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      Consequences of polyploidy and divergence as revealed by cytogenetic mapping of tandem repeats in African clawed frogs ( Xenopus, Pipidae)

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          Abstract

          Repetitive elements have been identified in several amphibian genomes using whole genome sequencing, but few studies have used cytogenetic mapping to visualize these elements in this vertebrate group. Here, we used fluorescence in situ hybridization and genomic data to map the U1 and U2 small nuclear RNAs and histone H3 in six species of African clawed frog (genus Xenopus), including, from subgenus Silurana, the diploid Xenopus tropicalis and its close allotetraploid relative X. calcaratus and, from subgenus Xenopus, the allotetraploid species X. pygmaeus, X. allofraseri, X. laevis, and X. muelleri. Results allowed us to qualitatively evaluate the relative roles of polyploidization and divergence in the evolution of repetitive elements because our focal species include allotetraploid species derived from two independent polyploidization events — one that is relatively young that gave rise to X. calcaratus and another that is older that gave rise to the other (older) allotetraploids. Our results demonstrated conserved loci number and position of signals in the species from subgenus Silurana; allotetraploid X. calcaratus has twice as many signals as diploid X. tropicalis. However, the content of repeats varied among the other allotetraploid species. We detected almost same number of signals in X. muelleri as in X. calcaratus and same number of signals in X. pygmaeus, X. allofraseri, X. laevis as in the diploid X. tropicalis. Overall, these results are consistent with the proposal that allopolyploidization duplicated these tandem repeats and that variation in their copy number was accumulated over time through reduction and expansion in a subset of the older allopolyploids.

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          Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution

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            Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle.

            Genetic sex determination by W and Z chromosomes has developed independently in different groups of organisms. To better understand the evolution of sex chromosomes and the plasticity of sex-determination mechanisms, we sequenced the whole genomes of a male (ZZ) and a female (ZW) half-smooth tongue sole (Cynoglossus semilaevis). In addition to insights into adaptation to a benthic lifestyle, we find that the sex chromosomes of these fish are derived from the same ancestral vertebrate protochromosome as the avian W and Z chromosomes. Notably, the same gene on the Z chromosome, dmrt1, which is the male-determining gene in birds, showed convergent evolution of features that are compatible with a similar function in tongue sole. Comparison of the relatively young tongue sole sex chromosomes with those of mammals and birds identified events that occurred during the early phase of sex-chromosome evolution. Pertinent to the current debate about heterogametic sex-chromosome decay, we find that massive gene loss occurred in the wake of sex-chromosome 'birth'.
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              Preservation of duplicate genes by complementary, degenerative mutations.

              The origin of organismal complexity is generally thought to be tightly coupled to the evolution of new gene functions arising subsequent to gene duplication. Under the classical model for the evolution of duplicate genes, one member of the duplicated pair usually degenerates within a few million years by accumulating deleterious mutations, while the other duplicate retains the original function. This model further predicts that on rare occasions, one duplicate may acquire a new adaptive function, resulting in the preservation of both members of the pair, one with the new function and the other retaining the old. However, empirical data suggest that a much greater proportion of gene duplicates is preserved than predicted by the classical model. Here we present a new conceptual framework for understanding the evolution of duplicate genes that may help explain this conundrum. Focusing on the regulatory complexity of eukaryotic genes, we show how complementary degenerative mutations in different regulatory elements of duplicated genes can facilitate the preservation of both duplicates, thereby increasing long-term opportunities for the evolution of new gene functions. The duplication-degeneration-complementation (DDC) model predicts that (1) degenerative mutations in regulatory elements can increase rather than reduce the probability of duplicate gene preservation and (2) the usual mechanism of duplicate gene preservation is the partitioning of ancestral functions rather than the evolution of new functions. We present several examples (including analysis of a new engrailed gene in zebrafish) that appear to be consistent with the DDC model, and we suggest several analytical and experimental approaches for determining whether the complementary loss of gene subfunctions or the acquisition of novel functions are likely to be the primary mechanisms for the preservation of gene duplicates. For a newly duplicated paralog, survival depends on the outcome of the race between entropic decay and chance acquisition of an advantageous regulatory mutation. Sidow 1996(p. 717) On one hand, it may fix an advantageous allele giving it a slightly different, and selectable, function from its original copy. This initial fixation provides substantial protection against future fixation of null mutations, allowing additional mutations to accumulate that refine functional differentiation. Alternatively, a duplicate locus can instead first fix a null allele, becoming a pseudogene. Walsh 1995 (p. 426) Duplicated genes persist only if mutations create new and essential protein functions, an event that is predicted to occur rarely. Nadeau and Sankoff 1997 (p. 1259) Thus overall, with complex metazoans, the major mechanism for retention of ancient gene duplicates would appear to have been the acquisition of novel expression sites for developmental genes, with its accompanying opportunity for new gene roles underlying the progressive extension of development itself. Cooke et al. 1997 (p. 362)
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                Author and article information

                Contributors
                martin.knytl@natur.cuni.cz
                Journal
                Eur J Wildl Res
                Eur J Wildl Res
                European Journal of Wildlife Research
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1612-4642
                1439-0574
                21 July 2023
                21 July 2023
                2023
                : 69
                : 4
                : 81
                Affiliations
                [1 ]GRID grid.4491.8, ISNI 0000 0004 1937 116X, Department of Cell Biology, Faculty of Science, , Charles University, ; Viničná 7, Prague, 12843 Czech Republic
                [2 ]GRID grid.448077.8, ISNI 0000 0000 9663 9052, Institute of Vertebrate Biology of the Czech Academy of Sciences, ; Brno, Czech Republic
                [3 ]GRID grid.425401.6, ISNI 0000 0001 2243 1723, Department of Zoology, , National Museum of the Czech Republic, ; Prague, Czech Republic
                [4 ]GRID grid.426567.4, ISNI 0000 0001 2285 286X, Department of Genetics and Reproduction, , CEITEC - Veterinary Research Institute, ; Hudcova 296/70, Brno, 62100 Czech Republic
                [5 ]GRID grid.29273.3d, ISNI 0000 0001 2288 3199, Department of Animal Biology and Conservation, , University of Buea, ; PO Box 63, Buea, 00237 Cameroon
                [6 ]GRID grid.440806.e, ISNI 0000 0004 6013 2603, Department of Aquatic Ecology, Biodiversity Monitoring Center, , University of Kisangani, ; Kisangani, Democratic Republic of the Congo
                [7 ]GRID grid.25073.33, ISNI 0000 0004 1936 8227, Department of Biology, , McMaster University, ; 1280 Main Street West, Hamilton, ON L8S4K1 Canada
                Author information
                http://orcid.org/0000-0002-4398-4076
                http://orcid.org/0000-0001-8678-7155
                http://orcid.org/0000-0003-4531-3580
                http://orcid.org/0000-0002-9512-8845
                http://orcid.org/0000-0002-6325-6957
                Article
                1709
                10.1007/s10344-023-01709-8
                10361878
                37483536
                1b5e16b8-ac4a-468f-817f-5c7d12f50840
                © The Author(s) 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 1 February 2023
                : 13 May 2023
                : 27 June 2023
                Funding
                Funded by: IVB CAS
                Award ID: RVO: 68081766
                Award Recipient :
                Funded by: Ministry of Culture of the Czech Republic
                Award ID: DKRVO 2019–2023/6.VII.e, National Museum, 00023272
                Award Recipient :
                Funded by: Ministry of Agriculture of the Czech Republic
                Award ID: MZE-RO0518
                Award ID: MZE-RO0518
                Award Recipient :
                Funded by: Natural Sciences and Engineering Research Council of Canada
                Award ID: RGPIN-2017-05770
                Award Recipient :
                Funded by: P JAC project, MSCA Fellowships CZ – UK
                Award ID: CZ.02.01.01/00/22_010/0002902
                Award Recipient :
                Funded by: Charles University
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                © Springer-Verlag GmbH Germany, part of Springer Nature 2023

                amphibians,anura,snrna,histone h3,allopolyploidization,in situ hybridization

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