The genetic consequences of population marginality: A case study in maritime pine

Abstract

Aim: Marginal tree populations, either those located at the edges of the species' range or in suboptimal environments, are often a valuable genetic resource for biological conservation. However, there is a lack of knowledge about the genetic consequences of population marginality, estimated across entire species' ranges. Our study addresses this gap by providing information about several genetic indicators and their variability in marginal and core populations identified using quantitative marginality indices. Location: Southwestern Europe and North Africa. Methods: Using 10,185 SNPs across 82 populations of maritime pine (Pinus pinaster Ait.), a widespread conifer characterised by a fragmented range, we modelled the relationship of seven genetic indicators potentially related to population evolutionary resilience, namely genetic diversity (based on both all SNPs and outlier SNPs), inbreeding, genetic differentiation, recessive genetic load and genomic offset, with population geographical, demo-historical and ecological marginality (as estimated by nine quantitative indices). Models were constructed for both regional (introducing gene pool as a random factor) and range-wide spatial scales. Results: We showed a trend towards decreasing overall genetic diversity and increasing differentiation with geographic marginality, supporting the centre-periphery hypothesis (CPH). However, we found no correlation between population inbreeding and marginality, while geographically marginal populations had a lower recessive genetic load (only models without the gene pool effect). Ecologically marginal populations had a higher genomic offset, suggesting higher maladaptation to future climate, albeit some of these populations also had high genetic diversity for climate outliers. Main Conclusions: Overall genetic diversity (but not outlier-based estimates) and differentiation patterns support the CPH. Ecologically marginal populations and those at the southern edge could be more vulnerable to climate change due to higher climate maladaptation, as predicted by genomic offsets, and/or lower potentially adaptive genetic diversity. This risk is exacerbated by typically small effective population sizes and increasing human impact in marginal populations.