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      A mega-cryptic species complex hidden among one of the most common annelids in the North East Atlantic

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          Abstract

          We investigate mitochondrial ( COI, 16S rDNA) and nuclear ( ITS2, 28S rDNA) genetic structure of North East Atlantic lineages of Terebellides, a genus of sedentary annelids mainly inhabiting continental shelf and slope sediments. We demonstrate the presence of more than 25 species of which only seven are formally described. Species boundaries are determined with molecular data using a broad range of analytical methods. Many of the new species are common and wide spread, and the majority of the species are found in sympatry with several other species in the complex. Being one of the most regularly encountered annelid taxa in the North East Atlantic, it is more likely to find an undescribed species of Terebellides than a described one.

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          Cryptic species as a window on diversity and conservation.

          The taxonomic challenge posed by cryptic species (two or more distinct species classified as a single species) has been recognized for nearly 300 years, but the advent of relatively inexpensive and rapid DNA sequencing has given biologists a new tool for detecting and differentiating morphologically similar species. Here, we synthesize the literature on cryptic and sibling species and discuss trends in their discovery. However, a lack of systematic studies leaves many questions open, such as whether cryptic species are more common in particular habitats, latitudes or taxonomic groups. The discovery of cryptic species is likely to be non-random with regard to taxon and biome and, hence, could have profound implications for evolutionary theory, biogeography and conservation planning.
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            Sequence-based species delimitation for the DNA taxonomy of undescribed insects.

            Cataloging the very large number of undescribed species of insects could be greatly accelerated by automated DNA based approaches, but procedures for large-scale species discovery from sequence data are currently lacking. Here, we use mitochondrial DNA variation to delimit species in a poorly known beetle radiation in the genus Rivacindela from arid Australia. Among 468 individuals sampled from 65 sites and multiple morphologically distinguishable types, sequence variation in three mtDNA genes (cytochrome oxidase subunit 1, cytochrome b, 16S ribosomal RNA) was strongly partitioned between 46 or 47 putative species identified with quantitative methods of species recognition based on fixed unique ("diagnostic") characters. The boundaries between groups were also recognizable from a striking increase in branching rate in clock-constrained calibrated trees. Models of stochastic lineage growth (Yule models) were combined with coalescence theory to develop a new likelihood method that determines the point of transition from species-level (speciation and extinction) to population-level (coalescence) evolutionary processes. Fitting the location of the switches from speciation to coalescent nodes on the ultrametric tree of Rivacindela produced a transition in branching rate occurring at 0.43 Mya, leading to an estimate of 48 putative species (confidence interval for the threshold ranging from 47 to 51 clusters within 2 logL units). Entities delimited in this way exhibited biological properties of traditionally defined species, showing coherence of geographic ranges, broad congruence with morphologically recognized species, and levels of sequence divergence typical for closely related species of insects. The finding of discontinuous evolutionary groupings that are readily apparent in patterns of sequence variation permits largely automated species delineation from DNA surveys of local communities as a scaffold for taxonomy in this poorly known insect group.
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              Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent.

              The focus of this article is a Bayesian method for inferring both species delimitations and species trees under the multispecies coalescent model using molecular sequences from multiple loci. The species delimitation requires no a priori assignment of individuals to species, and no guide tree. The method is implemented in a package called STACEY for BEAST2, and is a extension of the author's DISSECT package. Here we demonstrate considerable efficiency improvements by using three new operators for sampling from the posterior using the Markov chain Monte Carlo algorithm, and by using a model for the population size parameters along the branches of the species tree which allows these parameters to be integrated out. The correctness of the moves is demonstrated by tests of the implementation. The practice of using a pipeline approach to species delimitation under the multispecies coalescent, has been shown to have major problems on simulated data (Olave et al. in Syst Biol 63:263-271. doi: 10.1093/sysbio/syt106 , 2014). The same simulated data set is used to demonstrate the accuracy and improved convergence of the present method. We also compare performance with *BEAST for a fixed delimitation analysis on a large data set, and again show improved convergence.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: VisualizationRole: Writing – review & editing
                Role: Formal analysisRole: SoftwareRole: Writing – review & editing
                Role: ResourcesRole: VisualizationRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: Resources
                Role: Resources
                Role: ResourcesRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                20 June 2018
                2018
                : 13
                : 6
                : e0198356
                Affiliations
                [1 ] Sjöfartmuseet Akvariet, Göteborg, Sweden
                [2 ] Institutionen för marina vetenskaper, Göteborgs Universitet, Göteborg, Sweden
                [3 ] Departamento de Bioloxía, Facultade de Ciencias, Universidade da Coruña, A Coruña, Spain
                [4 ] Department of Biodiversity and Conservation, Mediterranean Institute for Advanced Studies, IMEDEA, Balearic Islands, Spain
                [5 ] Senckenberg Forschungsinstitute und Naturmuseun, German Centre for Marine Biodiversity Research, Hamburg, Germany
                [6 ] Norwegian University of Science and Technology, NTNU University Museum, Trondheim, Norway
                [7 ] Department of Natural History, University Museum of Bergen, Bergen, Norway
                [8 ] Norwegian Institute for Water Research, Region South, Grimstad, Norway
                [9 ] Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow, Russia
                [10 ] Akvaplan-niva AS, Fram Centre, Tromsø, Norway
                [11 ] Institute of Marine Research, Tromsø, Norway
                [12 ] Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia
                [13 ] Centre National de la Recherche Scientifique & Université de Bordeaux, Environnements et Paléoenvironnements Océaniques et Continentaux, Station Marine d’Arcachon, Arcachon, France
                [14 ] University of the Balearic Island, Department of Biology, Ctra. Valldemossa, Balearic Islands, Spain
                National Cheng Kung University, TAIWAN
                Author notes

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

                Author information
                http://orcid.org/0000-0001-5761-8803
                Article
                PONE-D-17-40550
                10.1371/journal.pone.0198356
                6010226
                29924805
                5c5bb218-d94b-4cdd-82a8-6dfebf3cb5ce
                © 2018 Nygren 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
                : 16 November 2017
                : 17 May 2018
                Page count
                Figures: 12, Tables: 4, Pages: 37
                Funding
                Funded by: Norwegian Taxonomy Initiative
                Award ID: knr 49-13, pnr 70184228
                Award Recipient :
                Funded by: Norwegian Taxonomy Initiative
                Award ID: knr 53-09, pnr 70184216
                Award Recipient :
                Funded by: Norwegian Taxonomy Initiative
                Award ID: knr 55-12, pnr 70184227
                Award Recipient :
                Funded by: Norwegian Taxonomy Initiative
                Award ID: pnr 70184215
                Award Recipient :
                Funded by: Swedish Taxonomy Initiative
                Award ID: 140/07 1.4
                Award Recipient :
                Funded by: Swedish Taxonomy Initiative
                Award ID: 166/08 1.4
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100005416, Norges Forskningsråd;
                Award ID: 248799
                Award Recipient :
                Funded by: Kungliga Fysiografiska sällskapet Nilsson-Ehle donationerna
                Award Recipient :
                Funded by: Akvaplan Niva
                Award Recipient :
                Funded by: Akvaplan Niva
                Award Recipient :
                Funded by: Spanish Ministerio de Economía, Industria y Competitividad, Agencia Estatal de Investigación, Comunidad Autónoma de las Islas Baleares and the European Social Fund
                Award ID: RYC-2016-20799
                Award Recipient :
                Financial support was provided by the Norwegian Taxonomy Initiative [ http://www.biodiversity.no/Pages/135523] to AN (Cryptic polychaete species in Norwegian waters, knr 49-13, pnr 70184228), to EO, TB and JAK (Polychaetes in Skagerrak, knr 53-09, pnr 70184216), to TB, EO and JAK (Polychaetes in the Norwegian Sea, knr 55-12, pnr 70184227); and by the Swedish Taxonomy Initiative [ https://www.artdatabanken.se/en/the-swedish-taxonomy-initiative/] (Polychaete species complexes in Swedish waters, dnr 140/07 1.4 and 166/08 1.4), and Kungliga Fysiografiska sällskapet Nilsson-Ehle donationerna [ https://www.fysiografen.se/sv/] to AN; and by the ForBio Research School funded by the Research Council of Norway [ https://www.forskningsradet.no/en/Home_page/1177315753906] (project no. 248799) and the Norwegian Taxonomy Initiative (pnr 70184215) and the Ramon y Cajal program (RYC-2016-20799) funded by Spanish Ministerio de Economía, Industria y Competitividad, Agencia Estatal de Investigación, Comunidad Autónoma de las Islas Baleares and the European Social Fund to MC; and by Akvaplan Niva [ http://www.akvaplan.niva.no/en/] to AS and JP. Publication fees were covered by NTNU's [ https://www.ntnu.no/] Publishing Fund to MC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                People and Places
                Population Groupings
                Ethnicities
                European People
                Norwegian People
                Biology and Life Sciences
                Genetics
                Heredity
                Genetic Mapping
                Haplotypes
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
                Sequence Alignment
                Biology and Life Sciences
                Biogeography
                Ecology and Environmental Sciences
                Biogeography
                Earth Sciences
                Geography
                Biogeography
                Biology and Life Sciences
                Evolutionary Biology
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                Speciation
                Species Delimitation
                Biology and Life Sciences
                Evolutionary Biology
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                Cryptic Speciation
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