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      New Miocene Fossils and the History of Penguins in Australia

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          Abstract

          Australia has a fossil record of penguins reaching back to the Eocene, yet today is inhabited by just one breeding species, the little penguin Eudyptula minor. The description of recently collected penguin fossils from the re-dated upper Miocene Port Campbell Limestone of Portland (Victoria), in addition to reanalysis of previously described material, has allowed the Cenozoic history of penguins in Australia to be placed into a global context for the first time. Australian pre-Quaternary fossil penguins represent stem taxa phylogenetically disparate from each other and E. minor, implying multiple dispersals and extinctions. Late Eocene penguins from Australia are closest to contemporaneous taxa in Antarctica, New Zealand and South America. Given current material, the Miocene Australian fossil penguin fauna is apparently unique in harbouring ‘giant penguins’ after they went extinct elsewhere; and including stem taxa until at least 6 Ma, by which time crown penguins dominated elsewhere in the southern hemisphere. Separation of Australia from Antarctica during the Palaeogene, and its subsequent drift north, appears to have been a major event in Australian penguin biogeography. Increasing isolation through the Cenozoic may have limited penguin dispersal to Australia from outside the Australasian region, until intensification of the eastwards-flowing Antarctic Circumpolar Current in the mid-Miocene established a potential new dispersal vector to Australia.

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          Early penguin fossils, plus mitochondrial genomes, calibrate avian evolution.

          Testing models of macroevolution, and especially the sufficiency of microevolutionary processes, requires good collaboration between molecular biologists and paleontologists. We report such a test for events around the Late Cretaceous by describing the earliest penguin fossils, analyzing complete mitochondrial genomes from an albatross, a petrel, and a loon, and describe the gradual decline of pterosaurs at the same time modern birds radiate. The penguin fossils comprise four naturally associated skeletons from the New Zealand Waipara Greensand, a Paleocene (early Tertiary) formation just above a well-known Cretaceous/Tertiary boundary site. The fossils, in a new genus (Waimanu), provide a lower estimate of 61-62 Ma for the divergence between penguins and other birds and thus establish a reliable calibration point for avian evolution. Combining fossil calibration points, DNA sequences, maximum likelihood, and Bayesian analysis, the penguin calibrations imply a radiation of modern (crown group) birds in the Late Cretaceous. This includes a conservative estimate that modern sea and shorebird lineages diverged at least by the Late Cretaceous about 74 +/- 3 Ma (Campanian). It is clear that modern birds from at least the latest Cretaceous lived at the same time as archaic birds including Hesperornis, Ichthyornis, and the diverse Enantiornithiformes. Pterosaurs, which also coexisted with early crown birds, show notable changes through the Late Cretaceous. There was a decrease in taxonomic diversity, and small- to medium-sized species disappeared well before the end of the Cretaceous. A simple reading of the fossil record might suggest competitive interactions with birds, but much more needs to be understood about pterosaur life histories. Additional fossils and molecular data are still required to help understand the role of biotic interactions in the evolution of Late Cretaceous birds and thus to test that the mechanisms of microevolution are sufficient to explain macroevolution.
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            Reorganization of Southern Ocean plankton ecosystem at the onset of Antarctic glaciation.

            The circum-Antarctic Southern Ocean is an important region for global marine food webs and carbon cycling because of sea-ice formation and its unique plankton ecosystem. However, the mechanisms underlying the installation of this distinct ecosystem and the geological timing of its development remain unknown. Here, we show, on the basis of fossil marine dinoflagellate cyst records, that a major restructuring of the Southern Ocean plankton ecosystem occurred abruptly and concomitant with the first major Antarctic glaciation in the earliest Oligocene (~33.6 million years ago). This turnover marks a regime shift in zooplankton-phytoplankton interactions and community structure, which indicates the appearance of eutrophic and seasonally productive environments on the Antarctic margin. We conclude that earliest Oligocene cooling, ice-sheet expansion, and subsequent sea-ice formation were important drivers of biotic evolution in the Southern Ocean.
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              Multiple cenozoic invasions of Africa by penguins (Aves, Sphenisciformes).

              Africa hosts a single breeding species of penguin today, yet the fossil record indicates that a diverse array of now-extinct taxa once inhabited southern African coastlines. Here, we show that the African penguin fauna had a complex history involving multiple dispersals and extinctions. Phylogenetic analyses and biogeographic reconstructions incorporating new fossil material indicate that, contrary to previous hypotheses, the four Early Pliocene African penguin species do not represent an endemic radiation or direct ancestors of the living Spheniscus demersus (blackfooted penguin). A minimum of three dispersals to Africa, probably assisted by the eastward-flowing Antarctic Circumpolar and South Atlantic currents, occurred during the Late Cenozoic. As regional sea-level fall eliminated islands and reduced offshore breeding areas during the Pliocene, all but one penguin lineage ended in extinction, resulting in today's depleted fauna.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                26 April 2016
                2016
                : 11
                : 4
                : e0153915
                Affiliations
                [1 ]School of Biological Sciences, Monash University, Clayton, Victoria, Australia
                [2 ]Palaeontology, Museum Victoria, Melbourne, Victoria, Australia
                [3 ]School of Earth Sciences, University of Melbourne, Victoria, Australia
                [4 ]CSIRO Radiogenic Isotope Facility, North Ryde, Sydney, New South Wales, Australia
                Smithsonian Institution, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: TP EMGF. Performed the experiments: TP EMGF SJG ET TA. Analyzed the data: TP EMGF SJG ET TA. Contributed reagents/materials/analysis tools: TP EMGF SJG TA. Wrote the paper: TP EMGF SJG.

                Article
                PONE-D-15-32526
                10.1371/journal.pone.0153915
                4845988
                27115739
                52906fc7-9c80-4328-81b7-7654245894f0
                © 2016 Park et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 24 July 2015
                : 6 April 2016
                Page count
                Figures: 5, Tables: 3, Pages: 21
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000923, Australian Research Council;
                Award ID: DP0558150
                Award Recipient :
                Grant number: DP0558150, Australian Research Council, funder's website: www.arc.gov.au, author who received funding: SJG and ET. Funding was for fieldwork associated with geologic data collection and subsequent stratigraphic analyses only. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Birds
                Seabirds
                Penguins
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                Paleontology
                Fossils
                Earth Sciences
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                Neogene Period
                Miocene Epoch
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                Oceania
                Australia
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                Musculoskeletal System
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