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 explored how the relationship between adaptive allele frequency and introgressed tract length differs between these two scenarios. During the spread of an adaptive wave, introgressed tracts are progressively eroded by recombination with the genetic background of the receiving species, so that tract length, like allele frequency, reflects the distance traveled by the wave. Under local adaptation, however, allele frequency depends on the local balance between selection and migration, generally breaking this relationship. Simulations predicted a positive correlation between allele frequency and tract length during the spread of an unconditionally advantageous allele, but no correlation under local adaptation. 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 evidence of a relationship between adaptive allele frequency and introgressed tract length, supporting a model of local adaptation rather than an ongoing travelling wave.