Adaptive introgression in subdivided populations leaves distinct genomic footprints under global and local selection: a case study in Ciona intestinalis
Year: 2026
Type: preprint
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. 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 sitting on longer introgressed tracts, whereas recently reached populations have lower frequencies and 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 characterizing the footprint of introgressed tract length using local ancestry reconstruction. 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.
Authors: Manon Le Goff, Frédérique Cerqueira, Benjamin Penaud, Pierre-Alexandre Gagnaire, Frédérique Viard, Nicolas Bierne
Language: English
Subfield: Genetics
Domain: Life Sciences
Open Access status: green
OpenAlex ID: W7219685155
