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      Mid-Cenozoic climate change, extinction, and faunal turnover in Madagascar, and their bearing on the evolution of lemurs

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          Abstract

          Background

          Was there a mid-Cenozoic vertebrate extinction and recovery event in Madagascar and, if so, what are its implications for the evolution of lemurs? The near lack of an early and mid-Cenozoic fossil record on Madagascar has inhibited direct testing of any such hypotheses. We compare the terrestrial vertebrate fauna of Madagascar in the Holocene to that of early Cenozoic continental Africa to shed light on the probability of a major mid-Cenozoic lemur extinction event, followed by an “adaptive radiation” or recovery. We also use multiple analytic approaches to test competing models of lemur diversification and the null hypothesis that no unusual mid-Cenozoic extinction of lemurs occurred.

          Results

          Comparisons of the terrestrial vertebrate faunas of the early Cenozoic on continental Africa and Holocene on Madagascar support the inference that Madagascar suffered a major mid-Cenozoic extinction event. Evolutionary modeling offers some corroboration, although the level of support varies by phylogeny and model used. Using the lemur phylogeny and divergence dates generated by Kistler and colleagues, RPANDA and TESS offer moderate support for the occurrence of unusual extinction at or near the Eocene-Oligocene (E-O) boundary (34 Ma). TreePar, operating under the condition of obligate mass extinction, found peak diversification at 31 Ma, and low probability of survival of prior lineages. Extinction at the E-O boundary received greater support than other candidate extinctions or the null hypothesis of no major extinction. Using the lemur phylogeny and divergence dates generated by Herrera & Dàvalos, evidence for large-scale extinction diminishes and its most likely timing shifts to before 40 Ma, which fails to conform to global expectations.

          Conclusions

          While support for large-scale mid-Cenozoic lemur extinction on Madagascar based on phylogenetic modeling is inconclusive, the African fossil record does provide indirect support. Furthermore, a major extinction and recovery of lemuriforms during the Eocene-Oligocene transition (EOT) would coincide with other major vertebrate extinctions in North America, Europe, and Africa. It would suggest that Madagascar’s lemurs were impacted by the climate shift from “greenhouse” to “ice-house” conditions that occurred at that time. This could, in turn, help to explain some of the peculiar characteristics of the lemuriform clade.

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          Most cited references64

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          Mass extinctions in the marine fossil record.

          A new compilation of fossil data on invertebrate and vertebrate families indicates that four mass extinctions in the marine realm are statistically distinct from background extinction levels. These four occurred late in the Ordovician, Permian, Triassic, and Cretaceous periods. A fifth extinction event in the Devonian stands out from the background but is not statistically significant in these data. Background extinction rates appear to have declined since Cambrian time, which is consistent with the prediction that optimization of fitness should increase through evolutionary time.
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            Cenozoic deep-Sea temperatures and global ice volumes from Mg/Ca in benthic foraminiferal calcite

            A deep-sea temperature record for the past 50 million years has been produced from the magnesium/calcium ratio (Mg/Ca) in benthic foraminiferal calcite. The record is strikingly similar in form to the corresponding benthic oxygen isotope (delta(18)O) record and defines an overall cooling of about 12 degrees C in the deep oceans with four main cooling periods. Used in conjunction with the benthic delta(18)O record, the magnesium temperature record indicates that the first major accumulation of Antarctic ice occurred rapidly in the earliest Oligocene (34 million years ago) and was not accompanied by a decrease in deep-sea temperatures.
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              Rapid stepwise onset of Antarctic glaciation and deeper calcite compensation in the Pacific Ocean.

              The ocean depth at which the rate of calcium carbonate input from surface waters equals the rate of dissolution is termed the calcite compensation depth. At present, this depth is approximately 4,500 m, with some variation between and within ocean basins. The calcite compensation depth is linked to ocean acidity, which is in turn linked to atmospheric carbon dioxide concentrations and hence global climate. Geological records of changes in the calcite compensation depth show a prominent deepening of more than 1 km near the Eocene/Oligocene boundary (approximately 34 million years ago) when significant permanent ice sheets first appeared on Antarctica, but the relationship between these two events is poorly understood. Here we present ocean sediment records of calcium carbonate content as well as carbon and oxygen isotopic compositions from the tropical Pacific Ocean that cover the Eocene/Oligocene boundary. We find that the deepening of the calcite compensation depth was more rapid than previously documented and occurred in two jumps of about 40,000 years each, synchronous with the stepwise onset of Antarctic ice-sheet growth. The glaciation was initiated, after climatic preconditioning, by an interval when the Earth's orbit of the Sun favoured cool summers. The changes in oxygen-isotope composition across the Eocene/Oligocene boundary are too large to be explained by Antarctic ice-sheet growth alone and must therefore also indicate contemporaneous global cooling and/or Northern Hemisphere glaciation.
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                Author and article information

                Contributors
                lgodfrey@anthro.umass.edu
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                8 August 2020
                8 August 2020
                2020
                : 20
                : 97
                Affiliations
                [1 ]GRID grid.266683.f, ISNI 0000 0001 2184 9220, Department of Anthropology, , University of Massachusetts, ; 217 Machmer Hall, 240 Hicks Way, Amherst, MA 01003 USA
                [2 ]GRID grid.261128.e, ISNI 0000 0000 9003 8934, Department of Biological Sciences, , Northern Illinois University, ; DeKalb, IL 60115 USA
                [3 ]GRID grid.266683.f, ISNI 0000 0001 2184 9220, Department of Public Health, School of Biostatistics and Epidemiology, , University of Massachusetts, ; Amherst, MA 01003 USA
                [4 ]GRID grid.4367.6, ISNI 0000 0001 2355 7002, Present Address: Department of Biology, , Washington University, ; St. Louis, MO 63130 USA
                [5 ]GRID grid.266683.f, ISNI 0000 0001 2184 9220, Department of Mathematics and Statistics, , University of Massachusetts, ; Amherst, MA 01003 USA
                [6 ]GRID grid.413759.d, ISNI 0000 0001 0725 8379, Present Address: USDA, APHIS, ; Riverdale, MD 20737 USA
                Author information
                http://orcid.org/0000-0001-9997-0207
                Article
                1628
                10.1186/s12862-020-01628-1
                7414565
                32770933
                e41da0f5-84be-45a9-a4ae-929da37396d0
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 11 March 2019
                : 18 May 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: BCS 1750598
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Evolutionary Biology
                primate,diversification,eocene-oligocene transition,mid-cenozoic extinction,colonization,fossils,evolutionary modeling, transoceanic dispersal

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