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      Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum'

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          Abstract

          We review knowledge about the roles of sex chromosomes in vertebrate hybridization and speciation, exploring a gradient of divergences with increasing reproductive isolation (speciation continuum). Under early divergence, well-differentiated sex chromosomes in meiotic hybrids may cause Haldane-effects and introgress less easily than autosomes. Undifferentiated sex chromosomes are more susceptible to introgression and form multiple (or new) sex chromosome systems with hardly predictable dominance hierarchies. Under increased divergence, most vertebrates reach complete intrinsic reproductive isolation. Slightly earlier, some hybrids (linked in ‘the extended speciation continuum') exhibit aberrant gametogenesis, leading towards female clonality. This facilitates the evolution of various allodiploid and allopolyploid clonal (‘asexual’) hybrid vertebrates, where ‘asexuality' might be a form of intrinsic reproductive isolation. A comprehensive list of ‘asexual' hybrid vertebrates shows that they all evolved from parents with divergences that were greater than at the intraspecific level (K2P-distances of greater than 5–22% based on mtDNA). These ‘asexual' taxa inherited genetic sex determination by mostly undifferentiated sex chromosomes. Among the few known sex-determining systems in hybrid ‘asexuals', female heterogamety (ZW) occurred about twice as often as male heterogamety (XY). We hypothesize that pre-/meiotic aberrations in all-female ZW-hybrids present Haldane-effects promoting their evolution. Understanding the preconditions to produce various clonal or meiotic allopolyploids appears crucial for insights into the evolution of sex, ‘asexuality' and polyploidy.

          This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

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          Hybridization and speciation.

          Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization. © 2013 The Authors. Journal of Evolutionary Biology © 2013 European Society For Evolutionary Biology.
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            Species concepts and species delimitation.

            The issue of species delimitation has long been confused with that of species conceptualization, leading to a half century of controversy concerning both the definition of the species category and methods for inferring the boundaries and numbers of species. Alternative species concepts agree in treating existence as a separately evolving metapopulation lineage as the primary defining property of the species category, but they disagree in adopting different properties acquired by lineages during the course of divergence (e.g., intrinsic reproductive isolation, diagnosability, monophyly) as secondary defining properties (secondary species criteria). A unified species concept can be achieved by treating existence as a separately evolving metapopulation lineage as the only necessary property of species and the former secondary species criteria as different lines of evidence (operational criteria) relevant to assessing lineage separation. This unified concept of species has several consequences for species delimitation, including the following: First, the issues of species conceptualization and species delimitation are clearly separated; the former secondary species criteria are no longer considered relevant to species conceptualization but only to species delimitation. Second, all of the properties formerly treated as secondary species criteria are relevant to species delimitation to the extent that they provide evidence of lineage separation. Third, the presence of any one of the properties (if appropriately interpreted) is evidence for the existence of a species, though more properties and thus more lines of evidence are associated with a higher degree of corroboration. Fourth, and perhaps most significantly, a unified species concept shifts emphasis away from the traditional species criteria, encouraging biologists to develop new methods of species delimitation that are not tied to those properties.
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              The genic view of the process of speciation

              Chung-I Wu (2001)
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                Author and article information

                Contributors
                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos Trans R Soc Lond B Biol Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                September 13, 2021
                July 26, 2021
                July 26, 2021
                : 376
                : 1833 , Theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’ compiled and edited by Lukáš Kratochvíl and Matthias Stöck
                : 20200103
                Affiliations
                [ 1 ]Leibniz-Institute of Freshwater Ecology and Inland Fisheries - IGB (Forschungsverbund Berlin), , Müggelseedamm 301, 12587 Berlin, Germany
                [ 2 ]Amphibian Research Center, Hiroshima University, , Higashi-Hiroshima 739-8526, Japan
                [ 3 ]Institute of Animal Physiology and Genetics, Laboratory of Fish Genetics, The Czech Academy of Sciences, , 277 21 Libechov, Czech Republic
                [ 4 ]Department of Zoology, Faculty of Science, Charles University, , Viničná 7, Prague 2, 128 00, Czech Republic
                [ 5 ]Research Department for Limnology, University of Innsbruck, , Mondseestrasse 9, A-5310 Mondsee, Austria
                [ 6 ]Department of Biology and Ecology, Faculty of Science, University of Ostrava, , 701 03 Ostrava, Czech Republic
                Author notes
                Author information
                http://orcid.org/0000-0003-4888-8371
                http://orcid.org/0000-0002-1152-813X
                http://orcid.org/0000-0001-5852-5174
                http://orcid.org/0000-0002-6023-4381
                http://orcid.org/0000-0002-5251-1617
                http://orcid.org/0000-0002-7866-4937
                Article
                rstb20200103
                10.1098/rstb.2020.0103
                8310718
                34304588
                cfe1fa69-2926-40e5-8039-8b76bfb5bf54
                © 2021 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : April 12, 2021
                Funding
                Funded by: Grantová Agentura, Univerzita Karlova, http://dx.doi.org/10.13039/100007543;
                Award ID: PRIMUS/19/SCI/008 to RR
                Funded by: Ministry of Education, Youth and Sports of the Czech Republic;
                Award ID: 539 EXCELLENCE CZ.02.1.01/0.0/0.0/15_003/0000460 O
                Funded by: COFASP/ERANET (STURGEoNOMICS);
                Award ID: 2816ERA04G to MS
                Funded by: Grantová Agentura České Republiky, http://dx.doi.org/10.13039/501100001824;
                Award ID: 19-21552S to KJ
                Award ID: 20-23794S to RR and ZS
                Award ID: 21-25185S to KJ
                Award ID: PPLZ L200452002 to DD
                Categories
                1001
                70
                197
                Articles
                Review Articles
                Custom metadata
                September 13, 2021

                Philosophy of science
                sex chromosomes,hybridization,evolution,clonal reproduction,speciation
                Philosophy of science
                sex chromosomes, hybridization, evolution, clonal reproduction, speciation

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