The role of hybridisation in the origin and evolutionary persistence of vertebrate parthenogens: a case study of Darevskia lizards

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  • A Correction to this article was published on 23 September 2019

Abstract

Obligate parthenogenesis is found in only 0.1% of the vertebrate species, is thought to be relatively short lived and is typically of hybrid origin. However, neither the evolutionary persistence of asexuality in vertebrates, nor the conditions that allow the generation of new parthenogenetic lineages are currently well understood. It has been proposed that vertebrate parthenogenetic lineages arise from hybridisation between two divergent taxa within a specific range of phylogenetic distances (the ‘Balance Hypothesis’). Moreover, parthenogenetic species often maintain a certain level of hybridisation with their closest sexual relatives, potentially generating new polyploid hybrid lineages. Here we address the role of hybridisation in the origin and evolutionary lifespan of vertebrate parthenogens. We use a set of microsatellite markers to characterise the origins of parthenogens in the lizard genus Darevskia, to study the distinctiveness of sexual and asexual taxa currently in sympatry, and to analyse the evolutionary consequences of interspecific hybridisation between asexual females and sexual males. We find that parthenogens result from multiple past hybridisation events between species from specific lineages over a range of phylogenetic distances. This suggests that the Balance Hypothesis needs to allow for lineage-specific effects, as envisaged in the Phylogenetic Constraint Hypothesis. Our results show recurrent backcrossing between sexual and parthenogenic Darevskia but neither gene flow nor formation of new asexual lineages. We suggest that, along with their demographic advantage, parthenogens gain additional leverage to outcompete sexuals in nature when the retention of sexual reproductive machinery allows backcrossing with their sexual ancestors.

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  • 23 September 2019

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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Acknowledgements

This work was supported by the project “Preserving Armenian biodiversity: Joint Portuguese – Armenian program for training in modern conservation biology” of Gulbenkian Foundation (Portugal) and the FCT grant SFRH/BD/81483/2011. The authors thank Anna Vardanyan, Claudia Corti and Elena Argaña for field assistance, Andy Krupa, Gavin Horsburgh and Susana Lopes for their assistance with the genotyping, and Steeves Buckland and Óscar Mira for their suggestions in the methods. We also thank Karel Janko and an anonymous reviewer for comments on previous versions of the manuscript. MA was supported by SCS MES RA - RFFR 18 RF-132 project. Capture permits were provided by the Ministry of Nature Protection of Republic Armenia Code 5/22.1/51043 and lizard handling followed the ethical guidelines of Yerevan State University.

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Freitas, S.N., Harris, D.J., Sillero, N. et al. The role of hybridisation in the origin and evolutionary persistence of vertebrate parthenogens: a case study of Darevskia lizards. Heredity 123, 795–808 (2019) doi:10.1038/s41437-019-0256-5

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