Spatial variation in population genomic responses to over a century of anthropogenic change within a tidal marsh songbird

Abstract

ABSTRACTHuman activities have wide-ranging impacts on natural populations, but our ability to pinpoint population responses to these activities is often limited to the analysis of populations studied well after the fact. Museum collections can provide critical baseline data on patterns of genetic diversity, connectivity, and population structure prior to the onset of human perturbation. Here, we leverage a spatially-replicated time series of specimens to document population genomic responses to the destruction of ∼90% of coastal habitats occupied by the Savannah sparrow (Passerculus sandwichensis) in California. We sequenced 219 sparrows collected from 1889-2017 across the state of California using an exome capture approach. Spatial-temporal analyses of genetic diversity indicate that sparrow populations from southern California historically exhibited lower levels of genetic diversity and have also experienced the most significant temporal declines in genetic diversity. In contrast, birds from the San Francisco Bay area exhibit near constant levels of genetic diversity, despite experiencing similar levels of habitat loss. Stable genetic diversity in Bay Area birds may stem from increased levels of gene flow from interior California populations. While greater levels of gene flow may prevent declines in genetic diversity, we also find that immigration from inland freshwater-adapted populations into tidal marsh populations has led to the erosion of divergence in loci associated with tidal marsh adaptation. Although gene flow can play an important role in mitigating inbreeding depression, our results point to the potential negative consequences of gene flow across environmental gradients on locally adapted populations.SIGNIFICANCEMuseum collections preserve a record of population responses to anthropogenic change. We analyzed genomic data from historic specimens to document the responses of coastal California Savannah sparrows to rampant tidal marsh loss over the past century. We find that temporal shifts in source-sink dynamics among populations allowed some populations to maintain high genetic diversity in the face of habitat loss, yet this led to the erosion of genetic divergence at loci associated with tidal marsh adaptation. Shifting patterns of gene flow through time in response to habitat loss may result in negative fitness consequences and outbreeding depression. This has important implications for the long-standing debate on assisted gene flow in populations threatened with inbreeding depression.