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Successful worldwide invasion of the veined rapa whelk, Rapana venosa, despite a dramatic genetic bottleneck

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Abstract

Biological invasions represent an important component of global change, with potentially huge detrimental effects on native biological biodiversity and ecosystems. Knowledge about invasion history provides information about the invasion process and the origin and genetic composition of invading populations. To clarify the source and invasive routes of a successful world-wide invader, the veined rapa whelk, Rapana venosa, genetic variability of samples from five representative native populations from coasts of Japan and China and 13 worldwide invasive populations was analyzed using 11 nuclear microsatellite loci. A dramatic decrease of genetic variation was detected in the invasive populations compared with the native populations. The results demonstrated that R. venosa was capable of establishing itself in many areas despite a dramatic genetic bottleneck, suggesting that a remarkable reduction of genetic diversity is not a limiting factor for short-term success of this invasive species. Considering the lack of mitochondrial variation previously observed in the invasive populations, the dramatic genetic bottleneck and the allele distribution detected using microsatellites suggested that the original introduced Black Sea population could have been founded by very few individuals, perhaps only a single female and a single male. The initial invasive Black Sea population was likely an accidental introduction from Japan, and then invaded the Adriatic Sea by range expansion, which served as a source for subsequent invasive populations in Europe and America by various transport vectors. In addition, microsatellite alleles in the invasive populations showed a tendency to mutate with the addition or deletion of a single repeat, which is consistent with the stepwise mutation model. Our findings provide a good example of how an aquatic invader with a drastic genetic bottleneck and very low genetic diversity rapidly expands its geographical range.

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Acknowledgements

The study was supported by AoShan Talents Program supported by Qingdao National Laboratory for Marine Science and Technology (No. 2015ASTP-ES05), a grant from the National Natural Science Foundation of China (No. 31200280), the NSFC-Shandong Joint Fund for Marine Ecology and Environmental Sciences (No. U1606404). We thank Nadya R. Mamoozadeh for his help in preparing samples.

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  1. Dong-Xiu Xue and John Graves have contributed equally to this work.

Authors and Affiliations

  1. CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao, 266071, Shandong, China

    Dong-Xiu Xue, Tao Zhang & Jin-Xian Liu

  2. Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Dong-Xiu Xue, Tao Zhang & Jin-Xian Liu

  3. Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA, 23062, USA

    John Graves

  4. Centro Universitario Regional del Este-CURE, Sede Maldonado Universidad de la República Uruguay, Montevideo, Uruguay

    Alvar Carranza

  5. Área Biodiversidady Conservación Museo Nacional de Historia Natural, Montevideo, Uruguay

    Alvar Carranza

  6. DCEE, Institute of Neurology, University College London, London, WC1N 3BG, UK

    Sergiy Sylantyev

  7. CCBS, University of Edinburgh, 49 Little France Crescent, Edinburgh, EH16 4SB, UK

    Sergiy Sylantyev

  8. Biological Department, Odesa National Mechnikov University, Odessa, 65082, Ukraine

    Sergey Snigirov

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  1. Dong-Xiu Xue
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Contributions

G.J. and L.J.X. designed research, X.D.X. performed research, C.A., S.S., S.S. and T.Z. provided some samples, X.D.X. and L.J.X. analyzed data, X.D.X., G.J. and L.J.X wrote the paper and all authors contributed substantially to revisions.

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Correspondence to Jin-Xian Liu.

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Xue, DX., Graves, J., Carranza, A. et al. Successful worldwide invasion of the veined rapa whelk, Rapana venosa, despite a dramatic genetic bottleneck. Biol Invasions 20, 3297–3314 (2018). https://doi.org/10.1007/s10530-018-1774-4

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