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      Study of male–mediated gene flow across a hybrid zone in the common shrew ( Sorex araneus ) using Y chromosome

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          Abstract

          Abstract

          Despite many studies, the impact of chromosome rearrangements on gene flow between chromosome races of the common shrew ( Sorex araneus Linnaeus, 1758) remains unclear. Interracial hybrids form meiotic chromosome complexes that are associated with reduced fertility. Nevertheless comprehensive investigations of autosomal and mitochondrial markers revealed weak or no barrier to gene flow between chromosomally divergent populations.

          In a narrow zone of contact between the Novosibirsk and Tomsk races hybrids are produced with extraordinarily complex configurations at meiosis I. Microsatellite markers have not revealed any barrier to gene flow, but the phenotypic differentiation between races is greater than may be expected if gene flow was unrestricted. To explore this contradiction we analyzed the distribution of the Y chromosome SNP markers within this hybrid zone. The Y chromosome variants in combination with race specific autosome complements allow backcrosses to be distinguished and their proportion among individuals within the hybrid zone to be evaluated. The balanced ratio of the Y variants observed among the pure race individuals as well as backcrosses reveals no male mediated barrier to gene flow. The impact of reproductive unfitness of backcrosses on gene flow is discussed as a possible mechanism of the preservation of race-specific morphology within the hybrid zone.

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          Most cited references37

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          The genetics of hybrid incompatibilities.

          Incompatibilities in interspecific hybrids, such as sterility and lethality, are widely observed causes of reproductive isolation and thus contribute to speciation. Because hybrid incompatibilities are caused by divergence in each of the hybridizing species, they also reveal genomic changes occurring on short evolutionary time scales that have functional consequences. These changes include divergence in protein-coding gene sequence, structure, and location, as well as divergence in noncoding DNAs. The most important unresolved issue is understanding the evolutionary causes of the divergence within species that in turn leads to incompatibility between species. Surprisingly, much of this divergence does not appear to be driven by ecological adaptation but may instead result from responses to purely mutational mechanisms or to internal genetic conflicts.
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            Dominance, epistasis and the genetics of postzygotic isolation.

            The sterility and inviability of species hybrids can be explained by between-locus "Dobzhansky-Muller" incompatibilities: alleles that are fit on their "normal" genetic backgrounds sometimes lower fitness when brought together in hybrids. We present a model of two-locus incompatibilities that distinguishes among three types of hybrid interactions: those between heterozygous loci (H(0)), those between a heterozygous and a homozygous (or hemizygous) locus (H(1)), and those between homozygous loci (H(2)). We predict the relative fitnesses of hybrid genotypes by calculating the expected numbers of each type of incompatibility. We use this model to study Haldane's rule and the large effect of X chromosomes on postzygotic isolation. We show that the severity of H(0) vs. H(1) incompatibilities is key to understanding Haldane's rule, while the severity of H(1) vs. H(2) incompatibilities must also be considered to explain large X effects. Large X effects are not inevitable in backcross analyses but rather-like Haldane's rule-may often reflect the recessivity of alleles causing postzygotic isolation. We also consider incompatibilities involving the Y (or W) chromosome and maternal effects. Such incompatibilities are common in Drosophila species crosses, and their consequences in male- vs. female-heterogametic taxa may explain the pattern of exceptions to Haldane's rule.
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              Microsatellites can be misleading: an empirical and simulation study.

              It has been long recognized that highly polymorphic genetic markers can lead to underestimation of divergence between populations when migration is low. Microsatellite loci, which are characterized by extremely high mutation rates, are particularly likely to be affected. Here, we report genetic differentiation estimates in a contact zone between two chromosome races of the common shrew (Sorex araneus), based on 10 autosomal microsatellites, a newly developed Y-chromosome microsatellite, and mitochondrial DNA. These results are compared to previous data on proteins and karyotypes. Estimates of genetic differentiation based on F- and R-statistics are much lower for autosomal microsatellites than for all other genetic markers. We show by simulations that this discrepancy stems mainly from the high mutation rate of microsatellite markers for F-statistics and from deviations from a single-step mutation model for R-statistics. The sex-linked genetic markers show that all gene exchange between races is mediated by females. The absence of male-mediated gene flow most likely results from male hybrid sterility.
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                Author and article information

                Journal
                Comp Cytogenet
                Comp Cytogenet
                CompCytogen
                Comparative Cytogenetics
                Pensoft Publishers
                1993-0771
                1993-078X
                2017
                19 June 2017
                : 11
                : 2
                : 421-430
                Affiliations
                [1 ] Institute of Cytology and Genetics, the Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia
                [2 ] Institute of Systematics and Ecology of Animals, the Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia
                Author notes
                Corresponding author: Andrei Polyakov ( polyakov@ 123456bionet.nsc.ru )

                Academic editor: Jan Zima

                Article
                10.3897/CompCytogen.v11i2.13494
                5596988
                8407f323-f00e-4618-94cf-c86d5edf6d39
                Andrei V. Polyakov, Viktor V. Panov

                This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 1 May 2017
                : 22 May 2017
                Categories
                Research Article

                sorex araneus,phenotypic evolution,hybrid zone,gene flow,y chromosome

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