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

ABSTRACT

Combating the current biodiversity crisis requires the accurate documentation of population responses to human-induced ecological change. However, our ability to pinpoint population responses to human activities is often limited to the analysis of populations studied well after the fact. Museum collections preserve a record of population responses to anthropogenic change that 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 nearly 90% of coastal habitats occupied by the Savannah sparrow (Passerculus sandwichensis) in California. We sequenced 219 sparrows collected from 1889 to 2017 across the state of California using an exome capture approach. Spatial-temporal analyses of genetic diversity found that the amount of habitat lost was not predictive of genetic diversity loss. Sparrow populations from southern California historically exhibited lower levels of genetic diversity and experienced the most significant temporal declines in genetic diversity. Despite experiencing the greatest levels of habitat loss, we found that genetic diversity in the San Francisco Bay area remained relatively high. This was potentially related to an observed increase in gene flow into the Bay Area from other populations. While gene flow may have minimized genetic diversity declines, we also found that immigration from inland freshwater-adapted populations into tidal marsh populations led to the erosion of divergence at loci associated with tidal marsh adaptation. Shifting patterns of gene flow through time in response to habitat loss may thus contribute to negative fitness consequences and outbreeding depression. Together, our results underscore the importance of tracing the genomic trajectories of multiple populations over time to address issues of fundamental conservation concern.