Automictic Reproduction in Interspecific Hybrids of Poeciliid Fish

Department of Physiological Chemistry I, University of Würzburg, Biocenter, Am Hubland, 97074 Würzburg, Germany.
Current Biology (Impact Factor: 9.57). 12/2007; 17(22):1948-53. DOI: 10.1016/j.cub.2007.09.064
Source: PubMed


Automixis, the process whereby the fusion of meiotic products restores the diploid state of the egg, is a common mode of reproduction in plants but has also been described in invertebrate animals. In vertebrates, however, automixis has so far only been discussed as one of several explanations for isolated cases of facultative parthenogenesis. Analyzing oocyte formation in F1 hybrids derived from Poecilia mexicana limantouri and P. latipinna crosses (the cross that led to the formation of the gynogenetic Poecilia formosa), we found molecular evidence for automictic oocyte production. The mechanism involves the random fusion of meiotic products after the second meiotic division. The fertilization of diploid oocytes gives rise to fully viable triploid offspring. Although the automictic production of diploid oocytes as seen in these F1 hybrids clearly represents a preadaptation to parthenogenetic reproduction, it is also a powerful intrinsic postzygotic isolation mechanism because the resulting next generation triploids were always sterile. The mechanism described here can explain facultative parthenogenesis, as well as varying ploidy levels reported in different animal groups. Most importantly, at least some of the reported cases of triploidy in humans can now be traced back to automixis.

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Available from: Dunja K Lamatsch, Jun 28, 2014
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    • "Equivalently, the term " terminal fusion " is used to 165 describe the fusion of any products that have been separated during meiosis II (or where 166 meiosis II is suppressed, Asher 1970), not only in ordered tetrads. 167 " Random fusion " can be defined as fusion of two randomly chosen products of a 168 meiotic tetrad (Suomalainen et al. 1987; Pearcy et al. 2006; Lampert et al. 2007). Hence, with 169 random fusion, 2/3 of the offspring are produced by central fusion and 1/3 by terminal fusion 170 (once one meiotic product is chosen, only one of the three remaining products carries the 171 same allele at the centromeric locus shown above, thus central fusion occurs with a 172 probability of 2/3). "
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    ABSTRACT: The breeding systems of many organisms are cryptic and difficult to investigate with observational data, yet they have profound effects on a species' ecology, evolution, and genome organization. Genomic approaches offer a novel, indirect way to investigate breeding systems, specifically by studying the transmission of genetic information from parents to offspring. Here we exemplify this method through an assessment of self-fertilization vs. automictic parthenogenesis in Daphnia magna. Self-fertilization reduces heterozygosity by 50% compared to the parents, but under automixis, whereby two haploid products from a single meiosis fuse, the expected heterozygosity reduction depends on whether the two meiotic products are separated during meiosis I or II (i.e., central vs. terminal fusion). Reviewing the existing literature and incorporating recombination interference, we derive an inter-chromosomal and an intra-chromosomal prediction of how to distinguish various forms of automixis from self-fertilization using offspring heterozygosity data. We then test these predictions using RAD-sequencing data on presumed automictic diapause offspring of so-called non-male producing strains and compare them with a "self-fertilized" offspring produced by within-clone mating. The results unequivocally show that these offspring were produced by automixis, mostly, but not exclusively, though terminal fusion. However, the results also show that this conclusion was only possible owing to genome-wide heterozygosity data, with phenotypic data as well as data from microsatellite markers yielding inconclusive or even misleading results. Our study thus demonstrates how to use the power of genomic approaches for elucidating breeding systems, and it provides the first demonstration of automictic parthenogenesis in Daphnia. Copyright © 2015, The Genetics Society of America.
    Genetics 09/2015; DOI:10.1534/genetics.115.179879 · 5.96 Impact Factor
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    • "It evolved presumably at least 120,000 years ago through a single hybridisation event [11] between a female Atlantic molly, P. mexicana[12], and a male sailfin molly, P. latipinna[13]. So far all experiments to artificially create Amazon molly like unisexuals through hybridisation of the parental species did not succeed [10,14,15], but always yield sexual F1 hybrids. "
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    ABSTRACT: The Amazon molly, Poecilia formosa (Teleostei: Poeciliinae) is an unisexual, all-female species. It evolved through the hybridisation of two closely related sexual species and exhibits clonal reproduction by sperm dependent parthenogenesis (or gynogenesis) where the sperm of a parental species is only used to activate embryogenesis of the apomictic, diploid eggs but does not contribute genetic material to the offspring.Here we provide and describe the first de novo assembled transcriptome of the Amazon molly in comparison with its maternal ancestor, the Atlantic molly Poecilia mexicana. The transcriptome data were produced through sequencing of single end libraries (100 bp) with the Illumina sequencing technique. 83,504,382 reads for the Amazon molly and 81,625,840 for the Atlantic molly were assembled into 127,283 and 78,961 contigs for the Amazon molly and the Atlantic molly, respectively. 63% resp. 57% of the contigs could be annotated with gene ontology terms after sequence similarity comparisons. Furthermore, we were able to identify genes normally involved in reproduction and especially in meiosis also in the transcriptome dataset of the apomictic reproducing Amazon molly. We assembled and annotated the transcriptome of a non-model organism, the Amazon molly, without a reference genome (de novo). The obtained dataset is a fundamental resource for future research in functional and expression analysis. Also, the presence of 30 meiosis-specific genes within a species where no meiosis is known to take place is remarkable and raises new questions for future research.
    BMC Research Notes 04/2014; 7(1):249. DOI:10.1186/1756-0500-7-249
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    • "This phenomenon has been well documented in the triploid offspring of poeciliid interspecific hybrids [42]. The resulting triploid products are not genetically identical to the parental genome, as segregation and recombination result in nonidentical homologous chromosomes [42], explaining the atypical genotype E observed herein. However, further studies are needed to evaluate whether this triploid event is due to automixis or whether hybridization facilitates polyploidization, as shown in other species [46]. "
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    ABSTRACT: Juvenile fish trade monitoring is an important task on Brazilian fish farms. However, the identification of juvenile fish through morphological analysis is not feasible, particularly between interspecific hybrids and pure species individuals, making the monitoring of these individuals difficult. Hybrids can be erroneously identified as pure species in breeding facilities, which might reduce production on farms and negatively affect native populations due to escapes or stocking practices. In the present study, we used a multi-approach analysis (molecular and cytogenetic markers) to identify juveniles of three serrasalmid species (Colossoma macropomum, Piaractus mesopotamicus and Piaractus brachypomus) and their hybrids in different stocks purchased from three seed producers in Brazil. The main findings of this study were the detection of intergenus backcrossing between the hybrid ♀ patinga (P. mesopotamicus×P. brachypomus)×♂ C. macropomum and the occurrence of one hybrid triploid individual. This atypical specimen might result from automixis, a mechanism that produces unreduced gametes in some organisms. Moreover, molecular identification indicated that hybrid individuals are traded as pure species or other types of interspecific hybrids, particularly post-F1 individuals. These results show that serrasalmid fish genomes exhibit high genetic heterogeneity, and multi-approach methods and regulators could improve the surveillance of the production and trade of fish species and their hybrids, thereby facilitating the sustainable development of fish farming.
    PLoS ONE 03/2014; 9(3):e89902. DOI:10.1371/journal.pone.0089902 · 3.23 Impact Factor
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