Phylogeography and climate shape the quantitative genetic landscape and range-wide plasticity of a prevalent conifer

Abstract

The contribution of genetic adaptation and plasticity to intraspecific phenotypic variability remains insufficiently studied in long-lived plants, as well as the relevance of neutral versus adaptive processes determining such divergence. We examined the importance of phylogeographic structure and climate in modulating genetic and plastic changes and their interdependence in fitness-related traits of a widespread Mediterranean conifer (Pinus pinaster). Four marker-based, previously defined neutral classifications along with two ad hoc climate-based categorizations of 123 range-wide populations were analyzed for their capacity to summarize genetic and plastic effects of height growth and survival (age 20) in 15 common gardens. The plasticity of tree height and differential survival were interpreted through mixed modeling accounting for heteroscedasticity in the genotype-by-environment dataset. The analysis revealed a slight superiority of phylogeographic classifications over climate categorizations on the explanation of genetic and plastic effects, which suggests that neutral processes can be at least as important as isolation by climate as a driving factor of evolutionary divergence in a prevalent pine. The best phylogeographic classification involved eight geographically discrete genetic groups, which explained 92% (height) and 52% (survival) of phenotypic variability, including between-group mean differentiation and differential expression across trials. For height growth, there was high predictability of plastic group responses described by different reaction norm slopes, which were unrelated to between-group mean differentiation. The latter differences (amounting to ca. 40% among groups) dominated intraspecific performance across trials. Local adaptation was evident for genetic groups tested in their native environments in terms of tree height and, especially, survival. This finding was supported by Q_ST > F_ST estimates. Additionally, our range-wide evaluation did not support a general adaptive syndrome by which less reactive groups to ameliorated conditions would be associated with high survival and low growth. In fact, a lack of relationship between mean group differentiation, indicative of genetic adaptation, and predictable group plasticity for height growth suggests different evolutionary trajectories of these mechanisms of phenotypic divergence. Altogether, the existence of predictable adaptive-trait phenotypic variation for the species, involving both genetic differentiation and plastic effects, should facilitate integrating genomics and environment into decision-making tools to assist forests in coping with climate change.