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      Mitogenome phylogenetics in the genus Palaemon (Crustacea: Decapoda) sheds light on species crypticism in the rockpool shrimp P. elegans

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          Abstract

          The genus Palaemon comprises worldwide marine and freshwater shrimps and prawns, and some of them are ecologically or commercially important species. Palaemon is not currently a monophyletic group, so phylogenetics and systematics are constantly changing. Species crypticism has been pointed out in several Palaemon species, being the clearest evidence in the European rockpool shrimp P. elegans. Here we sequenced and described seven European Palaemon mitochondrial genomes. The mitochondrial protein-coding genes were used, along with those of three other Palaemon species, to perform mitogenome phylogenetic analyses to clarify the evolutionary relationships within the genus, and particularly to shed light on the cryptic species found within P. elegans. The Messinian Salinity Crisis (5.3-5.9 Ma, late Miocene) was proposed to be the origin of this cryptic species and it was used as aged constraint for calibration analysis. We provide the largest and the first time-calibrated mitogenome phylogeny of the genus Palaemon and mitogenome substitution rate was estimated (1.59% per million years) in Decapoda for the first time. Our results highlighted the need for future systematics changes in Palaemon and crypticism in P. elegans was confirmed. Mitochondrial genome and cox1 (1.41%) substitution rate estimates matched those published elsewhere, arguing that the Messinian Salinity Crisis was a plausible event driving the split between P. elegans and its cryptic species. Molecular dating suggested that Pleistocene glaciations were likely involved in the differentiation between the Atlantic and Mediterranean populations of P. elegans. On the contrary, the divergence between the Atlantic and Mediterranean populations of the common littoral shrimp P. serratus was greater and dated to be much older (4.5-12.3 Ma, Plio-Miocene), so we considered that they could represent two separated species. Therefore, species crypticism in the genus Palaemon seems to be a common phenomenon.

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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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            Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty.

            Recent developments in marginal likelihood estimation for model selection in the field of Bayesian phylogenetics and molecular evolution have emphasized the poor performance of the harmonic mean estimator (HME). Although these studies have shown the merits of new approaches applied to standard normally distributed examples and small real-world data sets, not much is currently known concerning the performance and computational issues of these methods when fitting complex evolutionary and population genetic models to empirical real-world data sets. Further, these approaches have not yet seen widespread application in the field due to the lack of implementations of these computationally demanding techniques in commonly used phylogenetic packages. We here investigate the performance of some of these new marginal likelihood estimators, specifically, path sampling (PS) and stepping-stone (SS) sampling for comparing models of demographic change and relaxed molecular clocks, using synthetic data and real-world examples for which unexpected inferences were made using the HME. Given the drastically increased computational demands of PS and SS sampling, we also investigate a posterior simulation-based analogue of Akaike's information criterion (AIC) through Markov chain Monte Carlo (MCMC), a model comparison approach that shares with the HME the appealing feature of having a low computational overhead over the original MCMC analysis. We confirm that the HME systematically overestimates the marginal likelihood and fails to yield reliable model classification and show that the AICM performs better and may be a useful initial evaluation of model choice but that it is also, to a lesser degree, unreliable. We show that PS and SS sampling substantially outperform these estimators and adjust the conclusions made concerning previous analyses for the three real-world data sets that we reanalyzed. The methods used in this article are now available in BEAST, a powerful user-friendly software package to perform Bayesian evolutionary analyses.
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              FastQC: a quality-control tool for high-throughput sequence data.

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Resources
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                18 August 2020
                2020
                : 15
                : 8
                : e0237037
                Affiliations
                [1 ] Departamento de Biología and Centro de Investigaciones Científicas Avanzadas (CICA), Universidade da Coruña, A Coruña, Spain
                [2 ] Instituto Mediterráneo de Estudios Avanzados (IMEDEA), Consejo Superior de Investigaciones Científicas (CSIC) and Universitat de les Illes Balears, Esporles, Spain
                [3 ] Instituto de Ciencias Marinas de Andalucía (ICMAN), Consejo Superior de Investigaciones Científicas (CSIC), Puerto Real, Spain
                Shanghai Ocean University, CHINA
                Author notes

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

                Author information
                http://orcid.org/0000-0003-3334-4523
                Article
                PONE-D-20-14795
                10.1371/journal.pone.0237037
                7444591
                32810189
                73bc4472-733f-4b35-8bca-a8c295491141
                © 2020 González-Castellano 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
                : 18 May 2020
                : 17 July 2020
                Page count
                Figures: 3, Tables: 4, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003176, Ministerio de Educación, Cultura y Deporte;
                Award ID: FPU15/05265
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003329, Ministerio de Economía y Competitividad;
                Award ID: CTM2014-53838-R
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100010801, Xunta de Galicia;
                Award ID: ED431C 2018/S7
                Award Recipient :
                This work was funded by a CTM2014-53838-R grant from the Spanish Government (Ministerio de Economía y Competitividad) and by a ED431C 2018/S7 grant from Xunta de Galicia (Programa de Investigación Competitiva do Sistema Universitario Galego, Modalidade de grupos de referencia competitiva: Grupo de Investigación en Biología Evolutiva). I. González-Castellano was supported by a FPU scholarship from Ministerio de Educación, Cultura y Deporte (Spain).
                Categories
                Research Article
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Cryptic Speciation
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
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                Custom metadata
                The datasets generated and/or analyzed during the current study are available in the NCBI repository (accession numbers MT340086-MT340092 and MT340174-MT340196).

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