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Conservation genomics of an Australian cycad Cycas calcicola, and the Absence of Key Genotypes in Botanic Gardens

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Abstract

Understanding the genetic diversity of wild populations is fundamental to conserving species in-situ and ex-situ. To aid conservation plans and to inform ex-situ conservation, we examined the genetic diversity of the cycad Cycas calcicola (Cycadaceae). Samples were collected from wild populations in the Litchfield National Park and Katherine regions in the Northern Territory, Australia. Additional samples were obtained from botanic garden plants that were originally collected in the Katherine region, Daly River and Spirit Hills in the Northern Territory, Australia. Using RADseq we recovered 2271 informative genome-wide SNPs, revealing low to moderate levels of gene diversity (uHe = 0.037 to 0.135), very low levels of gene flow, and significant levels of inbreeding (mean FIS = 0.491). Population structure and multivariate analysis showed that populations fall into two genetic groups (Katherine vs Litchfield + Daly River + Spirit Hills). Genetic differentiation was twice as high between populations of the Katherine and Litchfield regions (FST ~ 0.1) compared to within these two regions (FST ~ 0.05). Increasing population fragmentation together with high levels of inbreeding and very little gene flow are concerning for the future adaptability of this species. The results indicated that the ex-situ collections (1) had significantly lower genetic diversity than the wild populations, and (2) only partly capture the genetic diversity present, particularly because the Litchfield National Park populations are not represented. We recommend that ex-situ collections be expanded to incorporate the genetic diversity found in Litchfield National Park and to increase the number of representatives from Daly River/Spirit Hills, and that in-situ populations from the Katherine and Greater Litchfield regions be conserved as separate management units.

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Data availability and material

RAW fastq sequinning files, assemblies and will be uploaded to NCBI GenBank after the initial review process has been completed, to be accessible for publication.

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Acknowledgements

We wish to acknowledge funding received from the Australian Flora Foundation, the Australasian Systematic Botany Society, and The Nature Conservatory—The Thomas Foundation for an Australian Conservation Taxonomy Award. Support from the Biotechnology and Biological Sciences Research Council (BBSRC) UK and the EASTBIO Doctoral Training Partnership studentship at the University of Edinburgh is greatly acknowledged. We wish to thank Lichfield National Park and Charles Darwin University for allowing us to collect samples. Joe Perner of Cycad International for helping us locate population of C. calcicola around the Katherine region. The staff at the Royal Botanic Gardens and Domain Trust, in particular, Carolyn Connolly is thanked for her support in the molecular laboratory, Hannah McPherson for helping with the initial quality testing of data. We also thank the California Academy of Sciences; Joe Russack for his support and assistance in data assembly and Athena Lam and Boni Cruz for their support in the molecular laboratory. The assistance of various botanic gardens is acknowledged for providing C. calcicola leaf tissue samples, including Patrick Griffith and Michael Calonje of the Montgomery Botanical Center, Florida, USA and George Brown Darwin Botanic Garden Darwin, Northern Territory, Australia. We wish to thank, Alan Meerow of the United States Department of Agriculture for his support and advice regarding population genetics of cycads. The Royal Botanic Garden Edinburgh is supported by the Scottish Government’s Rural and Environment Science and Analytical Services Division.

Funding

1. Australian Flora Foundation—Research grant—Australia. 2. The Australasian Systematic Botany Society and The Nature Conservatory–The Thomas Foundation for an Australian Conservation Taxonomy Award—Australia. 3. Biotechnology and Biological Sciences Research Council (BBSRC) UK and the EASTBIO Doctoral Training Partnership—UK, Ref: 1429569.

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Author notes

  1. James A. R. Clugston and Markus Ruhsam contributed equally to this work.

Authors and Affiliations

  1. National Herbarium of New South Wales, Royal Botanic Gardens and Domain Trust, Mrs Macquaries Rd, Sydney, NSW, 2000, Australia

    James A. R. Clugston

  2. Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH35LR, Scotland, UK

    James A. R. Clugston, Markus Ruhsam & Gregory J. Kenicer

  3. School of Biological Sciences, College of Science and Engineering, Institute of Molecular Plant Sciences, The University of Edinburgh, The Kings Building, West Mains Road, Edinburgh, EH9 3JN, Scotland, UK

    James A. R. Clugston & Richard Milne

  4. School of Life and Environmental Sciences, The University of Sydney, Heydon-Laurence Building A08, Camperdown, NSW, 2006, Australia

    Murray Henwood

  5. California Academy of Sciences, 55 Music Concourse Dr, San Francisco, CA, 94118, USA

    Nathalie S. Nagalingum

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  1. James A. R. Clugston
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  2. Markus Ruhsam
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  3. Gregory J. Kenicer
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Contributions

JARC—planning, conducted fieldwork, research, lab work, bioinformatics, main writer. MR—major contributor second writer, bioinformatics, statistics, manuscript structure. GJK—PhD supervisor, advice and manuscript feedback. MJH—PhD supervisor, manuscript editor, advice and input into research aims and outputs. RM—PhD supervisor, advice and manuscript feedback. NSN—PhD supervisor, obtained funding, conceived, planned and oversaw project, planned and conducted fieldwork, collected cultivated samples, manuscript editor, and provided feedback and overall guidance on manuscript.

Corresponding authors

Correspondence to James A. R. Clugston or Nathalie S. Nagalingum.

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Clugston, J.A.R., Ruhsam, M., Kenicer, G.J. et al. Conservation genomics of an Australian cycad Cycas calcicola, and the Absence of Key Genotypes in Botanic Gardens. Conserv Genet 23, 449–465 (2022). https://doi.org/10.1007/s10592-022-01428-8

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