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      Glacial History of a Modern Invader: Phylogeography and Species Distribution Modelling of the Asian Tiger Mosquito Aedes albopictus

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          Abstract

          Background

          The tiger mosquito, Aedes albopictus, is one of the 100 most invasive species in the world and a vector of human diseases. In the last 30 years, it has spread from its native range in East Asia to Africa, Europe, and the Americas. Although this modern invasion has been the focus of many studies, the history of the species’ native populations remains poorly understood. Here, we aimed to assess the role of Pleistocene climatic changes in shaping the current distribution of the species in its native range.

          Methodology/Principal Findings

          We investigated the phylogeography, historical demography, and species distribution of Ae. albopictus native populations at the Last Glacial Maximum (LGM). Individuals from 16 localities from East Asia were analyzed for sequence variation at two mitochondrial genes. No phylogeographic structure was observed across the study area. Demographic analyses showed a signature of population expansion that started roughly 70,000 years BP. The occurrence of a continuous and climatically suitable area comprising Southeast China, Indochinese Peninsula, and Sundaland during LGM was indicated by species distribution modelling.

          Conclusions/Significance

          Our results suggest an evolutionary scenario in which, during the last glacial phase, Ae. albopictus did not experience a fragmentation phase but rather persisted in interconnected populations and experienced demographic growth. The wide ecological flexibility of the species probably played a crucial role in its response to glacial-induced environmental changes. Currently, there is little information on the impact of Pleistocene climatic changes on animal species in East Asia. Most of the studies focused on forest-associated species and suggested cycles of glacial fragmentation and post-glacial expansion. The case of Ae. albopictus, which exhibits a pattern not previously observed in the study area, adds an important piece to our understanding of the Pleistocene history of East Asian biota.

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          Most cited references30

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          Arlequin (version 3.0): An integrated software package for population genetics data analysis

          Arlequin ver 3.0 is a software package integrating several basic and advanced methods for population genetics data analysis, like the computation of standard genetic diversity indices, the estimation of allele and haplotype frequencies, tests of departure from linkage equilibrium, departure from selective neutrality and demographic equilibrium, estimation or parameters from past population expansions, and thorough analyses of population subdivision under the AMOVA framework. Arlequin 3 introduces a completely new graphical interface written in C++, a more robust semantic analysis of input files, and two new methods: a Bayesian estimation of gametic phase from multi-locus genotypes, and an estimation of the parameters of an instantaneous spatial expansion from DNA sequence polymorphism. Arlequin can handle several data types like DNA sequences, microsatellite data, or standard multi-locus genotypes. A Windows version of the software is freely available on http://cmpg.unibe.ch/software/arlequin3.
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            A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation.

            We previously developed a cladistic approach to identify subsets of haplotypes defined by restriction endonuclease mapping or DNA sequencing that are associated with significant phenotypic deviations. Our approach was limited to segments of DNA in which little recombination occurs. In such cases, a cladogram can be constructed from the restriction site or sequence data that represents the evolutionary steps that interrelate the observed haplotypes. The cladogram is used to define a nested statistical design to identify mutational steps associated with significant phenotypic deviations. The central assumption behind this strategy is that any undetected mutation causing a phenotypic effect is embedded within the same evolutionary history that is represented by the cladogram. The power of this approach depends upon the confidence one has in the particular cladogram used to draw inferences. In this paper, we present a strategy for estimating the set of cladograms that are consistent with a particular sample of either restriction site or nucleotide sequence data and that includes the possibility of recombination. We first evaluate the limits of parsimony in constructing cladograms. Once these limits have been determined, we construct the set of parsimonious and nonparsimonious cladograms that is consistent with these limits. Our estimation procedure also identifies haplotypes that are candidates for being products of recombination. If recombination is extensive, our algorithm subdivides the DNA region into two or more subsections, each having little or no internal recombination. We apply this estimation procedure to three data sets to illustrate varying degrees of cladogram ambiguity and recombination.
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              A simulated annealing approach to define the genetic structure of populations.

              We present a new approach for defining groups of populations that are geographically homogeneous and maximally differentiated from each other. As a by-product, it also leads to the identification of genetic barriers between these groups. The method is based on a simulated annealing procedure that aims to maximize the proportion of total genetic variance due to differences between groups of populations (spatial analysis of molecular variance; samova). Monte Carlo simulations were used to study the performance of our approach and, for comparison, the behaviour of the Monmonier algorithm, a procedure commonly used to identify zones of sharp genetic changes in a geographical area. Simulations showed that the samova algorithm indeed finds maximally differentiated groups, which do not always correspond to the simulated group structure in the presence of isolation by distance, especially when data from a single locus are available. In this case, the Monmonier algorithm seems slightly better at finding predefined genetic barriers, but can often lead to the definition of groups of populations not differentiated genetically. The samova algorithm was then applied to a set of European roe deer populations examined for their mitochondrial DNA (mtDNA) HVRI diversity. The inferred genetic structure seemed to confirm the hypothesis that some Italian populations were recently reintroduced from a Balkanic stock, as well as the differentiation of groups of populations possibly due to the postglacial recolonization of Europe or the action of a specific barrier to gene flow.
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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, USA )
                1932-6203
                2012
                6 September 2012
                : 7
                : 9
                : e44515
                Affiliations
                [1 ]Department of Ecological and Biological Sciences, Tuscia University, Viterbo, Italy
                [2 ]Department of Environmental Biology, University “La Sapienza” of Rome, Rome, Italy
                [3 ]Agriculture and Environment Centre “G. Nicoli”, Crevalcore, Italy
                [4 ]Department of Parasitology, Chiang Mai University, Chiang Mai, Thailand
                Centro de Pesquisas René Rachou, Brazil
                Author notes

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

                Conceived and designed the experiments: DP SU. Performed the experiments: PS VM SU RB DP. Analyzed the data: DP VM. Contributed reagents/materials/analysis tools: PS VM SU RB DP. Wrote the paper: DP VM.

                Article
                PONE-D-12-10498
                10.1371/journal.pone.0044515
                3435282
                22970238
                60faee65-1ef6-492e-bbcb-252e43577fa2
                Copyright @ 2012

                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
                : 13 April 2012
                : 3 August 2012
                Page count
                Pages: 9
                Funding
                This work was funded by the Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR). The funders have no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Biodiversity
                Evolutionary Biology
                Population Genetics
                Genetic Polymorphism
                Haplotypes
                Evolutionary Ecology
                Microbiology
                Vector Biology
                Zoology
                Entomology

                Uncategorized
                Uncategorized

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