Population genomics of yellow-eyed penguins uncovers subspecies divergence and candidate genes linked to respiratory distress syndrome

Abstract

Yellow-eyed penguins (hoiho/takaraka, Megadyptes antipodes) are among the worlds rarest penguins and are regarded as a taonga (treasured) species in Aotearoa New Zealand. Since 2019, chicks on the New Zealand mainland have been affected by a deadly neonatal disease called respiratory distress syndrome (RDS), contributing to a decline to fewer than 143 breeding pairs. To investigate the putative genetic basis of this disease, we generated high-quality whole-genome data from 249 individuals spanning the species range, including from the New Zealand mainland (Northern range) and subantarctic Enderby and Campbell Islands (Southern). Population genomic analyses unexpectedly revealed three deeply divergent lineages with negligible gene flow, consistent with recognition of three distinct subspecies. Phylogenetic divergence dating suggests that these splits predate human arrival by several millennia, with the Northern lineage diverging from the Southern populations 5-16 ka. Genome scans for local adaptation revealed regions of strong differentiation, and genome-wide association analyses identified candidate immune and respiratory genes linked to RDS. In partnership with Ng[a]i Tahu, who hold indigenous guardianship over yellow-eyed penguins, we recommend recognition of three subspecies, urgent conservation action for the critically small and rapidly declining Northern subspecies, and the need for immediate population size and trend assessments for Auckland and Campbell Island populations.