Marginal populations are evolutionarily heterogeneous: Genetic signatures of population marginality in four European conifers

Populations at ecological or geographic range limits experience distinctive genetic processes driven by demographic constraints, adaptation to atypical environments and reduced gene flow. These marginal populations can constitute valuable genetic resources, yet, the relationship between marginality and genetic variation remains poorly understood in forest trees. We investigated this relationship in four European conifers (Pinus pinea, Pinus pinaster, Pinus sylvestris and Taxus baccata), which share main life-history traits but represent contrasting demographic histories and evolutionary strategies. Across 230 native populations, we quantified six marginality indices related to climate, geography, or demographic history, together with five SNP-based genetic indicators describing inbreeding, genetic diversity and differentiation, genetic load, and genomic offset. Using a comparative multi-species framework, we assessed the influence of marginality on genetic indicators and evaluated the consistency of patterns across species. Historical (i.e., linked to the post-glacial colonization history) and climatic marginality mainly reflected species-specific evolutionary trajectories, whereas distance from the distribution centroid was consistently associated with lower genetic diversity and higher population differentiation across species. Importantly, marginality and genetic distinctiveness only partially overlapped, indicating that range-edge populations do not form a homogeneous evolutionary category. Overall, our findings highlight the key role of demographic isolation and historical processes in shaping genetic patterns at species' range limits. They also showed that marginal populations may represent either genetically vulnerable populations or reservoirs of unique evolutionary potential. Integrating genomic information with quantitative measures of marginality can improve assessment of population vulnerability, evolutionary resilience and conservation value in forest trees.