Demography-driven and adaptive introgression in a hybrid zone of the Armeria syngameon

Syngameons represent networks of otherwise distinct species interconnected by limited gene exchange. Although most studies have focused on how species maintain their cohesiveness despite gene flow in these networks, there are additional relevant questions regarding the evolutionary dynamics of syngameons and their drivers, as well as the success of their members and the whole network. Using a ddRADseq approach, we analyzed the genetic structure, genomic clines and demographic history of a coastal hybrid zone involving two species of the Armeria (Plumbaginaceae) syngameon in Southern Spain. We inferred that one peripheral population of the sand dune-adapted A. pungens experienced genetic drift after a founder event and was subsequently introgressed by a local more abundant pinewood congener, A. macrophylla. This led to plastid capture resulting in extensive plastid DNA haplotype sharing between the two species across the whole hybrid zone. Genomic cline analysis identified bidirectional introgression, but more outliers with an excess ancestry of A. pungens than of A. macrophylla, which suggests A. pungens alleles are being selected for. This is consistent with the findings that A. pungens phenotype is selected for in open habitats. This scenario implies that bidirectional introgression is, on the one side, driven by demographic forces towards the immigrant range-edge bottlenecked population of A. pungens, which reduces its risk of stochastic extinction and increases its evolutionary potential as a novel hybrid lineage. On the other side, introgression towards A. macrophylla is driven by selection of alleles with A. pungens ancestry, enabling individuals to grow in open highly-irradiated habitats.