Evolution of Population Structure and Life History Types in Eelgrass (Zostera marina)

Abstract

Foundation species structure the ecosystems they inhabit, and their resilience is key to maintaining the stability of the environments that they support. The seagrass Zostera marina (eelgrass) is one such species with high ecological relevance, distributed across geographically complex estuarine systems throughout the northern temperate hemisphere. Rapid meadow declines have drawn increasing conservation attention, yet the success of recovery strategies may be hindered by a lack of data on population genetic diversity, connectivity, and the adaptive variation underlying ecologically important traits. In eelgrass, the annual strategy, which reproduces predominantly through seeds, may aid recovery following disturbance, while perennial clonal growth supports persistence under stable conditions. This dissertation employs genomic approaches to characterize the genetic structure, local adaptation, and evolution of key life history variation in eelgrass. (Chapter 1) I first characterized population genetic structure and connectivity across the Puget Sound and outer Pacific Coast, where eelgrass is distributed across geographically complex habitats and has experienced population declines. Using RAD sequencing across 16 Washington locations and outer-coast sites in Oregon and California, I found that clonality was more prevalent within the Puget Sound than along the outer coast, and that pairwise differentiation varied markedly (Fst = 0.02–0.42), with significant isolation by distance. Population assignment identified four major groups corresponding to the outer coast, north and south Puget Sound, and the Hood Canal. All populations exhibited small effective sizes and little contemporary gene flow, and outlier analyses revealed signatures of local adaptation that primarily reflected geography. Altogether, these findings provide a basis for informing management across the State, such as delineating management units. (Chapter 2) I next asked whether annual and perennial life histories in eelgrass that occur in close proximity represent locally adapted genetic variation or plastic phenotypes. Combining a common-garden reciprocal transplant experiment with population genetic analyses in a single estuary (Willapa Bay), I found no differential survival to maturity, but a greater likelihood of flowering in annual-sourced plants and branching in perennial-sourced shoots. Reproductive trait performance was greater for local individuals, indicating adaptive differentiation, and fine-scale structure separated life history types, distinguished mainly by whether seedlings flowered, regardless of geographic source or outplant location. These results provide the first evidence of genetic control of life history in the species, offer insight into the adaptive capacity of this variation, and establish a basis for considering it in restoration practices. (Chapter 3) Last, genetic differentiation between isolated regions exceeds that between life histories within a site, raising the possibility of independent evolutionary transitions between annual and perennial strategies. Thus, I investigated whether life history variation represents replicated evolution across the species range, and whether there was a shared genomic basis across locations. I used whole-genome sequencing to reconstruct evolutionary relationships and test for parallel divergence for annual and perennial plants across ten sites spanning the eastern Pacific and both Atlantic coasts. Phylogenetic inference supported multiple transitions between strategies, with the grouping of samples driven primarily by geography (a major division between Pacific and Atlantic samples). Parallel genomic divergence was identified across Pacific but not Atlantic life history types, and repeated allele frequency change at a subset of candidate loci (some implicated in life history divergence in other plant systems) indicated a partially shared genomic basis. From these results, I concluded that annual and perennial strategies have evolved repeatedly across the range, with shared standing variation underlying parallel divergence in the Pacific and more independent evolution of life histories in the Atlantic. Together, these chapters show that eelgrass population structure is governed by geography and oceanography, that annual and perennial strategies can be adaptively differentiated when co-located in close proximity, and that these life histories have evolved repeatedly across ocean basins, with parallel divergence within the Pacific likely originating from shared standing variation and a transition toward more independent genomic changes in the Atlantic. These findings contribute to our understanding of population structure, adaptation, and replicated evolution in a foundation species, informing the trait-based management of a declining foundation species and advancing a broader understanding of replicated evolution in the wild.