Population genomics of a predatory mammal reveals patterns of decline and impacts of exposure to toxic toads

Brenton von Takach, Louis Ranjard, Christopher P. Burridge, Skye F. Cameron, Teigan Cremona, Mark D.B. Eldridge, Diana O. Fisher, Stephen Frankenberg, Brydie M. Hill, Rosemary Hohnen, Chris J. Jolly, Ella Kelly, Anna J. MacDonald, Adnan Moussalli, Kym Ottewell, Ben L. Phillips, Ian J. Radford, Peter B.S. Spencer, Gavin J. Trewella, Linette S. UmbrelloSam C. Banks

Research output: Contribution to journalArticlepeer-review

15 Citations (Scopus)
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Abstract

Mammal declines across northern Australia are one of the major biodiversity loss events occurring globally. There has been no regional assessment of the implications of these species declines for genomic diversity. To address this, we conducted a species-wide assessment of genomic diversity in the northern quoll (Dasyurus hallucatus), an Endangered marsupial carnivore. We used next generation sequencing methods to genotype 10,191 single nucleotide polymorphisms (SNPs) in 352 individuals from across a 3220-km length of the continent, investigating patterns of population genomic structure and diversity, and identifying loci showing signals of putative selection. We found strong heterogeneity in the distribution of genomic diversity across the continent, characterized by (i) biogeographical barriers driving hierarchical population structure through long-term isolation, and (ii) severe reductions in diversity resulting from population declines, exacerbated by the spread of introduced toxic cane toads (Rhinella marina). These results warn of a large ongoing loss of genomic diversity and associated adaptive capacity as mammals decline across northern Australia. Encouragingly, populations of the northern quoll established on toad-free islands by translocations appear to have maintained most of the initial genomic diversity after 16 years. By mapping patterns of genomic diversity within and among populations, and investigating these patterns in the context of population declines, we can provide conservation managers with data critical to informed decision-making. This includes the identification of populations that are candidates for genetic management, the importance of remnant island and insurance/translocated populations for the conservation of genetic diversity, and the characterization of putative evolutionarily significant units.

Original languageEnglish
Pages (from-to)5468-5486
Number of pages19
JournalMolecular Ecology
Volume31
Issue number21
Early online dateSept 2022
DOIs
Publication statusPublished - Nov 2022

Bibliographical note

Funding Information:
We acknowledge the Traditional Custodians of the lands on which the research presented here was undertaken, and pay our respects to their Elders past, present and emerging. We also acknowledge the contribution of the Oz Mammals Genomics Initiative consortium (https://ozmammalsgenomics.com/consortium/) in the generation of data used in this publication. The Initiative is supported by funding from Bioplatforms Australia through the Australian Government National Collaborative Research Infrastructure Strategy (NCRIS). Thanks to Serina McConnell, Bethany Jackson, Sally South, Bill Sherwin, Alex Drew and Sally Drapes for organization and handling of tissue samples or extraction product, and Tom Schmidt for advice regarding heterozygosity calculations. Registration numbers of tissue samples provided by the CSIRO Australian National Wildlife Collection are M28622, M37124 and M37913 (https://ror.org/059mabc80). Many NT tissue samples were collected in collaboration with the Flora and Fauna Division, Department of Environment, Parks and Water Security, Northern Territory Government. Groote Eylandt (2018) samples were provided by Robbie S. Wilson through funding FT150100492 and DP180103134, awarded to R.S.W. We are grateful to funding from Charles Darwin University to Sam C. Banks that was instrumental in development of a mammal conservation genomics research program. We thank the Pawsey Supercomputing Centre for access to and technical support with the Nimbus cloud computing infrastructure, Philipp Bayer for assistance with plink and Kevin Murray for discussion of demographic inference methods. We also wish to acknowledge the use of New Zealand eScience Infrastructure (NeSI) high-performance computing facilities (https://www.nesi.org.nz). New Zealand's national facilities are provided by NeSI and funded jointly by NeSI's collaborator institutions and through the Ministry of Business, Innovation & Employment's Research Infrastructure programme. B.v.T. also acknowledges the support of the Forrest Research Foundation. We thank three anonymous reviewers and subject editor Prof. Angus Davison for their constructive comments which greatly improved the manuscript. Open access publishing facilitated by Curtin University, as part of the Wiley - Curtin University agreement via the Council of Australian University Librarians.

Funding Information:
We acknowledge the Traditional Custodians of the lands on which the research presented here was undertaken, and pay our respects to their Elders past, present and emerging. We also acknowledge the contribution of the Oz Mammals Genomics Initiative consortium ( https://ozmammalsgenomics.com/consortium/ ) in the generation of data used in this publication. The Initiative is supported by funding from Bioplatforms Australia through the Australian Government National Collaborative Research Infrastructure Strategy (NCRIS). Thanks to Serina McConnell, Bethany Jackson, Sally South, Bill Sherwin, Alex Drew and Sally Drapes for organization and handling of tissue samples or extraction product, and Tom Schmidt for advice regarding heterozygosity calculations. Registration numbers of tissue samples provided by the CSIRO Australian National Wildlife Collection are M28622, M37124 and M37913 ( https://ror.org/059mabc80 ). Many NT tissue samples were collected in collaboration with the Flora and Fauna Division, Department of Environment, Parks and Water Security, Northern Territory Government. Groote Eylandt (2018) samples were provided by Robbie S. Wilson through funding FT150100492 and DP180103134, awarded to R.S.W. We are grateful to funding from Charles Darwin University to Sam C. Banks that was instrumental in development of a mammal conservation genomics research program. We thank the Pawsey Supercomputing Centre for access to and technical support with the Nimbus cloud computing infrastructure, Philipp Bayer for assistance with plink and Kevin Murray for discussion of demographic inference methods. We also wish to acknowledge the use of New Zealand eScience Infrastructure (NeSI) high‐performance computing facilities ( https://www.nesi.org.nz ). New Zealand's national facilities are provided by NeSI and funded jointly by NeSI's collaborator institutions and through the Ministry of Business, Innovation & Employment's Research Infrastructure programme. B.v.T. also acknowledges the support of the Forrest Research Foundation. We thank three anonymous reviewers and subject editor Prof. Angus Davison for their constructive comments which greatly improved the manuscript. Open access publishing facilitated by Curtin University, as part of the Wiley ‐ Curtin University agreement via the Council of Australian University Librarians.

Publisher Copyright:
© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

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