Stocktake Sale on now: wide range of books at up to 70% off!
Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE (Open Access)

Evaluating conservation strategies for the endangered daisy Schoenia filifolia subsp. subulifolia (Asteraceae): fitness consequences of genetic rescue and hybridisation with a widespread subspecies

Leonie Monks https://orcid.org/0000-0001-9170-7738 A B * , David Coates A , Shelley McArthur A and Rachel J. Standish B
+ Author Affiliations
- Author Affiliations

A Biodiversity Conservation Science, Department of Biodiversity, Conservation and Attractions, Locked Bag 104, Bentley Delivery Centre, Bentley, WA 6983, Australia.

B Harry Butler Institute, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia.

* Correspondence to: leonie.monks@dbca.wa.gov.au

Handling Editor: Susan Hoebee

Australian Journal of Botany 70(5) 344-357 https://doi.org/10.1071/BT22006
Submitted: 21 January 2022  Accepted: 4 July 2022   Published: 27 July 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: To establish translocated populations of threatened plants with the genetic resources to adapt to changing environmental conditions, the source of propagation material is an important consideration.

Aim: We investigated the fitness consequences of genetic rescue and admixture for the threatened annual daisy Schoenia filifolia subsp. subulifolia, and the common S. filifolia subsp. filifolia, to inform seed-sourcing strategies for translocations of the threatened subspecies.

Methods: We evaluated genetic diversity of two populations of S. filifolia subsp. subulifolia and four populations of S. filifolia subsp. filifolia by using microsatellite markers. We grew seedlings from each study population and cross-pollinated inflorescences within and among populations of the same subspecies, and between subspecies. We evaluated the fitness consequences of each cross by using seed set, seed weight and seed viability.

Key results: There was a lower genetic diversity in the small (<50 plants, Nar = 3.28, He = 0.42) compared to the large (>10 000 plants, Nar = 4.42, He = 0.51) population of S. filifolia subsp. subulifolia, although none of the measures was significantly different, and seed fitness was slightly, although not significantly, reduced in interpopulation crosses compared with the small population. Genetic diversity was similar between the threatened and widespread subspecies; however, the subspecies were genetically divergent (Fst = 0.242–0.294) and cross-pollination between subspecies produced negligible amounts of seeds (<3% seed set).

Conclusions: Although genetic rescue or admixture of S. filifolia subsp. subulifolia would not necessarily result in greatly increased levels of genetic diversity or seed fitness, we still consider it a potential option. Negligible seed set in crosses between subspecies indicates that deliberate hybridisation is not a possibility.

Implications: Studies of fitness consequences of admixture or genetic rescue are rare yet critical to assessing the benefits of different translocation strategies.

Keywords: admixture, Asteraceae, demographic rescue, environmental change, genetic diversity, genetic rescue, reintroduction, seed fitness, threatened plants, translocation.


References

Ayre BM, Roberts DG, Phillips RD, Hopper SD, Krauss SL (2019) Near-neighbour optimal outcrossing in the bird-pollinated Anigozanthos manglesii. Annals of Botany 124, 423–436.
Near-neighbour optimal outcrossing in the bird-pollinated Anigozanthos manglesii.Crossref | GoogleScholarGoogle Scholar |

Baskett ML, Gomulkiewicz R (2011) Introgressive hybridization as a mechanism for species rescue. Theoretical Ecology 4, 223–239.
Introgressive hybridization as a mechanism for species rescue.Crossref | GoogleScholarGoogle Scholar |

Bell DA, Robinson ZL, Funk WC, Fitzpatrick SW, Allendorf FW, Tallmon DA, Whiteley AR (2019) The exciting potential and remaining uncertainties of genetic rescue. Trends in Ecology & Evolution 34, 1070–1079.
The exciting potential and remaining uncertainties of genetic rescue.Crossref | GoogleScholarGoogle Scholar |

Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. The Plant Cell 16, S228–S245.
Understanding apomixis: recent advances and remaining conundrums.Crossref | GoogleScholarGoogle Scholar |

Billingham MR, Simões T, Reusch TBH, Ester A, Serrão EA (2007) Genetic sub-structure and intermediate optimal outcrossing distance in the marine angiosperm Zostera marina. Marine Biology 152, 793–801.
Genetic sub-structure and intermediate optimal outcrossing distance in the marine angiosperm Zostera marina.Crossref | GoogleScholarGoogle Scholar |

Bouzat JL, Johnson JA, Toepfer JE, Simpson SA, Esker TL, Westemeier RL (2009) Beyond the beneficial effects of translocations as an effective tool for the genetic restoration of isolated populations. Conservation Genetics 10, 191–201.
Beyond the beneficial effects of translocations as an effective tool for the genetic restoration of isolated populations.Crossref | GoogleScholarGoogle Scholar |

Broadhurst LM, Lowe A, Coates DJ, Cunningham SA, McDonald M, Vesk PA, Yates C (2008) Seed supply for broadscale restoration: maximizing evolutionary potential. Evolutionary Applications 1, 587–597.
Seed supply for broadscale restoration: maximizing evolutionary potential.Crossref | GoogleScholarGoogle Scholar |

Byrne M, Macdonald B, Francki M (2001) Incorporation of sodium sulfite into extraction protocol minimizes degradation of Acacia DNA. BioTechniques 30, 742–748.
Incorporation of sodium sulfite into extraction protocol minimizes degradation of Acacia DNA.Crossref | GoogleScholarGoogle Scholar |

Byrne M, Stone L, Millar MA (2011) Assessing genetic risk in revegetation. Journal of Applied Ecology 48, 1365–1373.
Assessing genetic risk in revegetation.Crossref | GoogleScholarGoogle Scholar |

Chybicki IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. Journal of Heredity 100, 106–113.
Simultaneous estimation of null alleles and inbreeding coefficients.Crossref | GoogleScholarGoogle Scholar |

Commander LE, Coates DJ, Broadhurst L, Offord CA, Makinson RO, Matthes M (2018) ‘Guidelines for the translocation of threatened plants in Australia.’ 3rd edn. (Australian Network for Plant Conservation: Canberra, ACT, Australia)

DeMauro MM (1993) Relationship of breeding system to rarity in the Lakeside Daisy (Hymenoxys acaulis var. glabra). Conservation Biology 7, 542–550.
Relationship of breeding system to rarity in the Lakeside Daisy (Hymenoxys acaulis var. glabra).Crossref | GoogleScholarGoogle Scholar |

Doyle J (1991) DNA protocols for plants. In ‘Molecular techniques in taxonomy. Vol. 57’. NATO ASI Series H: cell biology. (Eds GM Hewitt, AW Johnston, JPW Young) pp. 283–293. (Springer-Verlag: Berlin, Germany)

Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |

Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology 16, 463–475.
Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management.Crossref | GoogleScholarGoogle Scholar |

Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software structure: a simulation study.Crossref | GoogleScholarGoogle Scholar |

Frankham R (2012) How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination. Heredity 108, 167–178.
How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination.Crossref | GoogleScholarGoogle Scholar |

Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Molecular Ecology 24, 2610–2618.
Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow.Crossref | GoogleScholarGoogle Scholar |

Frankham R (2016) Genetic rescue benefits persist to at least the F3 generation, based on a meta-analysis. Biological Conservation 195, 33–36.
Genetic rescue benefits persist to at least the F3 generation, based on a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conservation Biology 25, 465–475.
Predicting the probability of outbreeding depression.Crossref | GoogleScholarGoogle Scholar |

Frankham R, Ballou JD, Ralls K, Eldridge M, Dudash MR, Fenster CB, Lacy RC, Sunnucks P (2017) ‘Genetic management of fragmented animal and plant populations.’ (Oxford University Press: Oxford, UK)

Gavin-Smyth N, Kramer AT, Urbina-Casanova R, Vitt P, Fant JB (2021) Genetic rescue reduces mate limitation in a threatened, clonal, and self-incompatible plant species. Restoration Ecology 29, e13458
Genetic rescue reduces mate limitation in a threatened, clonal, and self-incompatible plant species.Crossref | GoogleScholarGoogle Scholar |

Guerrant EO (1996) Designing populations: demographic, genetic, and horticultural dimensions. In ‘Restoring diversity: strategies for reintroduction of endangered plants’. (Eds DA Falk, CI Millar, M Olwell) pp. 127–155. (Island Press: Covelo, CA, USA)

Harrisson KA, Pavlova A, Gonc A, da Silva A, Rose R, Bull JK, Lancaster ML, Murray N, Quin B, Menkhorst P, Magrath MJL, Sunnucks P (2016) Scope for genetic rescue of an endangered subspecies though re-establishing natural gene flow with another subspecies. Molecular Ecology 25, 1242–1258.
Scope for genetic rescue of an endangered subspecies though re-establishing natural gene flow with another subspecies.Crossref | GoogleScholarGoogle Scholar |

Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59, 1633–1638.
A standardized genetic differentiation measure.Crossref | GoogleScholarGoogle Scholar |

Hedrick PW, Garcia-Dorado A (2016) Understanding inbreeding depression, purging, and genetic rescue. Trends in Ecology & Evolution 31, 940–952.
Understanding inbreeding depression, purging, and genetic rescue.Crossref | GoogleScholarGoogle Scholar |

Hufbauer RA, Szucs M, Kasyon E, Youngberg C, Koontz MJ, Richards C, Tuff T, Melbourne BA (2015) Three types of rescue can avert extinction in a changing environment. Proceedings of the National Academy of Sciences 112, 10557–10562.
Three types of rescue can avert extinction in a changing environment.Crossref | GoogleScholarGoogle Scholar |

Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends in Ecology & Evolution 18, 147–155.
Plant ecotypes: genetic differentiation in the age of ecological restoration.Crossref | GoogleScholarGoogle Scholar |

Hufford KM, Krauss SL, Veneklaas EJ (2012) Inbreeding and outbreeding depression in Stylidium hispidum: implications for mixing seed sources for ecological restoration. Ecology and Evolution 2, 2262–2273.
Inbreeding and outbreeding depression in Stylidium hispidum: implications for mixing seed sources for ecological restoration.Crossref | GoogleScholarGoogle Scholar |

Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.
CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure.Crossref | GoogleScholarGoogle Scholar |

Johnson WE, Onorato DP, Roelke ME, Land ED, Cunningham M, Belden RC, McBride R, Jansen D, Lotz M, Shindle D, Howard J, Wildt DE, Penfold LM, Hostetler JA, Oli MK, O’Brien SJ (2010) Genetic restoration of the Florida panther. Science 329, 1641–1645.
Genetic restoration of the Florida panther.Crossref | GoogleScholarGoogle Scholar |

Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes 5, 187–189.
HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness.Crossref | GoogleScholarGoogle Scholar |

Kronenberger JA, Funk WC, Smith JW, Fitzpatrick SW, Angeloni LM, Broder ED, Ruell EW (2017) Testing the demographic effects of divergent immigrants on small populations of Trinidadian guppies. Animal Conservation 20, 3–11.
Testing the demographic effects of divergent immigrants on small populations of Trinidadian guppies.Crossref | GoogleScholarGoogle Scholar |

Lande R (1988) Genetics and demography in biological conservation. Science 241, 1455–1460.
Genetics and demography in biological conservation.Crossref | GoogleScholarGoogle Scholar |

Leffler EM, Bullaughey K, Matute DR, Meyer WK, Ségurel L, Venkat A, Andolfatto P, Przeworski M (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biology 10, e1001388
Revisiting an old riddle: what determines genetic diversity levels within species?Crossref | GoogleScholarGoogle Scholar |

Maschinski J, Albrecht MA (2017) Center for plant conservation’s best practice guidelines for the reintroduction of rare plants. Plant Diversity 39, 390–395.
Center for plant conservation’s best practice guidelines for the reintroduction of rare plants.Crossref | GoogleScholarGoogle Scholar |

Maschinski J, Albrecht MA, Monks L, Haskins KE (2012) Centre for Plant Conservation best reintroduction practice guidelines. In ‘Plant reintroduction in a changing climate: promises and perils’. (Eds J Maschinski, KE Haskins) pp. 277–306. (Island Press: Washington, DC, USA)

Maschinski J, Wright SJ, Koptur S, Pinto-Torres EC (2013) When is local the best paradigm? Breeding history influences conservation reintroduction survival and population trajectories in times of extreme climate events. Biological Conservation 159, 277–284.
When is local the best paradigm? Breeding history influences conservation reintroduction survival and population trajectories in times of extreme climate events.Crossref | GoogleScholarGoogle Scholar |

Meglécz E, Costedoat C, Dubut V, Gilles A, Malausa T, Pech N, Martin J-F (2010) QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics 26, 403–404.
QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects.Crossref | GoogleScholarGoogle Scholar |

Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Molecular Ecology Resources 11, 5–18.
Assessing population structure: FST and related measures.Crossref | GoogleScholarGoogle Scholar |

Montalvo AM, Ellstrand NC (2001) Nonlocal transplantation and outbreeding depression in the subshrub Lotus scoparius (Fabaceae). American Journal of Botany 88, 258–269.
Nonlocal transplantation and outbreeding depression in the subshrub Lotus scoparius (Fabaceae).Crossref | GoogleScholarGoogle Scholar |

Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |

Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research: an update. Bioinformatics 28, 2537–2539.
GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research: an update.Crossref | GoogleScholarGoogle Scholar |

Pickup M, Field DL, Rowell DM, Young AG (2013) Source population characteristics affect heterosis following genetic rescue of fragmented plant populations. Proceedings of the Royal Society B: Biological Sciences 280, 20122058
Source population characteristics affect heterosis following genetic rescue of fragmented plant populations.Crossref | GoogleScholarGoogle Scholar |

Plummer JA, Rogers AD, Turner DW, Bell DT (2001) Light, nitrogenous compounds, smoke and GA3 break dormancy and enhance germination in the Australian everlasting daisy Shoenia filifolia subsp. subulifolia. Seed Science and Technology 29, 321–330.

Png GK (2012) Pollination biology of Western Australia’s showy everlasting daisy (Schoenia filifolia subsp. subulifolia). Australasian Plant Conservation 21, 23–24.

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
Inference of population structure using multilocus genotype data.Crossref | GoogleScholarGoogle 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. Conservation Letters 11, e12412
Call for a paradigm shift in the genetic management of fragmented populations.Crossref | GoogleScholarGoogle Scholar |

Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.
GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism.Crossref | GoogleScholarGoogle Scholar |

Shi J, Joshi J, Tielbörger K, Verhoeven KJF, Macel M (2018) Costs and benefits of admixture between foreign genotypes and local populations in the field. Ecology and Evolution 8, 3675–3684.
Costs and benefits of admixture between foreign genotypes and local populations in the field.Crossref | GoogleScholarGoogle Scholar |

Smith MG, Jones A (2018) ‘Threatened and priority flora list, 5 December 2018.’ (Department of Biodiversity, Conservation and Attractions: Perth, WA, Australia)

Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends in Ecology & Evolution 19, 489–496.
The alluring simplicity and complex reality of genetic rescue.Crossref | GoogleScholarGoogle Scholar |

Valdiani A, Kadir MA, Saad MS, Talei D, Tan S-G (2012) Intra-specific hybridization: generator of genetic diversification and heterosis in Andrographis paniculata Nees. A bridge from extinction to survival. Gene 505, 23–36.
Intra-specific hybridization: generator of genetic diversification and heterosis in Andrographis paniculata Nees. A bridge from extinction to survival.Crossref | GoogleScholarGoogle Scholar |

Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Resources 4, 535–538.
MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar |

Van Rossum F, Hardy OJ, Le Pajolec S, Raspé O (2020) Genetic monitoring of translocated plant populations in practice. Molecular Ecology 29, 4040–4058.
Genetic monitoring of translocated plant populations in practice.Crossref | GoogleScholarGoogle Scholar |

Waser NM, Price MV (1989) Optimal outcrossing in Ipomopsis aggregata: seed set and offspring fitness. Evolution 43, 1097–1109.
Optimal outcrossing in Ipomopsis aggregata: seed set and offspring fitness.Crossref | GoogleScholarGoogle Scholar |

Weeks AR, Sgro CM, Young AG, Frankham R, Mitchell NJ, Miller KA, Byrne M, Coates DJ, Eldridge MDB, Sunnucks P, Breed MF, James EA, Hoffmann AA (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evolutionary Applications 4, 709–725.
Assessing the benefits and risks of translocations in changing environments: a genetic perspective.Crossref | GoogleScholarGoogle Scholar |

Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends in Ecology & Evolution 30, 42–49.
Genetic rescue to the rescue.Crossref | GoogleScholarGoogle Scholar |

Whitney KD, Ahern JR, Campbell LG, Albert LP, King MS (2010) Patterns of hybridization in plants. Perspectives in Plant Ecology, Evolution and Systematics 12, 175–182.
Patterns of hybridization in plants.Crossref | GoogleScholarGoogle Scholar |

Wilson PG (1992) The Lawrencella complex (Asteraceae: Gnaphalieae: Angianthinae) of Australia. Nuytsia 8, 361–377.

Zecherle LJ, Nichols HJ, Bar-David S, Brown RP, Hipperson H, Horsburgh GJ, Templeton AR (2021) Subspecies hybridization as a potential conservation tool in species reintroductions. Evolutionary Applications 14, 1216–1224.
Subspecies hybridization as a potential conservation tool in species reintroductions.Crossref | GoogleScholarGoogle Scholar |