Phylogenomics, introgression, and demographic history of extant flamingos (Aves: Phoenicopteridae)

The colorful and charismatic flamingos (Phoenicopteridae) have long been the focus of conservation studies, particularly because many of them are currently threatened. Additionally, they serve as flagship species, underscoring the importance of protecting and sustainably using the unique wetlands they inhabit. Although genome-wide genetic data have proven invaluable for both taxonomy and conservation, its application in this context remains limited, primarily due to restricted access to reference genomes of non-model species. In this study, we performed the first genome-wide analysisof thephylogeneticrelationships, introgression, demographic history, and current genomic diversity of all living flamingo species. Our phylogenomic analysis, utilizing mitogenome and nuclear autosomal genomes, confirms the existence of two main clades within the flamingo species tree: the deep-keeled clade (Phoenicopterus) and the shallow-keeled clade (Phoenicoparrus and Phoeniconaias), as previously proposed based on mandibular morphology. Furthermore, our study suggests that the well-supported shallow-keeled clade warrants the synonymization of Phoeniconaias under Phoenicoparrus. Next, we recovered divergence timing that places flamingo origins during the Pliocene between 3.7 and 4.1 Mya, which is substantially more recent than previously estimated. We also detected widespread historical gene flow across flamingo lineages, including signatures consistent with deep ancestral introgression. Our results further suggest that physical and behavioral barriers are important in maintaining species boundaries within the shallow-keeled clade. Next, genome-wide diversity, assessed by nucleotide diversity and runs of homozygosity, was consistent with the current threat status based on census size. More specific trends of genetic diversity were obtained through demographic analyses that revealed species-specific expansion and contraction events that correlate with the glacial-interglacial cycles of the Pleistocene, occurring during the last 0.5 to 2 Mya, which alternated between globally cooler/drier and warmer/wetter climates. Given evident declines in effective population sizes during historical periods of very warm temperatures, the flamingos will likely require additional conservation efforts with predicted warming climates in the Anthropocene.