Genomic data reveal the biogeographic and demographic history of Ammospiza sparrows in northeast tidal marshes

<p><b><i>Aim: </i></b>Shaped by both climate change and sea-level rise, tidal salt marshes represent ephemeral systems that are home to only a few, highly specialized species. The dynamic ecological histories and spatial complexities of these habitats, however, render it challenging to reconstruct the complete biogeographic histories of their endemic taxa. Here, we leverage three species of North American <i>Ammospiza </i>sparrows that inhabit tidal marshes ( <i>Ammospiza caudacuta</i>, <i>A. maritima</i>, and <i>A. n. subvirgatus</i>) and closely related freshwater species to demonstrate the utility of whole-genome data in resolving demographic and evolutionary history as it relates to divergence and dispersal events in ephemeral ecosystems. We employ a combination of demographic and biogeographic reconstructions to shed new light on the colonization history of freshwater-saline environments in this system.</p> <p><b><i>Location: </i></b>North America</p> <p><b><i>Taxon: </i></b> <i>Ammospiza Sparrows</i></p> <p><b><i>Methods: </i></b>We sequenced whole genomes from <i>Ammospiza </i>sparrows to address our objectives. We conducted phylogenomic analyses and reconstructed the demographic and biogeographic history of this clade based on 21 million SNPs from 54 total individuals.</p> <p><b><i>Results: </i></b>Phylogenies based on several million SNPs supported several well-resolved clades that predominantly corresponded to their prior species designations. Phylogenetic and biogeographic reconstructions suggest a series of saltwater to freshwater colonization events within this group, with some endemic taxa exhibiting associations with tidal marsh habitat over longer evolutionary time scales and some habitat transitions occurring as recently as 5,000 years ago. </p> <p><b><i>Main Conclusions: </i></b>Our reconstructions support a biogeographic hypothesis with fewer vicariance and dispersal events among <i>Ammospiza </i>sparrows that is in contrast with the currently supported evolutionary scenario. Biogeographic reconstructions further suggest saltwater to freshwater transitions in <i>A. n. subvirgatus </i>as opposed to the long hypothesized freshwater origin. Our results highlight the fact that reconstructing biogeographic and evolutionary dynamics in ephemeral systems poses challenges given the propensity for high turnover. This reinforces the importance of a multifaceted approach to biogeographic reconstructions in historically dynamic ecosystems.</p>