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      Mutual maintenance of di- and triploid Pelophylax esculentus hybrids in R-E systems: results from artificial crossings experiments

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          Abstract

          Background

          Interspecies animal hybrids can employ clonal or hemiclonal reproduction modes where one or all parental genomes are transmitted to the progeny without recombination. Nevertheless, some interspecies hybrids retain strong connection with the parental species needed for successful reproduction. Appearance of polyploid hybrid animals may play an important role in the substitution of parental species and in the speciation process.

          Results

          To establish the mechanisms that enable parental species, diploid and polyploid hybrids coexist we have performed artificial crossing experiments of water frogs of Pelophylax esculentus complex. We identified tadpole karyotypes and oocyte genome composition in all females involved in the crossings. The majority of diploid and triploid hybrid frogs produced oocytes with 13 bivalents leading to haploid gametes with the same genome as parental species hybrids usually coexist with. After fertilization of such gametes only diploid animals appeared. Oocytes with 26 bivalents produced by some diploid hybrid frogs lead to diploid gametes, which give rise to triploid hybrids after fertilization. In gonads of all diploid and triploid hybrid tadpoles we found DAPI-positive micronuclei (nucleus-like bodies) involved in selective genome elimination. Hybrid male and female individuals produced tadpoles with variable karyotype and ploidy even in one crossing owing to gametes with various genome composition.

          Conclusions

          We propose a model of diploid and triploid hybrid frog reproduction in R-E population systems. Triploid Pelophylax esculentus hybrids can transmit genome of parental species they coexist with by producing haploid gametes with the same genome composition. Triploid hybrids cannot produce triploid individuals after crossings with each other and depend on diploid hybrid females producing diploid eggs. In contrast to other population systems, the majority of diploid and triploid hybrid females unexpectedly produced gametes with the same genome as parental species hybrids coexist with.

          Electronic supplementary material

          The online version of this article (10.1186/s12862-017-1063-3) contains supplementary material, which is available to authorized users.

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          Most cited references56

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          The role of hybridization in evolution.

          N H Barton (2001)
          Hybridization may influence evolution in a variety of ways. If hybrids are less fit, the geographical range of ecologically divergent populations may be limited, and prezygotic reproductive isolation may be reinforced. If some hybrid genotypes are fitter than one or both parents, at least in some environments, then hybridization could make a positive contribution. Single alleles that are at an advantage in the alternative environment and genetic background will introgress readily, although such introgression may be hard to detect. 'Hybrid speciation', in which fit combinations of alleles are established, is more problematic; its likelihood depends on how divergent populations meet, and on the structure of epistasis. These issues are illustrated using Fisher's model of stabilizing selection on multiple traits, under which reproductive isolation evolves as a side-effect of adaptation in allopatry. This confirms a priori arguments that while recombinant hybrids are less fit on average, some gene combinations may be fitter than the parents, even in the parental environment. Fisher's model does predict heterosis in diploid F1s, asymmetric incompatibility in reciprocal backcrosses, and (when dominance is included) Haldane's Rule. However, heterosis arises only when traits are additive, whereas the latter two patterns require dominance. Moreover, because adaptation is via substitutions of small effect, Fisher's model does not generate the strong effects of single chromosome regions often observed in species crosses.
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            Hybrid speciation.

            Botanists have long believed that hybrid speciation is important, especially after chromosomal doubling (allopolyploidy). Until recently, hybridization was not thought to play a very constructive part in animal evolution. Now, new genetic evidence suggests that hybrid speciation, even without polyploidy, is more common in plants and also animals than we thought.
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              The role of hybridization in evolution: HYBRIDIZATION IN EVOLUTION

              N H Barton (2001)
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                Author and article information

                Contributors
                dmitrijdedukh@gmail.com
                slitvinchuk@yahoo.com
                rozanov@mail.cytspb.rssi.ru
                d.a.shabanov@gmail.com
                79213267671 , alla.krasikova@gmail.com
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                17 October 2017
                17 October 2017
                2017
                : 17
                : 220
                Affiliations
                [1 ]ISNI 0000 0001 2289 6897, GRID grid.15447.33, Saint-Petersburg State University, ; Saint-Petersburg, Russia
                [2 ]ISNI 0000 0000 9629 3848, GRID grid.418947.7, Institute of Cytology, Russian Academy of Sciences, ; Saint-Petersburg, Russia
                [3 ]ISNI 0000 0004 0517 6080, GRID grid.18999.30, V.N. Karazin Kharkiv National University, ; Kharkiv, Ukraine
                [4 ]ISNI 0000 0001 2289 6897, GRID grid.15447.33, Saint-Petersburg State University, ; 7-9, Universitetskaya nab, 199034 Saint-Petersburg, Russia
                Author information
                http://orcid.org/0000-0002-6571-5328
                Article
                1063
                10.1186/s12862-017-1063-3
                5645918
                29041900
                38c461df-c1a9-4b68-ad09-48294131c619
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 9 March 2017
                : 2 October 2017
                Funding
                Funded by: Russian Foundation of Basic Research
                Award ID: 15-34-21020
                Award Recipient :
                Funded by: Russian Foundation of Basic Research
                Award ID: 15-04-05068
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2017

                Evolutionary Biology
                hybrid population systems,polyploid hybrid,gamete,genome elimination,karyotype,hemiclonal reproduction

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