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      Multigene Molecular Systematics Confirm Species Status of Morphologically Convergent Pagurus Hermit Crabs

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          Abstract

          Introduction

          In spite of contemporary morphological taxonomy appraisals, apparent high morphological similarity raises uncertainty about the species status of certain Pagurus hermit crabs. This is exemplified between two European species, Pagurus excavatus (Herbst, 1791) and Pagurus alatus (Fabricius 1775), whose species status is still difficult to resolve using morphological criteria alone.

          Methodology/Principal Findings

          To address such ambiguities, we used combinations of Maximum Likelihood (ML) and Bayesian Inference (BI) methods to delineate species boundaries of P. alatus and P. excavatus and formulate an intermediate Pagurus phylogenetic hypothesis, based upon single and concatenated mitochondrial (cytochrome oxidase I [COI]) and nuclear (16S and 28s ribosomal RNA) gene partitions. The molecular data supported the species status of P. excavatus and P. alatus and also clearly resolved two divergent clades within hermit crabs from the Northeast Atlantic Ocean and the Mediterranean Sea.

          Conclusions/Significance

          Despite the abundance and prominent ecological role of hermit crabs, Pagurus, in North East Atlantic Ocean and Mediterranean Sea ecosystems, many important aspects of their taxonomy, biology, systematics and evolution remain poorly explored. The topologies presented here should be regarded as hypotheses that can be incorporated into the robust and integrated understanding of the systematic relationships within and between species of the genus Pagurus inhabiting the Northeast Atlantic Ocean and the Mediterranean Sea.

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          Most cited references117

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          MRBAYES: Bayesian inference of phylogenetic trees.

          The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
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            Codon-substitution models for heterogeneous selection pressure at amino acid sites.

            Comparison of relative fixation rates of synonymous (silent) and nonsynonymous (amino acid-altering) mutations provides a means for understanding the mechanisms of molecular sequence evolution. The nonsynonymous/synonymous rate ratio (omega = d(N)d(S)) is an important indicator of selective pressure at the protein level, with omega = 1 meaning neutral mutations, omega 1 diversifying positive selection. Amino acid sites in a protein are expected to be under different selective pressures and have different underlying omega ratios. We develop models that account for heterogeneous omega ratios among amino acid sites and apply them to phylogenetic analyses of protein-coding DNA sequences. These models are useful for testing for adaptive molecular evolution and identifying amino acid sites under diversifying selection. Ten data sets of genes from nuclear, mitochondrial, and viral genomes are analyzed to estimate the distributions of omega among sites. In all data sets analyzed, the selective pressure indicated by the omega ratio is found to be highly heterogeneous among sites. Previously unsuspected Darwinian selection is detected in several genes in which the average omega ratio across sites is 1. Genes undergoing positive selection include the beta-globin gene from vertebrates, mitochondrial protein-coding genes from hominoids, the hemagglutinin (HA) gene from human influenza virus A, and HIV-1 env, vif, and pol genes. Tests for the presence of positively selected sites and their subsequent identification appear quite robust to the specific distributional form assumed for omega and can be achieved using any of several models we implement. However, we encountered difficulties in estimating the precise distribution of omega among sites from real data sets.
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              Phenotypic plasticity in the interactions and evolution of species.

              When individuals of two species interact, they can adjust their phenotypes in response to their respective partner, be they antagonists or mutualists. The reciprocal phenotypic change between individuals of interacting species can reflect an evolutionary response to spatial and temporal variation in species interactions and ecologically result in the structuring of food chains. The evolution of adaptive phenotypic plasticity has led to the success of organisms in novel habitats, and potentially contributes to genetic differentiation and speciation. Taken together, phenotypic responses in species interactions represent modifications that can lead to reciprocal change in ecological time, altered community patterns, and expanded evolutionary potential of species.
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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
                2011
                9 December 2011
                : 6
                : 12
                : e28233
                Affiliations
                [1 ]Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Environment Centre for Wales, Bangor University, Bangor, Wales, United Kingdom
                [2 ]Departamento de Biologia, Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Aveiro, Portugal
                [3 ]Instituto Nacional de Recursos Biológicos, L-IPIMAR, Lisboa, Portugal
                [4 ]Departamento de Biologia, Centro de Biologia Molecular e Ambiental (CBMA), Universidade do Minho, Braga, Portugal
                Biodiversity Insitute of Ontario - University of Guelph, Canada
                Author notes

                Conceived and designed the experiments: JMdS AdS. Performed the experiments: JMdS. Analyzed the data: JMdS AdS. Contributed reagents/materials/analysis tools: JMdS AdS MRC FOC SC GRC. Wrote the paper: JMdS SC GRC.

                Article
                PONE-D-11-12542
                10.1371/journal.pone.0028233
                3235110
                22174780
                e03f808c-ea78-46e2-bc91-b0527cfa9e08
                Matzen da Silva 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
                : 3 July 2011
                : 4 November 2011
                Page count
                Pages: 10
                Categories
                Research Article
                Biology
                Ecology
                Biodiversity
                Evolutionary Biology
                Evolutionary Systematics
                Molecular Systematics
                Phylogenetics
                Marine Biology
                Marine Ecology
                Zoology
                Animal Phylogenetics

                Uncategorized
                Uncategorized

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