Adaptive Genetic Differentiation Between Spatially Proximate Annual and Perennial Life History Types of a Marine Foundation Species.

Abstract

Diversity in life expectancy is common in flowering plants. In the seagrass Zostera marina, a vital foundation species in estuarine ecosystems, annual and perennial varieties occur in close proximity, raising the question of whether these lifespan strategies represent locally adapted genetic variation or plastic phenotypes influenced by the environment. Our study combined field transplant experiments and population genetic analyses to investigate the phenotypic (juvenile survival, flowering, and branching) and genetic differentiation between paired annual and perennial eelgrass meadows in a single estuary (Willapa Bay, northeast Pacific Ocean, USA) over one growing season. A common garden reciprocal transplant experiment, based on seedlings, demonstrated no differential survival to maturity but revealed a greater likelihood of flowering in annual-sourced plants and branching in perennial-sourced shoots. Further, reproductive trait performance was greater for local individuals compared to non-local ones, which indicates adaptive differentiation. Experimental transplants of annual-sourced seeds into both annual and perennial-dominated sites flowered within a few months, regardless of overwintering conditions. Estimates of population structure based on 325 SNPs (RAD-seq) revealed fine-scale population structure between life history types. Population assignment tests identified two distinct groups, distinguished mainly by whether the seedling flowered or not, regardless of geographic source or outplant location. Tests for outlier loci between the two life histories provided further evidence of local adaptation. These insights shed light on the factors governing life cycle variation and resilience in Z. marina, offering implications for the evolution and trait-based management of eelgrass populations.