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Floral divergence in closely related Leucospermum tottum (Proteaceae) varieties pollinated by birds and long-proboscid flies

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Abstract

The Proteaceae are renowned for their floral diversity but surprisingly the role of pollinators in driving evolutionary divergence in this family has been underexplored. Here we focus on recently diverged taxa to gain insight into the processes that generate diversity by testing whether two varieties of Leucospermum tottum might have originated by pollinator mediated adaptive divergence. L. tottum var. tottum has pale salmon-coloured horizontally-oriented flowers, long nectar tubes, and small volumes of concentrated nectar. L. tottum var. glabrum has red and yellow vertically oriented flowers, short nectar tubes, and large volumes of dilute nectar. Despite the morphological divergence, the varieties are indistinguishable using eight molecular markers, indicating a very early stage of differentiation. Consistent with their morphologies, L. tottum var. tottum is pollinated by long-proboscid flies (Philoliche rostrata and Philoliche gulosa), Cape sugarbirds (Promerops cafer), and, to a lesser extent, by Orange-breasted sunbirds (Anthobaphes violacea), whereas, L. tottum var. glabrum is pollinated only by Orange-breasted sunbirds. A. violacea visits both varieties, but makes more frequent contact with pollen presenters when foraging on L. tottum var. glabrum. The exclusion of birds caused a steeper reduction in seed production in L. tottum var. glabrum than in L. tottum var. tottum, consistent with specialization for bird-pollination in this variety. Additionally, L. tottum var. glabrum exhibits autogamy, whereas L. tottum var. tottum does not. Floral divergence between the two L. tottum varieties corresponds with divergence in pollinator use.

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References

  • Aigner PA (2004) Floral specialization without trade-offs: optimal corolla flare in contrasting pollination environments. Ecology 85:2560–2569

    Article  Google Scholar 

  • Anderson B, Alexandersson R, Johnson SD (2010) Evolution and coexistence of pollination ecotypes in an African Gladiolus (Iridaceae). Evolution 64:960–972

    Article  PubMed  Google Scholar 

  • Armbruster WS, Pélabon C, Hansen TF, Mulder CPH (2004) Floral integration and modularity: distinguishing complex adaptations from genetic constraints. In: Pigliucci M, Preston KA (eds) The evolutionary biology of complex phenotypes. Oxford University Press, Oxford, pp 23–49

  • Baker HG (1955) Self-compatibility and establishment after “long-distance” dispersal. Evolution 9:347–368

    Article  Google Scholar 

  • Baker HG (1959) Reproductive methods as factors in speciation in flowering plants. Cold Spring Harb Symp Quant Biol 24:177–191

    Article  CAS  PubMed  Google Scholar 

  • Barker NP, Weston PH, Rutschmann F, Sauquet H (2007) Molecular dating of the ‘Gondwanan’ plant family Proteaceae is only partially congruent with the timing of the break-up of Gondwana. J Biogeogr 34:2012–2027

    Article  Google Scholar 

  • Beardsley PM, Yen A, Olmstead RG (2003) AFLP phylogeny of Mimulus section Erythranthe and the evolution of hummingbird pollination. Evolution 57:1397–1410

    Article  CAS  PubMed  Google Scholar 

  • Biccard A, Midgley JJ (2009) Rodent pollination in Protea nana. S Afr J Bot 75:720–725

    Article  Google Scholar 

  • Bond WJ (1994) Do mutualisms matter—assessing the impact of pollinator and disperser disruption on plant extinction. Philos Trans R Soc B Biol Sci 344:83–90

    Article  Google Scholar 

  • Bradshaw HD, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176–178

    Article  CAS  PubMed  Google Scholar 

  • Castellanos MC, Wilson P, Thomson JD (2003) Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon. Evolution 57:2742–2752

    Article  PubMed  Google Scholar 

  • Chalcoff VR, Aizen MA, Ezcurra C (2012) Erosion of a pollination mutualism along an environmental gradient in a south Andean treelet, Embothrium coccineum (Proteaceae). Oikos 121:471–480

    Article  Google Scholar 

  • Combs JK, Pauw A (2009) Preliminary evidence that the long-proboscid fly, Philoliche gulosa, pollinates Disa karonica and its proposed Batesian model Pelargonium stipulacea. S Afr J Bot 75:757–761

    Article  Google Scholar 

  • Darwin C (1862) On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing. John Murray, London, UK

  • Devoto M, Montaldo NH, Medan D (2006) Mixed hummingbird: long-proboscid fly pollination in “ornithophilous” Emothrium coccineum (Proteaceae) along a rainfall gradient in Patagonia, Argentina. Austral Ecol 31:512–519

    Article  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Faegri K, van der Pijl L (1970) The principles of pollination ecology, 3rd edn. Pergamon Press, Oxford

    Google Scholar 

  • Fenster CB, Martén-Rodríguez S (2007) Reproductive assurance and the evolution of pollination specialization. Int J Plant Sci 168:215–228

    Article  Google Scholar 

  • Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403

    Article  Google Scholar 

  • Fleming PA, Nicolson SW (2002) How important is the relationship between Protea humiflora (Proteaceae) and its non-flying mammal pollinators? Oecologia 132:361–368

    Article  Google Scholar 

  • Friedman J, Barrett SCH (2008) A phylogenetic analysis of the evolution of wind pollination in the angiosperms. Int J Plant Sci 169:49–58

    Article  Google Scholar 

  • Galen C (1989) Measuring pollinator-mediated selection on morphometric floral traits: bumblebees and the alpine sky pilot, Polemonium viscosum. Evolution 43:882–890

    Article  Google Scholar 

  • Geerts S, Pauw A (2009) African sunbirds hover to pollinate and invasive hummingbird pollinated plant. Oikos 118:573–579

    Article  Google Scholar 

  • Goldblatt P, Manning JC (1995) Pollination biology of Lapeirousia subgenus Lapeirousia (Iridaceae) in southern Africa; Floral divergence and adaptation for long-tongued fly pollination. Ann Mo Bot Gard 82:517–534

    Article  Google Scholar 

  • Goldblatt P, Manning JC (2000) The long-proboscid fly pollination system in southern Africa. Ann Mo Bot Gard 87:146–170

    Article  Google Scholar 

  • Gómez JM, Zamora R (1999) Generalization vs. specialization in the pollination system of Hormathophylla spinosa (Cruciferae). Ecology 80:796–805

    Article  Google Scholar 

  • Hargreaves SL, Johnson SD, Nol E (2004) Do floral syndromes predict specialization in plant pollination systems? An experimental test in an “ornithophilous” African Protea. Oecologia 140:295–301

    Article  PubMed  Google Scholar 

  • Herrera CM (1988) Variation in mutualisms: the spatio-temporal mosaic of a pollinator assemblage. Biol J Linn Soc 35:95–125

    Article  Google Scholar 

  • Hodges SA (1997) Floral nectar spurs and diversification. Int J Plant Sci 158:S81–S88

    Article  Google Scholar 

  • Johnson SD (1997) Pollination ecotypes of Satyrium hallackii (Orchidaceae) in South Africa. Bot J Linn Soc 123:225–235

    Google Scholar 

  • Johnson SD (2010) The pollination niche and its role in the diversification and maintenance of the southern African flora. Philos Trans R Soc B Biol Sci 365:499–516

    Article  Google Scholar 

  • Johnson CM, Pauw A (2014) Adaptation for rodent pollination in Leucospermum arenarium (Proteaceae) despite rapid pollen loss during grooming. Ann Bot 113:931–938

    Article  PubMed  Google Scholar 

  • Johnson SD, Steiner KE (1997) Long-tongued fly pollination and evolution of floral spur length in the Disa draconis complex (Orchidaceae). Evolution 51:45–53

    Article  Google Scholar 

  • Johnson SD, Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends Ecol Evol 15:140–143

    Article  PubMed  Google Scholar 

  • Johnson SD, Linder HP, Steiner KE (1998) Phylogeny and radiation of pollination systems in Disa (Orchidaceae). Am J Bot 85:402–411

    Article  CAS  PubMed  Google Scholar 

  • Johnson SD, Newman E, Anderson B (2012) Preliminary observations of insect pollination in Protea punctata (Proteaceae). S Afr J Bot 83:63–67

    Article  Google Scholar 

  • Kalisz S, Vogler DW, Hanley KM (2004) Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430:884–887

    Article  CAS  PubMed  Google Scholar 

  • Lamont B (1985) The comparative reproductive biology of three Leucospermum species (Proteaceae) in relation to fire responses and breeding system. Aust J Bot 33:139–145

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and ClustalX version 2. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Macior LW (1986) Floral resource sharing by bumblebees and hummingbirds in Pedicularis (Scrophulariaceae) pollination. Bull Torrey Bot Club 113:101–109

    Article  Google Scholar 

  • Manning JC (2004) Needles and pins: the exciting discovery of a new pollination system in the ribbon pincushion, Leucospermum tottum. Veld & Flora 90:10–14

  • Manning JC, Goldblatt P (1996) The Prosoeca peringueyi (Diptera: Nemistrinidae) pollination guild in southern Africa: long-tongued flies and their tubular flowers. Ann Mo Bot Gard 83:67–86

    Article  Google Scholar 

  • Manning JC, Goldblatt P (1997) The Moegistorhynchus longirostris (Diptera: Nemestrinidae) pollination guild: Long-tubed flowers and a specialized long-proboscid fly pollination system in southern Africa. Plant Syst Evol 206:51–69

    Article  Google Scholar 

  • Mast AR, Jones EH, Havery SP (2005) An assessment of old and new DNA sequence evidence for the paraphyly of Banksia with respect to Dryandra (Proteaceae). Aust Syst Bot 18:75–88

    Article  CAS  Google Scholar 

  • Moeller DA (2006) Geographic structure of pollinator communities, reproductive assurance, and the evolution of self-pollination. Ecology 87:1510–1522

    Article  PubMed  Google Scholar 

  • Morgan MT, Wilson WG (2005) Self-fertilization and the escape from pollen limitation in variable pollination environments. Evolution 59:1143–1148

    Article  PubMed  Google Scholar 

  • Muchhala N, Caiza A, Vizuete JC, Thomson JD (2008) A generalized pollination system in the tropics: bats, birds and Aphelandra acanthus. Ann Bot 103:1481–1487

    Article  Google Scholar 

  • Newman E, Anderson B, Johnson SD (2012) Flower colour adaptations in a mimetic orchid. Proc R Soc B Biol Sci 279:2309–2313

    Article  Google Scholar 

  • Ollerton J (1996) Reconciling ecological processes with phylogenetic patterns: the apparent paradox of plant-pollinator systems. J Ecol 84:767–769

    Article  Google Scholar 

  • Ollerton J (1998) Sunbird surprise for syndromes. Nature 6695:726–727

    Article  Google Scholar 

  • Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56:717–728

    Article  Google Scholar 

  • Olsson K, Ågren J (2002) Latitudinal population differentiation in phenology, life history and flowering phenology in the perennial herb Lythrum salicaria. J Evol Biol 15:983–996

    Article  Google Scholar 

  • Pauw A (2013) Can pollination niches facilitate plant coexistence? Trends Ecol Evol 28:30–37

    Article  PubMed  Google Scholar 

  • Pauw A, Softberg J, Waterman RJ (2009) Flies and flowers in Darwin’s race. Evolution 63:268–279

    Article  PubMed  Google Scholar 

  • Pérez F, Arroyo MTK, Medel R, Hershkovitz MA (2006) Ancestral reconstruction of flower morphology and pollination systems in Schizanthus (Solanaceae). Am J Bot 93:1029–1038

    Article  PubMed  Google Scholar 

  • Pérez F, Arroyo MTK, Armesto JJ (2009) Evolution of autonomous selfing accompanies increased specialization in the pollination system of Schizanthus (Solanaceae). Am J Bot 96:1168–1176

    Article  PubMed  Google Scholar 

  • Pérez-Barrales R, Arroyo J, Armbruster WS (2007) Differences in pollinator faunas may generate differences in floral morphology and integration in Narcissus papyraceus (Alarcissiopapyraceris). Oikos 116:1904–1918

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Robertson JL, Wyatt R (1990) Evidence for pollination ecotypes in the yellow-fringed orchid, Platanthera ciliaris. Evolution 44:121–133

    Article  Google Scholar 

  • Rourke JP (1971) Taxonomic studies on Leucospermum. Journal of South African Botany Supplementary Volume No. 8. Trustees of the National Botanical Gardens of South Africa, Kirstenbosch, South Africa

  • Rymer PD, Manning JC, Goldblatt P, Powell MP, Savolainen V (2010) Evidence of recent and continuous speciation in a biodiversity hotspot: a population genetic approach in southern African gladioli (Gladiolus; Iridaceae). Mol Ecol 19:4765–4782

    Article  PubMed  Google Scholar 

  • Sahley CT (1996) Bat and hummingbird pollination of an autotetraploid columnar cactus, Weberbauerocereus weberbaueri (Cactaceae). Am J Bot 83:1329–1336

    Article  Google Scholar 

  • Sauquet H, Western PH, Anderson CL, Barker NP, Cantrill DJ, Mast R, Savolainen V (2009) Contrasted patterns of hyperdiversification in Mediterranean hotspots. Proc Natl Acad Sci USA 106:221–225

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schemske DW, Horvitz CC (1989) Temporal variation in selection on floral character. Evolution 43:461–465

    Article  Google Scholar 

  • Servedio MR, Van Doorn GS, Kopp M, Frame AM, Nosil P (2011) Magic traits in speciation: ‘magic’ but not rare? Trends Ecol Evol 26:389–397

    Article  PubMed  Google Scholar 

  • Stebbins G (1970) Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annu Rev Ecol Syst 1:307–326

    Article  Google Scholar 

  • Steenhuisen SL, Johnson SD (2011) The influence of pollinators and seed predation on seed production in dwarf grassland Protea “sugarbushes” (Proteaceae). S Afr J Bot 79:77–83

    Article  Google Scholar 

  • Steenhuisen SL, Van der Bank H, Johnson SD (2012) The relative contributions of insect and bird pollinators to outcrossing in an African Protea (Proteaceae). Am J Bot 99:1104–1111

    Article  CAS  PubMed  Google Scholar 

  • Steiner KE (1998) The evolution of beetle pollination in a South African orchid. Am J Bot 85:1180–1193

    Article  CAS  PubMed  Google Scholar 

  • Turesson G (1922) The genotypical response of the plant species to the habitat. Hereditas 3:211–350

    Article  Google Scholar 

  • Ushimaru A, Hyodo F (2005) Why do bilaterally symmetrical flowers orient vertically? Flower orientation influences pollinator landing behaviour. Evol Ecol Res 7:151–160

    Google Scholar 

  • Ushimaru A, Dohzono I, Takami Y, Hyodo F (2009) Flower orientation enhances pollen transfer in bilaterally symmetrical flowers. Oecologia 160:667–674

    Article  PubMed  Google Scholar 

  • van der Niet T, Pirie MD, Shuttleworth A, Johnson SD, Midgley JJ (2014) Do pollinator distributions underlie the evolution of pollination ecotypes in the Cape shrub Erica plukenetii?. Ann Bot 113:301–315

    Article  PubMed  Google Scholar 

  • Waser NM (1998) Pollination, angiosperm speciation, and the nature of species boundaries. Oikos 82:198–201

    Article  Google Scholar 

  • Waterman RJ, Bidartondo MI, Softberg J, Combs JK, Gebauer G, Savolainen V, Barraclough TG, Pauw A (2011) The effects of above- and belowground mutualisms on orchid speciation and coexistence. Am Nat 177:E54–E68

    Article  PubMed  Google Scholar 

  • Whittall JB, Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 477:706–709

    Article  Google Scholar 

  • Wiens D, Rourke JP (1978) Rodent pollination in South African Protea spp. Nature 276:71–73

    Article  Google Scholar 

  • Zang F, Hui C, Pauw A (2013) Adaptive divergence in Darwin’s race: how coevolution can generate trait diversity in a pollination system. Evolution 67:548–560

    Article  Google Scholar 

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Acknowledgments

We thank Clive Kerr, The Mountain Club of South Africa, and Cape Nature for allowing access to the sites involved in this study, and Dr. Sim Lin Lim for assisting in assembling DNA sequence dataset and Marinus de Jager for help with the observational data. Additionally we thank Stellenbosch University for funding as well as Kari Segraves and Timo van der Neit for recommendations on a prior draft which improved this study. This study was partially supported by the Australian Research Council (DP120103389).

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  1. Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa

    Christopher Michael Johnson & Anton Pauw

  2. Department of Environment and Agriculture, Curtin University, PO Box U1987, Perth, WA, 6845, Australia

    Tianhua He

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  1. Christopher Michael Johnson
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Correspondence to Anton Pauw.

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Johnson, C.M., He, T. & Pauw, A. Floral divergence in closely related Leucospermum tottum (Proteaceae) varieties pollinated by birds and long-proboscid flies. Evol Ecol 28, 849–868 (2014). https://doi.org/10.1007/s10682-014-9712-0

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