Linking genome size variation to phenotypic selection on target traits.

Genome size (GS) is known to be highly variable among angiosperm species. However, this variation can also occur within species. Both interspecific and intraspecific variations in GS have been often found to be linked to phenotypic traits. Therefore, selective pressures acting on these target traits may indirectly shape GS evolution within and among species. However, the processes linking selective pressures to GS evolution are typically studied at broad phylogenetic scales, often overlooking how these processes operate at the microevolutionary level, where selection acts on standing variation within species. Recently diverging species or independently evolving lineages offer ideal settings to test whether selection shaping GS variation within lineages is reflected in patterns of GS variation among them, thereby linking microevolutionary and macroevolutionary processes. Here, we combined flow cytometric estimates of GS with measurements of leaf and floral traits, known to be targets of selective pressures, in both common garden and wild populations of two recently diverged Dianthus rupicola lineages. Then, we tested for an allometric relationship between GS and such phenotypic traits. Finally, we characterized the biotic and abiotic environment of wild populations and quantified plant reproductive success to identify selective pressures acting on traits showing an allometric relationship with GS. We found substantial GS variation, primarily driven by differences between the two lineages, but also occurring within lineages. GS showed a strong allometric relationship with two leaf traits, that is, stomata area and epidermal cell dimension, and one floral trait, that is, style length, in both lineages. Leaf traits reflected similar patterns of local adaptation to the edaphic environment in the two lineages, whereas divergent biotic pressures between lineages were associated with variation in style length. Our selection analysis revealed that style length was negatively associated with plant reproductive success in the lineage interacting with the pre-dispersal seed predator Hadena, while the opposite trend was observed in the lineage where this interaction is absent. By demonstrating how ecological factors shape traits covarying with GS both within and between lineages, this study provides a valuable framework to bridge micro- and macroevolutionary processes in GS evolution.