Skip to main content

Selection and localised genetic structure in the threatened Manauense Harlequin Frog (Bufonidae: Atelopus manauensis)

Abstract

Knowledge of genome-wide variation and the processes influencing gene flow are critical to managing threatened species. Here, we characterise genetic diversity and the environmental features associated with connectivity for a narrowly distributed and threatened Amazonian frog, Atelopus manauensis. We sampled 94 individuals throughout the upper, middle and lower courses from each of the five major rivers covering the species’ known geographic range and genotyped each individual at 3859 single nucleotide polymorphisms (SNPs). Genetic variation was significantly subdivided into six groups, each mostly containing individuals sampled within the same major river system. The genetic distances among these groups increased with geographic distance, and open forests and the extremities of the altitude gradient were associated with less genetic connectivity. Using FST outlier approaches and environmental association analyses, we identified SNPs indicative of localised adaptation, with 28 SNPs significantly associated with forest biomass and altitude. Evidence of divergent selection among the six genetic clusters suggests the presence of six Evolutionary Significant Units (ESUs). Overall, the ESUs were characterized by low contemporary effective population sizes (NE < 100) suggesting that genetic variation will be lost by random genetic drift. We demonstrate surprisingly high levels of divergence across the limited distribution of A. manauensis and suggest that each of the six adaptively divergent lineages be considered in conservation planning.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Data availability

The 3859 SNPs dataset used to produce the current study is available in Additional Data S1 and can also be available by authors on request. Environmental variables used during the current study can be obtained through the methods described in “Material and Methods” section from the coordinates provided in Online Resource Table S1 and raster layers available in cited literature. Biological material deposition is described in “Material and Methods” section.

Code availability

Codes for analyses are available in cited literature.

References

Download references

Acknowledgements

The authors would like to thank all the people who aided RFJ in field sampling. Sincere thanks are due to V. Albuquerque for taking RFJ to all sampling locations accessed by roads; E Polo, J O'Hare and W Ashley for helping in statistical analyses; A Santana and M Ferrão for suggestions in tissues preparation and shipment; N Higuchi, JL Camargo and Tenente SC dos S Gomes and all Army personnel (Centro de Instruções de Guerra na Selva do Exército Brasileiro – CIGS/EB) for logistic support at LBA/ZF-2, ARIE PDBFF and CIGS/EB training site, respectively; FP Werneck, F Annibale, L Lourenço, C Cornelius, F Toledo and M Anciães for valuable comments in an early draft of this manuscript. We also thank the Editor and two anonymous reviewers for their insightful comments on an early draft.

Funding

This work was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Universal Grant No.: 401120/2016-3 granted to APL) and by the Coordenação de Aperfeiçoamento do Pessoal de Nível Superior through its Programa de Suporte para Núcleos de Excelência (CAPES/PROEX Grant No.: 0616/2018). RFJ received a PhD scholarship from CAPES and Fundo de Amparo à Pesquisa do Estado do Amazonas (CAPES/FAPEAM Grant No.: 24/2014) and a partial-abroad PhD scholarship (Programa de Doutorado Sanduíche no Exterior – CAPES/PDSE Grant No.: 41/2018).

Author information

Authors and Affiliations

Authors

Contributions

Not applicable.

Corresponding author

Correspondence to Rafael Filgueira Jorge.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Ethical approval

Individuals were collected under permission number 56759 from the Sistema de Autorização e Informação da Biodiversidade do Instituto Chico Mendes de Conservação da Biodiversidade (SISBIO/ICMBio). This study was approved by the Instituto Nacional de Pesquisas da Amazônia (INPA) ethics committee (registration number 002/2017 – Comissão de Ética no Uso de Animais – CEUA/INPA).

Consent to participate

All authors consent to participate in this study.

Consent for publication

The authors agree for publication of the paper and all data relevant to this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 9434 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jorge, R.F., Lima, A.P. & Stow, A.J. Selection and localised genetic structure in the threatened Manauense Harlequin Frog (Bufonidae: Atelopus manauensis). Conserv Genet 23, 559–574 (2022). https://doi.org/10.1007/s10592-022-01436-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-022-01436-8

Keywords

  • Amazonia
  • Threatened frog
  • Connectivity
  • Landscape heterogeneity
  • Conservation