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Spatial–temporal patterns of flowering asynchrony and pollinator fidelity in hybridizing species of Narcissus

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Abstract

Speciation requires the evolution of reproductive barriers to achieve isolation between species. In this paper, we examine the role of two major pre-zygotic barriers in reducing the chance of F1 hybrid formation between two pairs of Narcissus species. Field experiments were performed over 5 years in eight natural populations to determine whether flowering phenology and pollinator fidelity could act as reproductive isolation barriers in Narcissus. Our results show that reproductive isolation due to flowering phenology is highly variable and asymmetric. In some populations, pollinator fidelity was so strong that the quantification of reproductive isolation was complete and a strong negative correlation was found between the strength of this barrier and the abundance of hybrids. Nevertheless, the degree of pollinator fidelity was quite variable among populations indicating that reproductive isolation varies geographically but very consistent across years indicating that plant-pollinator interactions are well established. In fact, the finding that hybrid formation between these species occurs only in sites where pollinator fidelity is incomplete suggests that hybrid formation also varies geographically and that divergent evolutionary outcomes may occur in different sympatric populations of Narcissus.

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References

  • Aldridge G, Campbell DR (2007) Variation in pollinator preference between two Ipomopsis contact sites that differ in hybridization rate. Evolution 61:99–110

    Article  PubMed  Google Scholar 

  • Alonso C (2005) Pollination success across an elevation and sex ratio gradient in gynodioecious Daphne laureola. Am J Bot 92:1264–1269

    Article  PubMed  Google Scholar 

  • Bosch M, Waser NM (1999) Effect of local density on pollination and reproduction in Delphinium nuttalianum and Aconitum columbianum (Ranunculaceae). Am J Bot 86:871–879

    Article  PubMed  CAS  Google Scholar 

  • Buerkle CA, Morris RJ, Asmussen MA, Rieseberg LH (2000) The likelihood of homoploid hybrid speciation. Heredity 84:441–451

    Article  PubMed  Google Scholar 

  • Burke JM, Bulger MR, Wesselingh RA, Arnold ML (2000) Frequency and spatial patterning of clonal reproduction in Louisiana Iris hybrid populations. Evolution 54:137–144

    PubMed  CAS  Google Scholar 

  • Carney SE, Gardner KA, Rieseberg LH (2000) Evolutionary changes over the fifty-year history of a hybrid population of sunflowers (Helianthus). Evolution 54:462–474

    PubMed  CAS  Google Scholar 

  • Castro S, Münzbergová Z, Raabová J, Loureiro J (2011) Breeding barriers at a diploid–hexaploid contact zone in Aster amellus. Evo Ecol 25:795–814

    Article  Google Scholar 

  • Chari J, Wilson P (2001) Factors limiting hybridization between Penstemon spectabilis and Penstemon centranthifolius. Can J Bot 79:1439–1448

    Google Scholar 

  • Cozzolino S, D’Emerico S, Widmer A (2004) Evidence for reproductive isolate selection in Mediterranean orchids: karyotype differences compensate for the lack of pollinator specificity. Proc R Soc Lond B Biol Sci 271:259–262

    Article  Google Scholar 

  • Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York

    Google Scholar 

  • Docker MF, Dale A, Heath DD (2003) Erosion of interspecific reproductive barriers resulting from hatchery supplementation of rainbow trout sympatric with cutthroat trout. Mol Ecol 12:3515–3521

    Article  PubMed  CAS  Google Scholar 

  • Egan SP, Funk DJ (2009) Ecologically dependent postmating isolation between sympatric host forms of Neochlamisus bebbianae leaf beetles. Proc Natl Acad Sci USA 106:19426–19431

    Article  PubMed  CAS  Google Scholar 

  • Ellis AG, Johnson SD (1999) Do pollinators determine hybridization patterns in sympatric Satyrium (Orchidaceae) species? Plant Syst Evol 219:137–150

    Article  Google Scholar 

  • Emms SK, Arnold ML (2000) Site-to-site differences in pollinator visitation patterns in a Louisiana Iris hybrid zone. Oikos 91:568–578

    Article  Google Scholar 

  • Fenster CB, Dudash MR (2001) Spatiotemporal variation in the role of hummingbirds as pollinators of Silene virginica (Caryophyllaceae). Ecology 82:844–851

    Google Scholar 

  • Fernandes A (1968) Keys to the identification of native and naturalized taxa of the genus Narcissus L. Daffodil Tulip Year Book 59:37–66

    Google Scholar 

  • Grant V (1949) Pollination systems as isolating mechanisms in angiosperms. Evolution 3:82–97

    Article  PubMed  CAS  Google Scholar 

  • Grant V (1992) Floral isolation between ornithophilous and sphingophilous species of Ipomopsis and Aquilegia. Proc Natl Acad Sci USA 89:11828–11831

    Article  PubMed  CAS  Google Scholar 

  • Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711

    Article  PubMed  CAS  Google Scholar 

  • Hanks GR (2002) Narcissus and daffodil: the genus Narcissus. Taylor and Francis, London

    Google Scholar 

  • Herrera CM, Castellanos MC, Medrano M (2006) Geographical context of floral evolution: towards an improved research programme in floral diversification. In: Harder DH, Barrett SCH (eds) Ecology and evolution of flowers. New York, Oxford, pp 278–294

    Google Scholar 

  • Husband BC, Sabara HA (2003) Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium. New Phytol 161:703–713

    Article  Google Scholar 

  • Jacquemyn H, Brys R, Cammue B, Honnay O, Lievens B (2011) Mycorrhizal associations and reproductive isolation in three closely related Orchis species. Ann Bot 107:347–356

    Article  PubMed  CAS  Google Scholar 

  • Jennersten O, Nilsson SG (1993) Insect flower visitation frequency and seed production in relation to patch size of Viscaria vulgaris (Caryophyllaceae). Oikos 68:283–292

    Article  Google Scholar 

  • Jersáková J, Castro S, Sonk N, Milchreit K, Schödelbauerová I, Tolasch T, Dötterl S (2010) Absence of pollinator-mediated premating barriers in mixed-ploidy populations of Gymnadenia conopsea s.l. (Orchidaceae). Evo Ecol 24:1199–1218

    Article  Google Scholar 

  • Kay KM (2006) Reproductive isolation between two closely related hummingbird-pollinated neotropical gingers. Evolution 60:538–552

    PubMed  Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • Keller B, Wolinska J, Manca M, Spaak P (2008) Spatial, environmental and anthropogenic effects on the taxon composition of hybridizing Daphnia. Phil Trans R Soc Lond B 363:2943–2952

    Article  Google Scholar 

  • Kevan P (2002) Flowers, pollination, and the associated diversity of flies. Biodiversity 3:16–18

    Article  Google Scholar 

  • Lamont BB, He T, Enright NJ, Krauss SL, Miller BP (2003) Anthropogenic disturbance promotes hybridization between Banksia species by altering their biology. J Evol Biol 16:551–557

    Article  PubMed  CAS  Google Scholar 

  • Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH (2008) The strength and genetic basis of reproductive isolating barriers in flowering plants. Phil Trans R Soc Lond B 363:3009–3021

    Article  Google Scholar 

  • Mallet J (2007) Hybrid speciation. Nature 446:279–283

    Article  PubMed  CAS  Google Scholar 

  • Marques I, Rosselló-Graell A, Draper D, Iriondo JM (2007) Pollination patterns limit hybridization between two sympatric species of Narcissus (Amaryllidaceae). Am J Bot 94:1352–1359

    Article  PubMed  Google Scholar 

  • Marques I, Nieto Feliner N, Draper Munt D, Martins-Loução MA, Fuertes Aguilar J (2010) Unraveling cryptic reticulate relationships and the origin of orphan hybrid disjunct populations in Narcissus. Evolution 64:2353–2368

    PubMed  Google Scholar 

  • Marques I, Nieto Feliner N, Martins-Loução MA, Fuertes Aguilar J (2011) Fitness in Narcissus hybrids: low fertility is overcome by early hybrid vigour, absence of exogenous selection and high bulb propagation. J Ecol 99:1508–1519

    Article  Google Scholar 

  • Martin NH, Willis JH (2007) Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 61:68–82

    Article  PubMed  Google Scholar 

  • Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York

    Google Scholar 

  • Meléndez-Ackerman EJ, Campbell DR, Waser NN (1997) Hummingbird behavior and mechanisms of selection on flower color in Ipomopsis. Ecology 78:2532–2541

    Google Scholar 

  • Nosil P, Crespi BJ (2006) Experimental evidence that predation promotes divergence during adaptive radiation. Proc Natl Acad Sci USA 103:9090–9095

    Article  PubMed  CAS  Google Scholar 

  • Ramsey J, Bradshaw HD, Schemske DW (2003) Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:1520–1534

    PubMed  Google Scholar 

  • Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389

    Article  Google Scholar 

  • Rieseberg LH, Blackman BK (2010) Speciation genes in plants. Ann Bot 106:439–455

    Article  PubMed  CAS  Google Scholar 

  • Schwarz D, McPheron BA (2007) When ecological isolation breaks down: sexual isolation is an incomplete barrier to hybridization between Rhagoletis species. Evol Ecol Res 9:829–841

    Google Scholar 

  • Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R et al (2008) Speciation through sensory drive in cichlid fish. Nature 455:620–626

    Article  PubMed  CAS  Google Scholar 

  • Shmida A, Dafni A (1989) Blooming strategies, flower size and advertisement in the “Lily Group” geophytes of Israel. Herbertia 45:111–123

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman, New York

    Google Scholar 

  • Taylor EB, Boughman JW, Groenenboom M, Sniatynski M, Schluter D, Gow JL (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol Ecol 15:343–355

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD (2001) How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system? Oecologia 126:386–394

    Article  Google Scholar 

  • Tiffin P, Olson MO, Moyle LC (2001) Asymmetrical crossing barriers in angiosperms. Proc R Soc Lond B 268:861–867

    Article  CAS  Google Scholar 

  • Turelli M, Moyle LC (2007) Asymmetric postmating isolation: Darwin’s corollary to Haldane’s rule. Genetics 176:1059–1088

    Article  PubMed  Google Scholar 

  • Utelli A-B, Roy BA (2000) Pollinator abundance and behavior on Aconitum lycoctonum (Ranunculaceae): an analysis of the quantity and quality components of pollination. Oikos 89:461–470

    Article  Google Scholar 

  • Vallejo-Marín M, Dorken ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Ann Rev Ecol Syst 41:193–213

    Article  Google Scholar 

  • Whittemore A, Schaal BA (1991) Interspecific gene flow in sympatric oaks. Proc Natl Acad Sci USA 88:2540–2544

    Article  PubMed  CAS  Google Scholar 

  • Wolf DE, Takebayashi N, Rieseberg LR (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank D. Draper, E. Salvado, S. Albano, H. Silva, J. Soler, E. Laguna, P. Pérez, J. Pérez, M.J. Albert for field support, R.G. Albaladejo, M. Alarcón, J. Aldasoro, A. González, J. M. Iriondo, two anonymous referees and M. Vallejo-Marín, Evol. Ecol. Associate Editor, for their useful comments on a previous version of the manuscript, D. Gilson for linguistic assistance. This work has been supported by a PhD-fellowship to I.M. from FCT, Ministério da Ciência e do Ensino Superior, Portugal (SFRH/BD/19053/2004) and a FPVI European-funded Integrated Infrastructure Initiative “SYNTHESYS“(ES-TAF 023-2004).

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  1. Isabel Marques

    Present address: Universidad Técnica Particular de Loja, San Cayetano Alto s/n, CP 11 01 608, Loja, Ecuador

Authors and Affiliations

  1. Museu Nacional de História Natural, Jardim Botânico, Universidade de Lisboa, Rua da Escola Politécnica 58, 1280-102, Lisbon, Portugal

    Isabel Marques & Maria Amélia Martins-Loução

  2. Real Jardín Botánico, CSIC, Plaza de Murillo, 2, 28014, Madrid, Spain

    Isabel Marques, Javier Fuertes Aguilar & Gonzalo Nieto Feliner

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  1. Isabel Marques
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Correspondence to Isabel Marques.

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Marques, I., Aguilar, J.F., Martins-Loução, M.A. et al. Spatial–temporal patterns of flowering asynchrony and pollinator fidelity in hybridizing species of Narcissus . Evol Ecol 26, 1433–1450 (2012). https://doi.org/10.1007/s10682-012-9554-6

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