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The interaction of clonality, breeding system and genomics for a highly threatened plant species and the management implications

Biodiversity and Conservation volume 29, pages 3009–3029 (2020)Cite this article

Abstract

Clonal plants provide a challenge to ecological management and restoration programs. Clonal plants frequently occur as few genets over large spatial scales and may persist for hundreds of years. Hence population structures, effective population sizes and breeding systems of clonal plants are not well understood or managed at scales applicable to non-clonal species. This is a critical issue because clonality is a common trait including among threatened plants and more studies into the management requirements of clonal plant species are required. We investigate the impact of reducing the population size of a highly clonal species and how these impacts can be minimized. Persoonia hindii has a restricted distribution in forested ridges on Newnes Plateau west of Sydney, Australia. We collated data and surveyed populations, undertook assessments of reproductive patterns (flowering; pollination; fruit set and fall), and modelled pollen dispersal among genets. We relate this assessment to planning approaches uninformed by genet structure and reproductive patterns. Small sites likely function as discrete populations, each with low numbers of genets. Genet diversity at this site scale is important as it is associated with increased fruit set. Loss of plants from populations poses a significant risk to population level fitness if genet diversity is reduced. There is an urgent need for more biologically informed approaches for the management of clonal plant species.

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References

  • Ahrens C, Tierney DA, Rymer P (2020) Clonality and inbreeding amplifies genetic isolation and mate limitation in a rare montane woody plant (Persoonia hindii; Proteaceae). https://www.biorxiv.org/content/10.1101/2020.05.25.114231v1

  • Ally D, Ritland K, Otto SP (2010) Aging in a long-lived clonal tree. PLoS Biol 8:e1000454. https://doi.org/10.1371/journal.pbio.1000454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Appleby N, Edwards D, Batley J (2009) New technologies for ultra-high throughput genotyping in plants. Methods Mol Biol 513:19–39

    CAS  PubMed  Google Scholar 

  • Ayre DJ, Ottewell KM, Krauss SL, Whelan RJ (2009) Genetic structure of seedling cohorts following repeated wildfires in the fire-sensitive shrub Persoonia mollis ssp nectens. J Ecol 97:752–760

    Google Scholar 

  • Barrett SC (2010) Understanding plant reproductive diversity. Philos Trans R Soc B 365:99–109

    Google Scholar 

  • Barrett SC (2015) Influences of clonality on plant sexual reproduction. Proc Natl Acad Sci USA 112:8859–8866

    CAS  PubMed  Google Scholar 

  • Beekman M, Ratnieks FLW (2000) Long-range foraging by the honey-bee, Apis mellifera L. Funct Ecol 14:490–496

    Google Scholar 

  • Bembrick C (1980) Geology of the Blue Mountains. In: Herbert C, Helby R (eds) Western Sydney basin, a guide to the Sydney basin. Sydney, AU, Geological Survey of NSW, pp 134–161

    Google Scholar 

  • Bernhardt P, Weston PH (1996) The pollination ecology of Persoonia (Proteaceae) in eastern Australia. Telopea 6:775–804

    Google Scholar 

  • Broadhurst L, Coates D (2017) Plant conservation in australia: current directions and future challenges. Plant Diversity 39:348–356

    PubMed  PubMed Central  Google Scholar 

  • Busch JW, Schoen DJ (2008) The evolution of self-incompatibility when mates are limiting. Trends Plant Sci 13:128–136

    CAS  PubMed  Google Scholar 

  • Cadzow B, Carthew SM (2000) Breeding system and fruit development in Persoonia juniperina (Proteaceae). Cunninghamia 64:941–950

    Google Scholar 

  • Crone EE (2001) Is survivorship a better fitness surrogate than fecundity? Evolution 55:2611–2614

    CAS  PubMed  Google Scholar 

  • Crone EE, Rapp JM (2014) Resource depletion, pollen coupling, and the ecology of mast seeding. Ann N Y Acad Sci 1322:21–34

    CAS  PubMed  Google Scholar 

  • Davis HG, Taylor CM, Lambrinos JG, Strong DR (2004) Pollen limitation causes an Allee effect in a wind-pollinated invasive grass (Spartina alterniflora). Proc Natl Acad Sci 101:13804–13807

    CAS  PubMed  Google Scholar 

  • de Santaolalla , JLSH (2015) Biología y conservación de las especies de Sonchus sect Pustulati (Asteráceas): endemismos rupícolas del complejo Bético – Rifeño (Mediterráneo Occidental) Phd thesis, Universidad de Sevilla. https://www.researchgatenet/profile/Jose_Silva_Hernandez_De_Santaolalla. Accessed 3 May 2019

  • Department of Planning, Industry and Environment (2019) Unit of measure outcomes, species final data. Unpublished report, Department of Planning, Industry and Environment, NSW, Australia

    Google Scholar 

  • Emery NJ, Offord CA (2019) The effects of endocarp, heat-shock and short-term storage on the germination of Persoonia hirsuta (Proteaceae) seeds. Seed Sci Technol 47:107–112

    Google Scholar 

  • Engler R, Hordijk W, Guisan A (2012) The MIGCLIM R package—seamless integration of dispersal constraints into projections of species distributions. Ecography 35:872–887

    Google Scholar 

  • Erskine P, Fletcher A, Brownstein G, Blick R (2013) Persoonia hindii: Management and research program. https://data.centennialcoal.com.au/domino/centennialcoal/cc205.nsf/0/BBE73B01E82F7261CA2580D5000C92A5/$file/ATTD8ZNC.pdf

  • Field D, Ayre DJ, Whelan RJ (2005) The effect of local plant density on pollinator behavior and the breeding system of Persoonia bargoensis (Proteaceae). Int J Plant Sci 166:969–977

    Google Scholar 

  • Fox J, Sanford W (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks

    Google Scholar 

  • Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63

    Google Scholar 

  • Gill AM, Catling PC (2002) Fire regimes and biodiversity of forested landscapes of southern Australia. In: Bradstock RA, Williams JE, Gill AM (eds) Flammable Australia: the fire regimes and biodiversity of a continent. Cambridge, Cambridge Press, pp 351–369

    Google Scholar 

  • Gross CL, Caddy HAR (2006) Are differences in breeding mechanisms and fertility among populations contributing to rarity in Grevillea rhizomatosa (Proteaceae)? Am J Bot 93:1791–1799

    CAS  PubMed  Google Scholar 

  • Gross CL, Nelson PA, Haddadchi A, Fatemi M (2012) Somatic mutations contribute to genotypic diversity in sterile and fertile populations of the threatened shrub, Grevillea rhizomatosa (Proteaceae). Ann Bot 109:331–342

    CAS  PubMed  Google Scholar 

  • Gross CL, Fatemi M, Simpson IH (2016) Seed provenance for changing climates: early growth traits of nonlocal seed are better adapted to future climate scenarios, but not current field conditions. Restor Ecol 25:577–586

    Google Scholar 

  • Hopper SD (1996) The use of genetic information in establishing reserves for nature conservation. In: Szaro RC, Johnston DW (eds) Biodiversity in managed landscapes: theory and practice. UK, Oxford, pp 253–260

    Google Scholar 

  • IUCN (2019) Guidelines for using the IUCN red list categories and criteria, version 14. prepared by the standards and petitions subcommittee. https://www.iucnredlistorg/documents/RedListGuidelinespdf. Accessed 2 May 2019

  • James SH (1982) The relevance of genetic systems in Isotoma petraea to conservation practice. In: Groves RH, Ride WDL (eds) Species at risk research in Australia. Australian Academy of Science, Canberra, pp 63–71

    Google Scholar 

  • James EA, McDougall KL (2014) Spatial genetic structure reflects extensive clonality, low genotypic diversity and habitat fragmentation in Grevillea renwickiana (Proteaceae), a rare, sterile shrub from south-eastern Australia. Ann Bot 114:413–423

    PubMed  PubMed Central  Google Scholar 

  • Krauss SL (1994) Restricted gene flow within the morphologically complex species Persoonia mollis (Proteaceae): contrasting evidence from the mating system and pollen dispersal. Heredity 73:142–154

    Google Scholar 

  • Lynch AJJ, Barnes RW, Cambecèdes J, Vaillancourt RE (1998) Genetic evidence that Lomatia tasmanica (Proteacae) is an ancient clone. Aust J Bot 46:25–33

    Google Scholar 

  • Neal PR, Anderson GJ (2004) Does the ‘old bag’ makes a good ‘wind bag’? Comparison of four fabrics commonly used as exclusion bags in studies of pollination and reproductive biology. Ann Bot 93:603–607

    PubMed  PubMed Central  Google Scholar 

  • O’Brien EK, Denham AJ, Ayre DJ (2014) Patterns of genotypic diversity suggest a long history of clonality and population isolation in the Australian arid zone shrub Acacia carneorum. Plant Ecol 215:55–71

    Google Scholar 

  • Office of Environment and Heritage (2018) Biodiversity assessment method operational manual—stage 1. Office of Environment and Heritage, Parramatta, NSW, Australia. https://www.environmentnswgovau/topics/animals-and-plants/biodiversity/biobanking. Accessed 2 May 2019

  • Pearson RG, Dawson TP (2005) Long-distance plant dispersal and habitat fragmentation: identifying conservation targets for spatial landscape planning under climate change. Biol Conserv 123:389–401

    Google Scholar 

  • Pfab MF, Witkowski ETF (2000) A simple population viability analysis of the critically endangered Euphorbia clivicola RA Dyer under four management scenarios. Biol Conserv 96:263–270

    Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. Austria, Vienna

    Google Scholar 

  • Ralls K, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC, Sunnucks P, Frankham R (2018) Call for a paradigm shift in the genetic management of fragmented populations. Conserv Let 11:1–6

    Google Scholar 

  • Roberts DG, Forrest C, Denham AJ, Ayre DJ (2016) Varying levels of clonality and ploidy create barriers to gene flow and challenges for conservation of an Australian arid-zone ecosystem engineer, Acacia loderi. Biol J Lin Soc 118:330–343

    Google Scholar 

  • Rymer PD (2006) Plant rarity: species distributional patterns, population genetics, pollination biology and seed dispersal in Persoonia (Proteacae), PhD thesis, School of Biological Sciences, University of Wollongong. https://www.rouoweduau/theses/634/

  • Rymer PD, Whelan RJ, Ayre DJ, Weston PH, Russell KG (2005) Reproductive success and pollinator effectiveness differ in common and rare Persoonia species (Proteaceae). Biol Conserv 123:521–532

    Google Scholar 

  • Sork VL (2018) Genomic studies of local adaptation in natural plant populations. J Hered 109:3–15

    Google Scholar 

  • Tepedino VJ (2012) Overestimating population sizes of rare clonal plants. Conserv Biol 26:945–947

    CAS  PubMed  Google Scholar 

  • Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, de Siqueira MF, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Peterson AT, Phillips OL, Williams SE (2004) Extinction risk from climate change. Nature 427:145–148

    CAS  PubMed  Google Scholar 

  • Thrall PH, Encinas-Viso F, Hoebee SE, Young AG (2014) Life history mediates mate limitation and population viability in self-incompatible plant species. Ecol Evolut 4:673–687

    Google Scholar 

  • Tierney DA, Sommerville KD, Tierney KE, Fatemi M, Gross CL (2017) Trading populations—can biodiversity offsets effectively compensate for population losses? Biodivers Conserv 26:2115–2131

    Google Scholar 

  • Traill LW, Bradshaw CJA, Brook BW (2007) Minimum viable population size: a meta-analysis of 30 years of published estimates. Biol Conserv 139:159–166

    Google Scholar 

  • Vallejo-Marin M, Dorken ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Annu Rev Ecol Evol Syst 41:191–213

    Google Scholar 

  • Wallace HM, Maynard GV, Trueman SJ (2002) Insect flower visitors, foraging behaviour and their effectiveness as pollinators of Persoonia virgata R Br (Proteaceae). Aust J Entomol 41:55–59

    Google Scholar 

  • Wang X, Zhao W, Li L, You J, Ni B, Chen X (2018) Clonal plasticity and diversity facilitates the adaptation of Rhododendron aureum Georgi to alpine environment. PLoS ONE 13:e0197089. https://doi.org/10.1371/journal.pone.0197089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warton DI, Hui FK (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    PubMed  Google Scholar 

  • Wassertein RL, Schirm AL, Lazer NA (2019) Moving to a World Beyond “p < 0.05”. Am Stat 73 Suppl 1:1–19

    Google Scholar 

  • Young AG, Murray BG (2000) Genetic bottlenecks and dysgenic gene flow in re-established populations of the endangered grassland daisy Rutidosis leptorrhynchoides. Aust J Bot 48:409–416

    Google Scholar 

  • Young AG, Broadhurst LM, Thrall PH (2012) Non-additive effects of pollen limitation and self-incompatibility reduce plant reproductive success and population viability. Ann Bot 109:643–653

    PubMed  Google Scholar 

  • Zeng-miao D, Xin-sheng C, Yong-hong X, Ya-jun X, Zhi-yong H (2015) The role of seedling recruitment from juvenile populations of Carex brevicuspis (Cyperaceae) at the Dongting Lake wetlands China. Sci Rep 5:8646. https://doi.org/10.1038/srep08646

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by research fellowships in the School of Life and Environmental Sciences, The University of Sydney and The Centre for Mined Land Rehabilitation, University of Queensland to David Tierney. The contributions of two anonymous reviewers substantially improved this manuscript. Field assistance was provided by Tom Le Breton, Eren Delgado, Kate Tierney and Heidi Zimmer.

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Authors and Affiliations

  1. School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, 2006, Australia

    D. A. Tierney

  2. Centre for Mined Land Rehabilitation, The University of Queensland, St Lucia, QLD, 4067, Australia

    D. A. Tierney

  3. Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW, 2753, Australia

    C. Ahrens & P. Rymer

  4. School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, NSW, 2522, Australia

    T. D. Auld

  5. Centre for Ecosystem Science, University of New South Wales, Kensington, 2052, Australia

    T. D. Auld

Authors
  1. D. A. Tierney
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  2. C. Ahrens
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  3. P. Rymer
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  4. T. D. Auld
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Correspondence to D. A. Tierney.

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Communicated by Daniel Sanchez Mata.

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Tierney, D.A., Ahrens, C., Rymer, P. et al. The interaction of clonality, breeding system and genomics for a highly threatened plant species and the management implications. Biodivers Conserv 29, 3009–3029 (2020). https://doi.org/10.1007/s10531-020-02012-7

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  • DOI: https://doi.org/10.1007/s10531-020-02012-7

Keywords

  • Clonal plants
  • Pollination
  • Population genetics
  • Genet
  • Ramet
  • Population size

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