Penguins are the only extant family of flightless diving birds. They currently comprise at least 18 species, distributed from polar to tropical environments in the Southern Hemisphere. The history of their diversification and adaptation to these diverse environments remains controversial. We used 22 new genomes from 18 penguin species to reconstruct the order, timing, and location of their diversification, to track changes in their thermal niches through time, and to test for associated adaptation across the genome. Our results indicate that the penguin crown-group originated during the Miocene in New Zealand and Australia, not in Antarctica as previously thought, and that Aptenodytes is the sister group to all other extant penguin species. We show that lineage diversification in penguins was largely driven by changing climatic conditions and by the opening of the Drake Passage and associated intensification of the Antarctic Circumpolar Current (ACC). Penguin species have introgressed throughout much of their evolutionary history, following the direction of the ACC, which might have promoted dispersal and admixture. Changes in thermal niches were accompanied by adaptations in genes that govern thermoregulation and oxygen metabolism. Estimates of ancestral effective population sizes (Ne) confirm that penguins are sensitive to climate shifts, as represented by three different demographic trajectories in deeper time, the most common (in 11 of 18 penguin species) being an increased Ne between 40 and 70 kya, followed by a precipitous decline during the Last Glacial Maximum. The latter effect is most likely a consequence of the overall decline in marine productivity following the last glaciation.
Climate shifts are key drivers of ecosystem change. Despite the critical importance of Antarctica and the Southern Ocean for global climate, the extent of climate-driven ecological change in this region remains controversial. In particular, the biological effects of changing sea ice conditions are poorly understood. We hypothesize that rapid postglacial reductions in sea ice drove biological shifts across multiple widespread Southern Ocean species. We test for demographic shifts driven by climate events over recent millennia by analyzing population genomic datasets spanning 3 penguin genera (Eudyptes,Pygoscelis, andAptenodytes). Demographic analyses for multiple species (macaroni/royal, eastern rockhopper, Adélie, gentoo, king, and emperor) currently inhabiting southern coastlines affected by heavy sea ice conditions during the Last Glacial Maximum (LGM) yielded genetic signatures of near-simultaneous population expansions associated with postglacial warming. Populations of the ice-adapted emperor penguin are inferred to have expanded slightly earlier than those of species requiring ice-free terrain. These concerted high-latitude expansion events contrast with relatively stable or declining demographic histories inferred for 4 penguin species (northern rockhopper, western rockhopper, Fiordland crested, and Snares crested) that apparently persisted throughout the LGM in ice-free habitats. Limited genetic structure detected in all ice-affected species across the vast Southern Ocean may reflect both rapid postglacial colonization of subantarctic and Antarctic shores, in addition to recent genetic exchange among populations. Together, these analyses highlight dramatic, ecosystem-wide responses to past Southern Ocean climate change and suggest potential for further shifts as warming continues.
Since at least the middle-Miocene, the Antarctic Polar Front (APF) and the Subtropical Front (STF) appear to have been the main drivers of diversification of marine biota in the Southern Ocean. However, highly migratory marine birds and mammals challenge this paradigm and the importance of oceanographic barriers. Eudyptes penguins range from the Antarctic Peninsula to subantarctic islands and some of the southernmost subtropical islands. Because of recent diversification, the number of species remains uncertain. Here we analyze two mtDNA (HVRI, COI) and two nuclear (ODC, AK1) markers from 13 locations of five putative Eudyptes species: rockhopper (E. filholi, E. chrysocome, and E. moseleyi), macaroni (E. chrysolophus) and royal penguins (E. schlegeli). Our results show a strong phylogeographic structure among rockhopper penguins from South America, subantarctic and subtropical islands supporting the recognition of three separated species of rockhopper penguins. Although genetic divergence was neither observed among macaroni penguins from the Antarctic Peninsula and sub-Antarctic islands nor between macaroni and royal penguins, population genetic analyses revealed population genetic structure in both cases. We suggest that the APF and STF can act as barriers for these species. While the geographic distance between colonies might play a role, their impact/incidence on gene flow may vary between species and colonies.
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