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Monophyletic origin of multiple clonal lineages in an asexual fish (Poecilia formosa)

Authors

  • MATTHIAS STÖCK,

    1. Department of Ecology and Evolution, University of Lausanne, Biophore, CH-1015 Lausanne, Switzerland
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    • Equal contribution.

  • KATHRIN P. LAMPERT,

    1. Evolutionary Ecology and Biodiversity of Animals, University of Bochum, Universitaetsstr. 150, Bld. ND05 Room 785, D-44780 Bochum, Germany
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    • Equal contribution.

  • DIRK MÖLLER,

    1. Department of Zoology, University of Hamburg, Martin-Luther-King Pl. 3, D-20146 Hamburg, Germany
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  • INGO SCHLUPP,

    1. Department of Zoology, University of Hamburg, Martin-Luther-King Pl. 3, D-20146 Hamburg, Germany
    2. Department of Zoology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019, USA
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  • MANFRED SCHARTL

    1. Theodor-Boveri-Institut, Physiologische Chemie I, University of Würzburg, Biozentrum, Am Hubland, D-97074 Würzburg, Germany
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Matthias Stöck, Fax: +41 21 692 4265;
E-mail: Matthias.stoeck@unil.ch

Abstract

Despite the advantage of avoiding the costs of sexual reproduction, asexual vertebrates are very rare and often considered evolutionarily disadvantaged when compared to sexual species. Asexual species, however, may have advantages when colonizing (new) habitats or competing with sexual counterparts. They are also evolutionary older than expected, leaving the question whether asexual vertebrates are not only rare because of their ‘inferior’ mode of reproduction but also because of other reasons. A paradigmatic model system is the unisexual Amazon molly, Poecilia formosa, that arose by hybridization of the Atlantic molly, Poecilia mexicana, as the maternal ancestor, and the sailfin molly, Poecilia latipinna, as the paternal ancestor. Our extensive crossing experiments failed to resynthesize asexually reproducing (gynogenetic) hybrids confirming results of previous studies. However, by producing diploid eggs, female F1-hybrids showed apparent preadaptation to gynogenesis. In a range-wide analysis of mitochondrial sequences, we examined the origin of P. formosa. Our analyses point to very few or even a single origin(s) of its lineage, which is estimated to be approximately 120 000 years old. A monophyletic origin was supported from nuclear microsatellite data. Furthermore, a considerable degree of genetic variation, apparent by high levels of clonal microsatellite diversity, was found. Our molecular phylogenetic evidence and the failure to resynthesize the gynogenetic P. formosa together with the old age of the species indicate that some unisexual vertebrates might be rare not because they suffer the long-term consequences of clonal reproduction but because they are only very rarely formed as a result of complex genetic preconditions necessary to produce viable and fertile clonal genomes and phenotypes (‘rare formation hypothesis’).

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