestinalis , using haplotagging to reconstruct phased genomes and local ancestry. We found no relationship between adaptive allele frequency and introgressed tract length, providing additional support for a model of local adaptation rather than ongoing global selective sweep. Author summary Hybridization between species can transfer beneficial genetic variants from one species to another, enabling the latter to adapt to a new environment. However, such variants are not necessarily advantageous throughout the recipient species range. In geographically subdivided populations, a low-frequency introgressed allele may either have arrived recently or be selected against locally. Using simulations, we show that combining allele frequency with introgressed tract lengths clarifies this ambiguity, offering a straightforward method to distinguish between globally positive and locally varying selection. When an adaptive allele is beneficial everywhere, it spreads through populations as a travelling wave. Over time, recombination progressively shortens introgressed tracts. Populations reached first have higher frequencies of the adaptive allele on longer introgressed tracts, whereas recently reached populations have lower frequencies on shorter tracts. When selection varies among populations, this relationship disappears because allele frequency reflects local selection rather than the history of the adaptive wave. We tested this prediction in a confirmed case of adaptive introgression in a sea squirt species by reconstructing ancestry along chromosomes and measuring introgressed tract lengths. We found no correlation between allele frequency and introgressed tract length, supporting the hypothesis that variation in introgressed allele frequency reflects local selection rather than a traveling adaptive wave.