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      Historical Mammal Extinction on Christmas Island (Indian Ocean) Correlates with Introduced Infectious Disease

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          Abstract

          It is now widely accepted that novel infectious disease can be a leading cause of serious population decline and even outright extinction in some invertebrate and vertebrate groups (e.g., amphibians). In the case of mammals, however, there are still no well-corroborated instances of such diseases having caused or significantly contributed to the complete collapse of species. A case in point is the extinction of the endemic Christmas Island rat ( Rattus macleari): although it has been argued that its disappearance ca. AD 1900 may have been partly or wholly caused by a pathogenic trypanosome carried by fleas hosted on recently-introduced black rats ( Rattus rattus), no decisive evidence for this scenario has ever been adduced. Using ancient DNA methods on samples from museum specimens of these rodents collected during the extinction window (AD 1888–1908), we were able to resolve unambiguously sequence evidence of murid trypanosomes in both endemic and invasive rats. Importantly, endemic rats collected prior to the introduction of black rats were devoid of trypanosome signal. Hybridization between endemic and black rats was also previously hypothesized, but we found no evidence of this in examined specimens, and conclude that hybridization cannot account for the disappearance of the endemic species. This is the first molecular evidence for a pathogen emerging in a naïve mammal species immediately prior to its final collapse.

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          Most cited references35

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          Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers.

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            The general stochastic model of nucleotide substitution.

            DNA sequence evolution through nucleotide substitution may be assimilated to a stationary Markov process. The fundamental equations of the general model, with 12 independent substitution parameters, are used to obtain a formula which corrects the effect of multiple and parallel substitutions on the measure of evolutionary divergence between two homologous sequences. We show that only reversible models, with six independent parameters, allow the calculation of the substitution rates. Simulation experiments on DNA sequence evolution through nucleotide substitution call into question the effectiveness of the general model (and of any other more detailed description); nevertheless, the general model results are slightly superior to any of its particular cases.
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              Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers.

              With a standard set of primers directed toward conserved regions, we have used the polymerase chain reaction to amplify homologous segments of mtDNA from more than 100 animal species, including mammals, birds, amphibians, fishes, and some invertebrates. Amplification and direct sequencing were possible using unpurified mtDNA from nanogram samples of fresh specimens and microgram amounts of tissues preserved for months in alcohol or decades in the dry state. The bird and fish sequences evolve with the same strong bias toward transitions that holds for mammals. However, because the light strand of birds is deficient in thymine, thymine to cytosine transitions are less common than in other taxa. Amino acid replacement in a segment of the cytochrome b gene is faster in mammals and birds than in fishes and the pattern of replacements fits the structural hypothesis for cytochrome b. The unexpectedly wide taxonomic utility of these primers offers opportunities for phylogenetic and population research.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2008
                5 November 2008
                : 3
                : 11
                : e3602
                Affiliations
                [1 ]Biological Sciences Department, Old Dominion University, Norfolk, Virginia, United States of America
                [2 ]Department of Biology, University of Copenhagen, Copenhagen, Denmark
                [3 ]Sackler Institute for Comparative Genomics and Division of Invertebrate Zoology, American Museum of Natural History, New York, New York, United States of America
                [4 ]Consortium for Conservation Medicine, Wildlife Trust, New York, New York, United States of America
                [5 ]Vertebrate Zoology, American Museum of Natural History, New York, New York, United States of America
                Centre for DNA Fingerprinting and Diagnostics, India
                Author notes

                Conceived and designed the experiments: PD RM AG. Performed the experiments: KBW PFC MTPG. Analyzed the data: KBW SOK AG. Contributed reagents/materials/analysis tools: MTPG WH RD PD. Wrote the paper: RM AG. Performed the phylogenetic analysis and aided in writing the manuscript: SOK.

                Article
                08-PONE-RA-05845R1
                10.1371/journal.pone.0003602
                2572834
                18985148
                8f3e6674-59e2-4cab-8fa1-4ac4c0d3142e
                Wyatt 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
                : 6 August 2008
                : 8 October 2008
                Page count
                Pages: 9
                Categories
                Research Article
                Ecology/Conservation and Restoration Ecology
                Ecology/Environmental Microbiology
                Ecology/Evolutionary Ecology
                Evolutionary Biology/Evolutionary Ecology
                Evolutionary Biology/Microbial Evolution and Genomics
                Microbiology/Environmental Microbiology
                Microbiology/Microbial Evolution and Genomics
                Microbiology/Parasitology
                Infectious Diseases/Protozoal Infections

                Uncategorized
                Uncategorized

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