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      Loss of species and genetic diversity during colonization: Insights from acanthocephalan parasites in northern European seals

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          Abstract

          Studies on host–parasite systems that have experienced distributional shifts, range fragmentation, and population declines in the past can provide information regarding how parasite community richness and genetic diversity will change as a result of anthropogenic environmental changes in the future. Here, we studied how sequential postglacial colonization, shifts in habitat, and reduced host population sizes have influenced species richness and genetic diversity of Corynosoma (Acanthocephala: Polymorphidae) parasites in northern European marine, brackish, and freshwater seal populations. We collected Corynosoma population samples from Arctic, Baltic, Ladoga, and Saimaa ringed seal subspecies and Baltic gray seals, and then applied COI barcoding and triple‐enzyme restriction‐site associated DNA (3RAD) sequencing to delimit species, clarify their distributions and community structures, and elucidate patterns of intraspecific gene flow and genetic diversity. Our results showed that Corynosoma species diversity reflected host colonization histories and population sizes, with four species being present in the Arctic, three in the Baltic Sea, two in Lake Ladoga, and only one in Lake Saimaa. We found statistically significant population‐genetic differentiation within all three Corynosoma species that occur in more than one seal (sub)species. Genetic diversity tended to be high in Corynosoma populations originating from Arctic ringed seals and low in the landlocked populations. Our results indicate that acanthocephalan communities in landlocked seal populations are impoverished with respect to both species and intraspecific genetic diversity. Interestingly, the loss of genetic diversity within Corynosoma species seems to have been less drastic than in their seal hosts, possibly due to their large local effective population sizes resulting from high infection intensities and effective intra‐host population mixing. Our study highlights the utility of genomic methods in investigations of community composition and genetic diversity of understudied parasites.

          Abstract

          Acanthocephalan parasite communities in northern European landlocked seal populations are impoverished with respect to both species and intraspecific genetic diversity. Interestingly, the loss of genetic diversity within Corynosoma species seems to have been less drastic than in their seal hosts, possibly due to their large local effective population sizes resulting from high infection intensities and effective intra‐host population mixing. Our study highlights the utility of the 3RAD method in investigations of community composition and genetic diversity of understudied parasites.

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          MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms.

          The Molecular Evolutionary Genetics Analysis (Mega) software implements many analytical methods and tools for phylogenomics and phylomedicine. Here, we report a transformation of Mega to enable cross-platform use on Microsoft Windows and Linux operating systems. Mega X does not require virtualization or emulation software and provides a uniform user experience across platforms. Mega X has additionally been upgraded to use multiple computing cores for many molecular evolutionary analyses. Mega X is available in two interfaces (graphical and command line) and can be downloaded from www.megasoftware.net free of charge.
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            IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era

            Abstract IQ-TREE (http://www.iqtree.org, last accessed February 6, 2020) is a user-friendly and widely used software package for phylogenetic inference using maximum likelihood. Since the release of version 1 in 2014, we have continuously expanded IQ-TREE to integrate a plethora of new models of sequence evolution and efficient computational approaches of phylogenetic inference to deal with genomic data. Here, we describe notable features of IQ-TREE version 2 and highlight the key advantages over other software.
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              A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.

              Some simple formulae were obtained which enable us to estimate evolutionary distances in terms of the number of nucleotide substitutions (and, also, the evolutionary rates when the divergence times are known). In comparing a pair of nucleotide sequences, we distinguish two types of differences; if homologous sites are occupied by different nucleotide bases but both are purines or both pyrimidines, the difference is called type I (or "transition" type), while, if one of the two is a purine and the other is a pyrimidine, the difference is called type II (or "transversion" type). Letting P and Q be respectively the fractions of nucleotide sites showing type I and type II differences between two sequences compared, then the evolutionary distance per site is K = -(1/2) ln [(1-2P-Q) square root of 1-2Q]. The evolutionary rate per year is then given by k = K/(2T), where T is the time since the divergence of the two sequences. If only the third codon positions are compared, the synonymous component of the evolutionary base substitutions per site is estimated by K'S = -(1/2) ln (1-2P-Q). Also, formulae for standard errors were obtained. Some examples were worked out using reported globin sequences to show that synonymous substitutions occur at much higher rates than amino acid-altering substitutions in evolution.
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                Author and article information

                Contributors
                ludmila.sromek@ug.edu.pl
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                19 October 2023
                October 2023
                : 13
                : 10 ( doiID: 10.1002/ece3.v13.10 )
                : e10608
                Affiliations
                [ 1 ] Department of Marine Ecosystems Functioning, Institute of Oceanography University of Gdansk Gdynia Poland
                [ 2 ] Department of Environmental and Biological Sciences University of Eastern Finland Joensuu Finland
                [ 3 ] Natural Resources Institute Finland Joensuu Finland
                [ 4 ] Department of Ecosystem in the Barents Region Norwegian Institute of Bioeconomy Research Svanvik Norway
                [ 5 ] Department of Biological and Environmental Sciences University of Jyväskylä Jyväskylä Finland
                [ 6 ] Red Sea Research Center King Abdullah University of Science and Technology Jeddah Saudi Arabia
                [ 7 ] Norwegian Polar Institute, Fram Centre Tromsø Norway
                [ 8 ] Institute of Biology, Karelian Research Centre Russian Academy of Sciences Petrozavodsk Russia
                [ 9 ] The Baltic Ringed Seal Foundation St. Petersburg Russia
                [ 10 ] Department of Biology and Bioinformatics, School of Bioscience University of Skövde Skövde Sweden
                Author notes
                [*] [* ] Correspondence

                Ludmila Sromek, Institute of Oceanography, University of Gdansk, Al. Marszalka Pilsudskiego 46, 81‐378 Gdynia, Poland.

                Email: ludmila.sromek@ 123456ug.edu.pl

                Author information
                https://orcid.org/0000-0002-3260-8032
                https://orcid.org/0000-0003-2849-3989
                https://orcid.org/0000-0003-3612-8842
                https://orcid.org/0000-0002-9372-4360
                https://orcid.org/0000-0003-4706-7256
                https://orcid.org/0000-0003-3868-2345
                https://orcid.org/0000-0002-3985-8405
                https://orcid.org/0000-0001-8289-7752
                https://orcid.org/0000-0003-2061-0570
                Article
                ECE310608 ECE-2023-06-01076.R1
                10.1002/ece3.10608
                10585441
                37869427
                994e77bf-8fa6-45e0-8bb3-de933322be9f
                © 2023 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 22 September 2023
                : 27 June 2023
                : 25 September 2023
                Page count
                Figures: 5, Tables: 1, Pages: 21, Words: 16314
                Funding
                Funded by: Academy of Finland , doi 10.13039/501100002341;
                Award ID: 294466
                Funded by: Betty Väänänen Foundation
                Funded by: Narodowe Centrum Nauki , doi 10.13039/501100004281;
                Award ID: 2019/32/C/NZ8/00335
                Funded by: Nestori Foundation
                Funded by: Norwegian Biodiversity Information Centre , doi 10.13039/501100015044;
                Award ID: Project 27‐19
                Funded by: Raija and Ossi Tuuliainen Foundation
                Funded by: Societas pro Fauna et Flora Fennica , doi 10.13039/501100018756;
                Categories
                Ecological Genetics
                Population Genetics
                Research Article
                Research Articles
                Custom metadata
                2.0
                October 2023
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.4 mode:remove_FC converted:19.10.2023

                Evolutionary Biology
                acanthocephala,genetic diversity,phylogeography,population bottlenecks,population genomics,seal parasites

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