Evolutionary history of the salt marsh harvest mouse mitogenome is concordant with ancient patterns of sea level rise

Coastal wetland ecosystems support unique biodiversity and are imminently threatened by climate change-driven sea level rise. However, the impact of climate change on their demographic and evolutionary histories is poorly understood. To improve our understanding, we examined how past climatic events have shaped the evolutionary history of the salt marsh harvest mouse (Reithrodontomys raviventris), an endangered species and a salt marsh habitat specialist, completely restricted to coastal wetlands in the San Francisco Estuary (SFE). We used whole mitochondrial genome sequences of 102 salt marsh harvest mice to characterize phylogeography and demographic history. Then, we predicted the ancient distribution of salt marsh habitat and examined correspondence between divergence, demographic history, and changes in ancient marsh habitat caused by sea level rise. A Bayesian Skyline Plot revealed demographic expansions during periods of sea level rise, particularly during the formation of the modern SFE (similar to 10 kya), and rapid decline consistent with recent anthropogenic landscape change. Bayesian estimates of divergence time were consistent with subspecies divergence similar to 10 kya, and subpopulation divergence similar to 5 kya, consistent with multiple episodes of vicariance caused by Holocene sea level rise. Spatial Analysis of Molecular Variance and Phi(ST) revealed a mismatch between the morphological and molecular subspecies assignment of two populations. Our study implicates sea level rise as a force of demographic change and evolutionary divergence in coastal marsh ecosystems. Our study also aids conservation of an endangered species by clarifying genetic subspecies boundaries and highlighting the unique nature of isolated populations that are increasingly threatened by modern sea level rise.