Abstract: Serpentine soils are characterized by high levels of heavy metals, low nutrient availability, and water scarcity, presenting significant ecological challenges for plant species. Soil variation associated with serpentine outcrops generates sharp environmental contrasts over short geographic distances, providing an opportunity for study of lineage divergence and population structure across a heterogeneous edaphic landscape. Here, we examine the evolutionary history of three often sympatric plant species, Lavandula stoechas L., Phlomis purpurea L. (both Lamiaceae), and Halimium atriplicifolium (Lam) Spach. (Cistaceae), which inhabit adjacent serpentine and non-serpentine habitat in the southern Iberian Peninsula. Using a comparative population genomic framework, we test whether serpentine populations represent distinct evolutionary lineages or parallel colonizations of this edaphic habitat, and to what degree genomic differentiation reflects both edaphic conditions and geographic isolation. Highly supported, maximum likelihood population phylogenies suggest repeated, parallel colonizations of serpentine habitat by all three species. The degree of isolation-by-distance and the geographic distribution of ancestral group membership in populations differ notably among these sympatric species. Demographic simulations revealed low to intermediate levels of recent, asymmetric gene flow, characterized by a directional genetic contribution from serpentine patches into adjacent non-serpentine populations, while genotype-environment associations identified potential candidate loci under edaphic selection. Significant variation in plant height among populations on differing soils represents environmentally associated phenotypic differentiation and suggests ecotypic differences, while the magnitude of this association varies among the species. Together, our results show that parallel radiation to serpentine habitat, population ancestry, isolation-by-distance and ongoing gene flow contribute differentially to population genomic structure in these three species.

Key words: ddRADseq, ecotype, edaphic differentiation, functional traits, gene flow, parallel evolution, population divergence