Extreme elevational migration spurred cryptic speciation in giant hummingbirds

The eco-evolutionary drivers of species niche expansion or contraction are critical for biodiversity but challenging to infer. Niche expansion may be promoted by local adaptation or constrained by physiological performance trade-offs. For birds, evolutionary shifts in migratory behavior permit broadening of the climatic niche by expansion into varied, seasonal environments. Broader niches can be short-lived if diversifying selection and geography promote speciation and niche subdivision across climatic gradients. To illuminate niche breadth dynamics, we can ask how ‘outlier’ species defy constraints. Of the 363 hummingbird species, the giant hummingbird (Patagona gigas) has the broadest climatic niche by a large margin. To test the roles of migratory behavior, performance trade-offs, and genetic structure in maintaining its exceptional niche breadth, we studied its movements, respiratory traits, and population genomics. Satellite and light-level geolocator tracks revealed an >8,300-km loop migration over the Central Andean Plateau. This migration included a three-week, ~4,100 m ascent punctuated by upward bursts and pauses, resembling the acclimatization routines of human mountain climbers, and accompanied by surging blood-hemoglobin concentrations. Extreme migration was accompanied by deep genomic divergence from high-elevation resident populations, with decisive postzygotic barriers to gene flow. The two forms occur side-by-side but differ almost imperceptibly in size, plumage, and respiratory traits. The high-elevation resident taxon is the world’s largest hummingbird, a new species that we describe and name here. The giant hummingbirds demonstrate evolutionary limits on niche breadth: When the ancestral niche expanded due to evolution (or loss) of an extreme migratory behavior, speciation followed.

Methods
Data were collected from wild-caught individuals in the field and from museum specimens spanning 154 years. We used satellite transmitters and geolocators to track giant hummingbirds from sea-level breeding areas in Chile to non-breeding areas. We collected respiratory trait data from >175 individuals across the elevational range and from Chile to Peru from 2006–2021. We analyzed genomic sequences from 101 individuals (whole genomes and ultra-conserved elements) across the geographic range; genomic data were taken from flash-frozen tissues and toe pads of historic museum specimens. All analysis code and scripts may be found on GitHub (https://github.com/jlwilliamson/jlwilliamson-patagona-blood-migration-genomics; DOI: 10.5281/zenodo.10975589); genomic data on Sequence Read Archive; and migration data on MoveBank (Project ID 3594892529). Specimen data are available in the Arctos database (www.arctosdb.org).