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Ancient, but not recent, population declines have had a genetic impact on alpine yellow-bellied toad populations, suggesting potential for complete recovery

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Abstract

Reduction in population size and local extinctions have been reported for the yellow-bellied toad, Bombina variegata, but the genetic impact of this is not yet known. In this study, we genotyped 200 individuals, using mtDNA cytochrome b and 11 nuclear microsatellites. We investigated fine-scale population structure and tested for genetic signatures of historical and recent population decline, using several statistical approaches, including likelihood methods and approximate Bayesian computation. Five major genetically divergent groups were found, largely corresponding to geography but with a clear exception of high genetic isolation in a highly touristic area. The effective sizes in the last few generations, as estimated from the random association among markers, never exceeded a few dozen of individuals. Our most important result is that several analyses converge in suggesting that genetic variation was shaped in all groups by a 7- to 45-fold demographic decline, which occurred between a few hundred and a few 1000 years ago. Remarkably, only weak evidence supports recent genetic impact related to human activities. We believe that the alpine B. variegata populations should be monitored and protected to stop their recent decline and to prevent local extinctions, with highest priority given to genetically isolated populations. Nonetheless, current genetic variation pattern, being mostly shaped in earlier times, suggests that complete recovery can be achieved. In general, our study is an example of how the potential for recovery should be inferred even under the co-occurrence of population decline, low genetic variation, and genetic bottleneck signals.

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Acknowledgments

Funding was provided by the University of Ferrara, the Autonomous Province of Trento under the Grande Progetto ACE-SAP (Alpine Ecosystems in a Changing Environment: Biodiversity Sensitivity and Adaptive Potential; University and Scientific Research Service, regulation number 23, 12 June 2008, Trento) and the Fondazione Edmund Mach under the FEM International Research School of Trentino (FIRS>T). We thank Alexis Marchesini and Barbara Crestanello for their assistance during sampling. We thank Matteo Girardi for invaluable assistance during lab work. Many thanks to Daniele Canestrelli and Heidi Hauffe for helpful comments during the study and on the manuscript. GB is also grateful to Christian Schlötterer for his hospitality at the Institute of Population Genetics in Vienna during the revision of this paper. SH was also supported by a Postdoctoral Fellow at the National Institute for Mathematical and Biological Synthesis, an Institute sponsored by the National Science Foundation through NSF Award #DBI-1300426, with additional support from The University of Tennessee, Knoxville.

Author contributions

LC and CV conceived and designed the study, collected the samples, and genetically typed the individuals. LC, GB and AB planned and performed the statistical analyses and interpreted them. GB wrote the manuscript, with the assistance of SH and LC. All authors examined data, discussed results, contributed to manuscript revision and approved the final draft.

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Correspondence to Giorgio Bertorelle.

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Data accessibility

Mitochondrial sequences are available in GenBank with accession numbers KP784451 to KP784453. Microsatellite data are deposited in Dryad with doi:10.5061/dryad.2vp4v.

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Cornetti, L., Benazzo, A., Hoban, S. et al. Ancient, but not recent, population declines have had a genetic impact on alpine yellow-bellied toad populations, suggesting potential for complete recovery. Conserv Genet 17, 727–743 (2016). https://doi.org/10.1007/s10592-016-0818-5

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