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

Abstract

AbstractAimShaped by climate change and sea‐level rise, tidal salt marshes represent ephemeral systems that are home to only a few species. The dynamic ecological histories of these habitats, however, render it challenging to reconstruct the complete biogeographical histories of their endemic taxa. To better understand the evolutionary history of tidal marsh endemic sparrows, we employ genomic data to evaluate the timing and direction of tidal marsh colonization events and leverage these data to test a series of models describing the biogeographical history of our study taxa.LocationNorth America.TaxonAmmospiza Sparrows.MethodsWe sampled 54 individuals from the Ammospiza clade from freshwater and saltwater habitats. We sequenced whole genomes and generated a dataset containing 21 million SNPs. Detailed phylogenomic analyses were conducted to identify relationships between tidal marsh and freshwater species. These phylogenies were then used to date divergence times and reconstruct the biogeographical history of the clade as well as identify historic signals of introgression.ResultsPhylogenies based on several million SNPs supported well‐resolved clades that correspond to all previous species designations. Demographic modelling within A. nelsoni provided further resolution into the subspecies topology. Phylogenetic and biogeographical reconstructions support a series of saltwater to freshwater colonization events, 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.Main ConclusionsBiogeographical and phylogenomic reconstructions support an original freshwater origin of the Ammospiza sparrows currently inhabiting tidal marshes in North America. We also found strong evidence for a saltwater to freshwater transition in A. n. subvirgatus as opposed to the long hypothesized freshwater origin of this group. We conclude that the increased resolution from genomic data paired with an integrative framework of phylogenomic, demographic and biogeographical reconstructions is important for resolving evolutionary histories in complex and ephemeral environments.