Rapid radiation of Southern Ocean shags in response to receding sea ice

Abstract

Aim: Understanding how natural populations respond to climatic shifts is a fundamental goal of biological research in a fast-changing world. The Southern Ocean represents a fascinating system for assessing large-scale climate-driven biological change, as it contains extremely isolated island groups within a predominantly westerly, circumpolar wind and current system. Blue-eyed shags represent a paradoxical seabird radiation—a circumpolar distribution implies strong dispersal capacity yet their species-rich nature suggests local adaptation and isolation. Here we attempt to resolve this paradox in light of the history of repeated cycles of climate change in the Southern Ocean. Location: Southern Ocean. Taxa: 16 species and subspecies of blue-eyed shags (Phalacrocoracidae; Leucocarbo spp.). Methods: We use mitochondrial and nuclear sequence data from individuals across the geographical range of the genus to conduct the first comprehensive, time-calibrated phylogenetic analyses and ancestral-range biogeographical reconstructions of the blue-eyed shags. Results: The origins of many island-endemic lineages are remarkably recent, consistent with a recent high-latitude circumpolar radiation in the Pliocene or Early Pleistocene. This recent sub-Antarctic expansion contrasts with significantly deeper lineages detected in South America and, to a lesser extent, New Zealand. These regions, particularly South America, acted as glacial refugia and sources for multiple waves of post-glacial dispersal. Main conclusions: The blue-eyed shag paradox is resolved, with at least two waves of dispersal, linked to interglacial cycles, explaining the current distribution and diversity. Descendants of a Pliocene or Early Pleistocene wave of dispersal out of South America survive in the New Zealand region. In contrast, taxa distributed on sub-Antarctic islands originated much later, possibly since the Last Glacial Maximum. Blue-eyed shags therefore represent a powerful model system—comprising several natural replicates—for studying the early stages of founder-event speciation and adaptation in a Southern-Ocean bird group.