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Polyandry and non-random fertilisation maintain long-term genetic diversity in an isolated island population of adders (Vipera berus)

Abstract

Conservation genetic theory suggests that small and isolated populations should be subject to reduced genetic diversity i.e., heterozygosity and allelic diversity. Our 34 years study of an isolated island population of adders (Vipera berus) in southern Sweden challenges this notion. Despite a lack of gene flow and a yearly mean estimated reproductive adult population size of only 65 adult adders (range 12–171), the population maintains high levels of heterozygosity and allelic diversity similar to that observed in two mainland populations. Even a 14-year major “bottleneck” i.e., a reduction in adult adder numbers, encompassing at least four adder generations, did not result in any reduction in the island adders’ heterozygosity and allelic diversity. Female adders are polyandrous, and fertilisation is non-random, which our empirical data and modelling suggest are underpinning the maintenance of the population’s high level of heterozygosity. Our empirical results and subsequent modelling suggest that the positive genetic effects of polyandry in combination with non-random fertilisation, often overlooked in conservation genetic analyses, deserve greater consideration when predicting long-term survival of small and isolated populations.

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Fig. 1: Fertilisation success at three different levels of fertilisation relationships (random, intermediate non-random fertilisation and high non-random fertilisation) as a function of male–female genetic similarity.
Fig. 2: Annual number of adult male adders captured, estimated annual adult male numbers, with associated 95% confidence intervals and estimated total number of reproductive adders (see methods for its calculation).
Fig. 3: PCA biplot of the first two principal component analyses of the Euclidean genetic distances among individuals from the three populations.
Fig. 4: Simulated temporal evolution of heterozygosity in nine populations of adders over a period of 100 years varying across three levels of initial heterozygosity (low, medium and high) and three levels of mating (random, non-random intermediate fertilisation and non-random high fertilisation, see Fig. 1).

Data availability

SNP data used in the analyses, unfiltered and filtered as per Methods, have been deposited on DRYAD (https://doi.org/10.5061/dryad.73n5tb31c).

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Acknowledgements

We are very grateful for comments on a previous version made by the associate editor and four reviewers which greatly improved our manuscript. The assistance provided by R.S. Waples that has been instrumental when preparing the manuscript and our analyses of Ne. We would also like to express our gratitude to B. Stille, H. Anderberg, L. Anderberg and C. Anderberg for their field work assistance. The study was financed by private funds.

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TM initiated and conceived the study. Field work was conducted by TM and BU. DB performed the population dynamics analyses. AG performed the molecular genetic analyses. BG performed the estimates of effective population size. MK performed the modelling analyses. TM wrote the manuscript with significant contributions from all co-authors.

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Correspondence to Thomas Madsen.

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Madsen, T., Ujvari, B., Bauwens, D. et al. Polyandry and non-random fertilisation maintain long-term genetic diversity in an isolated island population of adders (Vipera berus). Heredity 130, 64–72 (2023). https://doi.org/10.1038/s41437-022-00578-2

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