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Limited pollen-mediated dispersal and partial self-incompatibility in the rare ironstone endemic Tetratheca paynterae subsp. paynterae increase the risks associated with habitat loss

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Abstract

Patterns of mating and dispersal are key factors affecting the dynamics, viability and evolution of plant populations. Changes in mating system parameters can provide evidence of anthropogenic impacts on populations of rare plants. Tetratheca paynterae subsp. paynterae is a critically endangered perennial shrub confined to a single ironstone range in Western Australia. Mining of the range removed 25% of plants in 2004 and further plants may be removed if the viability of the remaining populations is not compromised. To provide baseline genetic data for monitoring mining impacts, we characterised the mating system and pollen dispersal over two seasons in T. paynterae subsp. paynterae and compared mating system parameters with two other ironstone endemics, T. paynterae subsp. cremnobata and T. aphylla subsp. aphylla that were not impacted by mining. T. paynterae subsp. paynterae was the only taxon showing evidence of inbreeding (t m = 0.89), although hand pollination revealed pre-zygotic self-incompatibility limits the production of seed from self-pollen. In a year of lower fruit set (2005), the estimate of correlated paternity increased from 20 to 35%. Direct estimates of realised pollen dispersal, made by paternity assignment in two small populations where all adult plants were genotyped, revealed a leptokurtic distribution with 30% of pollen dispersed less than 3 m and 90% less than 15 m. Restricted pollen dispersal maintains the strong genetic structuring of the adult populations in succeeding generations. As a consequence of preferential outcrossing, any reduction in effective population size, flowering plant density and/or the abundance and activity of pollinators may impact negatively on population viability through reduced seed set, increased inbreeding and increased correlated paternity.

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References

  • Alexander MP, Ganeshan S (1989) An improved method for in vitro germination of recalcitrant pollen. Biotechnic Histochem 64:225–227

    Article  CAS  Google Scholar 

  • Alford JJ (1995) Two new species of Tetratheca (Tremandraceae), from the Coolgardie and Austin Botanical Districts, Western Australia. Nuytsia 10:143–149

    Google Scholar 

  • Bond WJ (1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Phil Trans R Soc Lond B 344:83–90

    Article  Google Scholar 

  • Buchmann SL, Cane JH (1989) Bees assess pollen returns while sonicating Solanum flowers. Oecologia 81:289–294

    Article  Google Scholar 

  • Butcher PA, Krauss SL (2009) Development of microsatellites from the rare ironstone endemic, Tetratheca paynterae subsp. paynterae and cross species amplification. Mol Ecol Res 9:386–389

    Article  CAS  Google Scholar 

  • Butcher PA, Moran GF, Perkins HD (1998) RFLP diversity in the nuclear genome of Acacia mangium. Heredity 81:205–213

    Article  CAS  Google Scholar 

  • Butcher PA, McNee SA, Krauss SL (2009) Genetic impacts of habitat loss on the rare ironstone endemic, Tetratheca paynterae subsp. paynterae. Conserv Genet 10:1735–1746

    Article  Google Scholar 

  • Butcher R (2007) New taxa of ‘leafless’ Tetratheca (Elaeocarpaceae, formerly Tremandraceae) from Western Australia. Aust Syst Bot 20:139–160

    Article  Google Scholar 

  • Butcher R, Byrne M, Crayn DM (2007) Evidence for convergent evolution among phylogenetically distant rare species of Tetratheca (Elaeocarpaceae, formerly Tremandraceae) from Western Australia. Aust Syst Bot 20:126–138

    Article  CAS  Google Scholar 

  • Crawford TJ (1984) The estimation of neighbourhood parameters for plant populations. Heredity 52:273–283

    Article  Google Scholar 

  • de Nettancourt D (1997) Incompatibility in angiosperms. Sex Plant Reprod 10:185–199

    Article  Google Scholar 

  • Driscoll C (2003) Pollination ecology of Tetratheca juncea (Tremandaceae): finding the pollinators. Cunninghamia 8:133–140

    Google Scholar 

  • Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou P-O, Goodwillie C, Johnston MO, Kelly JK, Moeller DA, Porcher E, Ree RH, Vallejo-Marin M, Winn AA (2009) Plant mating systems in a changing world. TREE 25:35–43

    PubMed  Google Scholar 

  • Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Ann Rev Ecol Syst 24:217–242

    Article  Google Scholar 

  • Gibson N, Coates DJ, Thiele KR (2007) Taxonomic research and the conservation status of flora in the Yilgarn banded iron formation ranges. Nuytsia 17:1–12

    Google Scholar 

  • Gibson N, Yates CJ, Dillon R (2010) Plant communities of the ironstone ranges of South Western Australia: hotspots for plant diversity and mineral deposits. Biodivers Conserv 19:3951–3962

    Article  Google Scholar 

  • Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations and empirical evidence. Annu Rev Ecol Syst 36:47–79

    Article  Google Scholar 

  • Gross CL, Mackay D (1998) Honeybees reduce fitness in the pioneer shrub Melastoma affine (Melastomataceae). Biol Conserv 86:169–178

    Article  Google Scholar 

  • Gross CL, Bartier FV, Mulligan DR (2003) Floral structure, breeding system and fruit set in the threatened sub shrup Tetratheca juncea Smith (Tremandaceae). Ann Bot 92:771–777

    Article  PubMed  CAS  Google Scholar 

  • Harder LD, Barclay RMR (1994) The functional significance of poricidal anthers and buzz pollination: controlled pollen removal from Dodecatheon. Funct Ecol 8:509–517

    Article  Google Scholar 

  • Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322:49–86

    Article  CAS  Google Scholar 

  • Ivey CT, Wyatt R (1999) Family outcrossing rates and neighbourhood floral density in natural populations of swamp milkweed (Asclepias incarnata); potential statistical artifacts. Theor App Genet 98:1063–1071

    Article  Google Scholar 

  • Jain SK (1976) The evolution of inbreeding in plants. Annu Rev Ecol Syst 7:469–495

    Article  Google Scholar 

  • Jarne P, Charlesworth D (1993) The evolution of selfing rate in functionally hermaphrodite plants and animals. Annu Rev Ecol Syst 24:441–466

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • King MJ, Buchmann SL (1996) Sonication dispensing of pollen from Solanum laciniatum flowers. Funct Ecol 10:449–456

    Article  Google Scholar 

  • Knight TM, Steets JA, Vamosi JC et al (2005) Pollen limitation of plant reproduction: pattern and process. Annu Rev Ecol Evol Syst 36:467–497

    Article  Google Scholar 

  • Lascalles DF (2007) Black smokers and density currents: a uniformitarian model for the genesis of banded iron-formations. Ore Geol Rev 32:281–411

    Google Scholar 

  • Lloyd DG (1965) Evolution of self-compatibility and racial differentiation in Leavenworthia (Crucifereae). Contrib Gray Herb Harv Univ 195:3–134

    Google Scholar 

  • Lloyd DG (1992) Self- and cross-fertilization in plants. II. The selection of self-fertilization. Int J Plant Sci 153:370–380

    Article  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  PubMed  CAS  Google Scholar 

  • Mathews ML, Endress PK (2002) Comparative floral structure and systematics in Oxalidales (Oxalidaceae, Connaraceae, Brunelliaceae, Cephalotaceae, Cunoniaceae, Elaeocarpaceae, Tremandraceae). Bot J Linn Soc 140:321–381

    Article  Google Scholar 

  • Mucina L, Wardell-Johnson GW (2011) Landscape age and soil fertility, climatic stability, and fire regime predicability: beyond the OCBIL framework. Plant Soil. doi:10.1007/s11104-011-0734-x

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco callus culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Ritland K (1989) Correlated matings in the partial selfer Mimulus guttatus. Evolution 43:848–859

    Article  Google Scholar 

  • Ritland K (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88:221–228

    Article  PubMed  Google Scholar 

  • Schoen DJ (1982) The breeding system of Gilia archilleifolia: variation in floral characteristics and outcrossing rate. Evolution 36:352–360

    Article  Google Scholar 

  • Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. TREE 22:25–33

    PubMed  Google Scholar 

  • Sharifi MR, Gibson AC, Rundel PW (1997) Surface dust impacts on gas exchange in Mojave Desert shrubs. J Appl Ecol 34:837–846

    Article  Google Scholar 

  • Shaw DV, Kahler AL, Allard RW (1980) A multilocus estimator of mating system parameters in plant populations. Proc Natl Acad Sci USA 78:1298–1302

    Article  Google Scholar 

  • Underwood AJ (1994) On beyond BACI: sampling designs that might reliably detect environmental disturbances. Ecol Appl 4:3–15

    Article  Google Scholar 

  • Uyenoyama MK (1986) Inbreeding and the cost of meiosis: the evolution of selfing in populations practicing biparental inbreeding. Evolution 40:388–404

    Article  Google Scholar 

  • Vaknin Y, Gan-Mor S, Bechar A, Ronen B, Eisikowitch D (2000) The role of electrostatic forces in pollination. Plant Syst Evol 222:133–142

    Article  Google Scholar 

  • Willi Y, Van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Ann Rev Ecol Evol Syst 37:433–458

    Article  Google Scholar 

  • Wyatt R (1986) Ecology and evolution of self-pollination in Arenaria uniflora (Caryophyllaceae). J Ecol 74:403–418

    Article  Google Scholar 

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Acknowledgments

Funding from Portman Iron Ore Pty Ltd and access to unpublished technical reports is gratefully acknowledged. We also acknowledge support provided by Piers Goodman, James Hesford and Rob Howard from Portman Iron Ore Pty Ltd, field assistance provided by Janet Anthony from Kings Park and Botanic Garden (BGPA), Geoff Cockerton, Shapelle McNee and Gemma McLean from Western Botanical, Colin Yates and Rebecca Dillon from the Department of Environment and Conservation and technical advice on pollination provided by Patrick Courtney from BGPA. Constructive comments from two anonymous referees are also acknowledged. Seed was collected under permit No. SW010813 issued under the Western Australian Wildlife Conservation Act 1950.

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Authors and Affiliations

  1. Kings Park and Botanic Garden, Botanic Gardens and Parks Authority, Fraser Avenue, West Perth, WA, 6005, Australia

    P. A. Butcher, D. Bradbury & S. L. Krauss

  2. 14 Bombi Road South, Macmasters Beach, NSW, 2251, Australia

    P. A. Butcher

  3. School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    D. Bradbury & S. L. Krauss

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  1. P. A. Butcher
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  2. D. Bradbury
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  3. S. L. Krauss
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Correspondence to P. A. Butcher.

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Butcher, P.A., Bradbury, D. & Krauss, S.L. Limited pollen-mediated dispersal and partial self-incompatibility in the rare ironstone endemic Tetratheca paynterae subsp. paynterae increase the risks associated with habitat loss. Conserv Genet 12, 1603–1618 (2011). https://doi.org/10.1007/s10592-011-0258-1

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  • DOI: https://doi.org/10.1007/s10592-011-0258-1

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