Gamete production patterns and mating systems in water frogs of the hybridogeneticPelophylax esculentuscomplex in north-eastern Ukraine

Hybridization and polyploidy play an important role in animal speciation. European water frogs of the Pelophylax esculentus complex demonstrate unusual genetic phenomena associated with hybridization, clonality and polyploidy which presumably indicate an initial stage of reticulate speciation. The Seversky Donets River drainage in north-eastern Ukraine is inhabited by both sexes of the diploid and triploid hybrid P. esculentus and only one parental species Pelophylax ridibundus. Based on the presence of various types of hybrids, all populations studied can be divided into three geographical groups: I) P. ridibundus–P. esculentus without triploids; II) P. ridibundus–P. esculentus without diploid hybrids; and III) P. ridibundus–P. esculentus with a mixture of diploids and triploids. A study of gametogenesis revealed that diploid P. esculentus in populations of the first type usually produced haploid gametes of P. ridibundus and a mixture of haploid gametes that carried one or another parental genome (hybrid amphispermy). In populations of the second type, hybrids are derived from crosses of P. ridibundus males with triploid hybrid females producing haploid eggs with a genome of P. lessonae. Therefore, we suggest that clonal genome duplication in these eggs might be the result of suppression of second polar body formation or extra precleavage endoreduplication. In populations of the third type, some diploid females can produce diploid gametes. Fertilization of these eggs with haploid sperm can result in triploid hybrids. Other hybrids here produce haploid gametes with one or another parental genome or their mixture giving rise to new diploid hybrids.

[1]  P. Kotlík,et al.  Two water frog populations from western Slovakia consisting of diploid females and diploid and triploid males of the hybridogenetic hybrid Rana esculenta (Anura, Ranidae) , 2001 .

[2]  S. Otto,et al.  Polyploid incidence and evolution. , 2000, Annual review of genetics.

[3]  H. Reyer,et al.  From Clonal to Sexual Hybrids: Genetic Recombination Via Triploids in All-Hybrid Populations of Water Frogs , 2009, Evolution; international journal of organic evolution.

[4]  M. Rybacki,et al.  Types of water frog populations (Rana esculenta complex) in Poland , 2001 .

[5]  L. Berger,et al.  A LEAKY HYBRIDOGENETIC SYSTEM (AMPHIBIA SALIENTIA) , 2016 .

[6]  C. Casola,et al.  Gametogenesis of intergroup hybrids of hemiclonal frogs. , 2007, Genetical research.

[7]  R. Günther,et al.  Inheritance Patterns in TriploidRana “esculenta” (Amphibia, Salientia) , 1979 .

[8]  M. M. Coelho,et al.  Speciation towards tetraploidization after intermediate processes of non-sexual reproduction , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[9]  J. Mallet Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[10]  J. Mallet Hybrid speciation , 2007, Nature.

[11]  H. Tunner,et al.  Premeiotic genome exclusion during oogenesis in the common edible frog,Rana esculenta , 1981, Naturwissenschaften.

[12]  A. Vinogradov,et al.  Genome elimination in diploid and triploid Rana esculenta males: cytological evidence from DNA flow cytometry. , 1990, Genome.

[13]  H. Tunner,et al.  Genome exclusion and two strategies of chromosome duplication in oogenesis of a hybrid frog , 2005, Naturwissenschaften.

[14]  R. Schultz Hybridization, Unisexuality, and Polyploidy in the Teleost Poeciliopsis (Poeciliidae) and Other Vertebrates , 1969, The American Naturalist.

[15]  M. Rybacki Diploid males of Rana esculenta from natural populations in Poland producing diploid spermatozoa , 1994 .

[16]  Von H. G. Tunner Kreuzungsexperimente mit Wasserfroschen aus österreichischen und polnischen M ischpopulationen (Rana lessonae + Rana esculenta): Eine Analyse biochemischer und morphologischer Merkmale , 2009 .

[17]  J. Gui,et al.  Meiosis completion and various sperm responses lead to unisexual and sexual reproduction modes in one clone of polyploid Carassius gibelio , 2015, Scientific Reports.

[18]  Litvinchuk,et al.  Cryptic speciation in Pelobates fuscus (Anura, Pelobatidae): evidence from DNA flow cytometry , 2001 .

[19]  S. Litvinchuk,et al.  The First Record of Mass Triploidy in Hybridogenic Green Frog Rana esculenta in Russia (Rostov Oblast , 2005 .

[20]  L. Berger,et al.  Inheritance patterns of water frog males from the environments of Nature Reserve Steckby, Germany , 1992 .

[21]  K. Fog,et al.  REPRODUCTION AND HYBRID LOAD IN ALL‐HYBRID POPULATIONS OF RANA ESCULENTA WATER FROGS IN DENMARK , 2005, Evolution; international journal of organic evolution.

[22]  J. Graf,et al.  Experimental gynogenesis provides evidence of hybridogenetic reproduction in theRana esculenta complex , 1979, Experientia.

[23]  P. Moler,et al.  THE AMPHIBIAN TREE OF LIFE , 2006 .

[24]  M. W. Olsen Frequency and cytological aspects of diploid parthenogenesis in turkey eggs , 2004, Theoretical and Applied Genetics.

[25]  Y. Kondo Developmental Capacity and Chromosome Number in the Offspring of Artificially Produced Autotetraploids of Rana nigromaculata , 2002, Zoological science.

[26]  C. Jakob,et al.  Coexistence of diploid and triploid hybrid water frogs: population differences persist in the apparent absence of differential survival , 2010, BMC Ecology.

[27]  P. Mikulíček,et al.  Mode of hybridogenesis and habitat preferences influence population composition of water frogs (Pelophylax esculentus complex, Anura: Ranidae) in a region of sympatric occurrence (western Slovakia) , 2015 .

[28]  L. Berger,et al.  Genome exclusion in gametogenesis by an interspecific Rana hybrid: Evidence from electrophoresis of individual oocytes , 1980 .

[29]  Ditte G Christiansen,et al.  Gamete types, sex determination and stable equilibria of all-hybrid populations of diploid and triploid edible frogs (Pelophylax esculentus) , 2009, BMC Evolutionary Biology.

[30]  R. Ydenberg,et al.  Winter body mass and over-ocean flocking as components of danger management by Pacific dunlins , 2010, BMC Ecology.

[31]  M. Arnold Evolution through Genetic Exchange , 2006 .

[32]  H. Kawahara PRODUCTION OF TRIPLOID AND GYNOGENETIC DIPLOID XENOPUS BY COLD TREATMENT , 1978, Development, growth & differentiation.

[33]  H. Tunner,et al.  Chromosomal Constitution And C-Banding in HomotypicRana esculenta Crosses , 1979 .

[34]  Gaston-Denis Guex,et al.  DELETERIOUS ALLELES AND DIFFERENTIAL VIABILITY IN PROGENY OF NATURAL HEMICLONAL FROGS , 2002, Evolution; international journal of organic evolution.

[35]  L. Berger,et al.  Progeny of water frog populations in central Poland , 1992 .

[36]  H. Reyer,et al.  Genetic diversity and distribution patterns of diploid and polyploid hybrid water frog populations (Pelophylax esculentus complex) across Europe , 2015, Molecular ecology.

[37]  C Vorburger FIXATION OF DELETERIOUS MUTATIONS IN CLONAL LINEAGES: EVIDENCE FROM HYBRIDOGENETIC FROGS , 2001, Evolution; international journal of organic evolution.

[38]  H. Tunner Die klonale Struktur einer Wasserfroschpopulation1 , 2009 .

[39]  M. Ogielska Nucleus-like bodies in gonial cells of Rana esculenta [Amphibia, Anura] tadpoles - a putative way of chromosome elimination , 1994 .

[40]  S. Litvinchuk,et al.  Optional Endoreplication and Selective Elimination of Parental Genomes during Oogenesis in Diploid and Triploid Hybrid European Water Frogs , 2015, PloS one.

[41]  A. Vinogradov,et al.  Two germ cell lineages with genomes of different species in one and the same animal. , 2008, Hereditas.

[42]  H. Reyer,et al.  Gamete production patterns, ploidy, and population genetics reveal evolutionary significant units in hybrid water frogs (Pelophylax esculentus) , 2013, Ecology and evolution.

[43]  J. Bogart,et al.  Evolution and Ecology of Unisexual Vertebrates , 1989 .

[44]  K. Bi,et al.  Genetic and Genomic Interactions of Animals with Different Ploidy Levels , 2013, Cytogenetic and Genome Research.

[45]  S. Litvinchuk,et al.  MASS OCCURRENCE OF POLYPLOID GREEN FROGS (Rana esculenta COMPLEX) IN EASTERN UKRAINE , 2004 .

[46]  J. Greilhuber,et al.  Premeiotic chromosome doubling after genome elimination during spermatogenesis of the species hybrid Rana esculenta , 1982, Theoretical and Applied Genetics.

[47]  S. Bucci,et al.  Lampbrush and mitotic chromosomes of the hemiclonally reproducing hybrid Rana esculenta and its parental species. , 1990, The Journal of experimental zoology.

[48]  C. Jakob,et al.  Genetic diversity in water frog hybrids (Pelophylax esculentus) varies with population structure and geographic location , 2010, Molecular ecology.

[49]  P. Chaplin,et al.  A Multicenter, Open-Label, Controlled Phase II Study to Evaluate Safety and Immunogenicity of MVA Smallpox Vaccine (IMVAMUNE) in 18–40 Year Old Subjects with Diagnosed Atopic Dermatitis , 2015, PloS one.