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Is variation in flower shape and length among native and non-native populations of Nicotiana glauca a product of pollinator-mediated selection?

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Abstract

Due to drastic changes in pollinators between native and invaded habitats, we might expect that pollinator-mediated selection on floral traits of alien plants differ from that in their native ranges. Here, through geometric morphometric tools and phenotypic selection analyses, we examined whether adaptation in flower shape and length occurred in Nicotiana glauca as a response to pollinator selection in contrasting pollination environments. We assessed populations of this plant species in the native range (South America), where plants depend on hummingbird pollination, and in two invaded areas, one where sunbirds act as pollinators (South Africa), and another where nectar feeding birds are absent and reproduction is entirely by autonomous self-pollination (Mallorca, Spain). Corolla length and shape varied significantly among pollination environments. Non-native sites were less variable and their range of variation fell within the native range of variation. Flower length in native populations and in a South African population matched the bill length of their respective pollinators. In contrast with the straight floral tubes in the native range, both non-native areas had significantly curved tubes. Curvature may improve the fit with the curved bills of sunbirds in South Africa (versus straight beaks of hummingbirds) and may enhance self-pollination in Mallorca, but this similarity between invaded areas may equally be due to drift and a shared colonization route. We found spatial variation in selection acting on corolla length but not on corolla shape. Overall, selection patterns were not consistent with floral trait variation. Although some results are consistent with both drift and selection, our study suggests that population divergence in flower shape and length is more likely the result of long-term diversifying pollinator-driven selection, which is difficult to detect by studying a single selection event.

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References

  • Benítez-Vieyra S, Medina AM, Cocucci AA (2009) Variable selection patterns on the labellum shape of Geoblasta pennicillata, a sexually deceptive orchid. J Evol Biol 22:2345–2362

    Google Scholar 

  • Benítez-Vieyra S, Glinos E, Medina AM et al (2012) Temporal variation in the selection on floral traits in Cyclopogon elatus (Orchidaceae). Evol Ecol 26:1451–1468

    Google Scholar 

  • Bodbyl Roels SA, Kelly JK (2011) Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution 65(9):2541–2552

    PubMed Central  Google Scholar 

  • Bookstein FL (1997) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Brodie E III, Moore A, Janzen F (1995) Visualizing and quantifying natural selection. Trends Ecol Evol 10(8):313–318

    PubMed  Google Scholar 

  • Bromilow C (2001) Problem plants of South Africa. Briza Publications, Pretoria

    Google Scholar 

  • Camargo ID, Nattero J, Careaga SA, Núñez-Farfán J (2017) Flower-level developmental plasticity to nutrient availability in Datura stramonium: implications for the mating system. Ann Bot 120(4):603–615

    PubMed  PubMed Central  Google Scholar 

  • Campbell DR (1996) Evolution of floral traits in a hermaphroditic plant: field measurements of heritabilities and genetic correlations. Evolution 50(4):1442–1453

    PubMed  Google Scholar 

  • Campos EO, Bradshaw HD, Daniel TL (2015) Shape matters: corolla curvature improves nectar discovery in the hawkmoth Manduca sexta. Func Ecol 29:462–468

    CAS  Google Scholar 

  • Carroll AB, Pallardy SG, Galen C (2001) Drought stress, plant water status, and floral trait expression in fireweed, Epilobium angustifolium (Onagraceae). Am J Bot 88(3):438–446

    CAS  PubMed  Google Scholar 

  • Caruso CM, Peterson SB, Ridley CE (2003) Natural selection on floral traits of Lobelia (Lobeliaceae): spatial and temporal variation. Am J Bot 90(9):1333–1340

    PubMed  Google Scholar 

  • Caruso CM, Eisen KE, Martin RA et al (2019) A meta-analysis of the agents of selection on floral traits. Evolution 73(1):4–14

    PubMed  Google Scholar 

  • Charlesworth B, Morgan MT, Charlesworth D (1991) Multilocus models of inbreeding depression with synergistic selection and partial self-fertilization. Genet Res 57(2):177–194

    Google Scholar 

  • Charlesworth D (2003) Effects of inbreeding on the genetic diversity of populations. Philos Trans R Soc B 358(1434):1051–1070

    CAS  Google Scholar 

  • Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10(11):783–796

    CAS  PubMed  Google Scholar 

  • Colautti RI, Eckert CG, Barrett SC (2010) Evolutionary constraints on adaptive evolution during range expansion in an invasive plant. Proc R Soc B Biol Sci 277(1689):1799–1806

    Google Scholar 

  • Colautti RI, Lau JA (2015) Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol Ecol 24(9):1999–2017

    PubMed  Google Scholar 

  • Conner JK, Rush S, Jennetten P (1996) Measurements of natural selection on floral traits in wild radish (Raphanus raphanistrum). I. Selection through lifetime female fitness. Evolution 50(3):1127–1136

    PubMed  Google Scholar 

  • Cronk QCB, Fuller JL (1995) Invasive plants: the threat to natural ecosystems worldwide. Chapman & Hall, London

    Google Scholar 

  • Dixon PM (1993) The bootstrap and the jackknife: describing the precision of ecological indices. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman & Hall, New York, pp 290–318

    Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    CAS  PubMed  Google Scholar 

  • Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton

    Google Scholar 

  • Falconer DS, Mackay TFC (1996) Inbreeding and crossbreeding. In: Introduction to quantitative genetics. Longman Group Ltd, Essex, pp 247–262

    Google Scholar 

  • Faucheux MJ (2013) Sensillum types on the proboscis of the Lepidoptera: a review. Ann Soc Entomol Fr 49(1):73–90

    Google Scholar 

  • Fenster CB, Ritland K (1994) Evidence for natural selection on mating system in Mimulus (Schrophulariaceae). Int J Plant Sci 155:588–596

    Google Scholar 

  • Fishman L, Willis JH (2008) Pollen limitation and natural selection on floral characters in the yellow monkeyflower, Mimulus guttatus. New Phytol 177(3):802–810

    PubMed  Google Scholar 

  • Galen C (1999) Why do flowers vary? Bioscience 49(8):631–640

    Google Scholar 

  • Galetto L, Bernardello L (1993) Nectar secretion pattern and removal effects in three species of Solanaceae. Can J Bot 71:1394–1398

    Google Scholar 

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

    Google Scholar 

  • Gómez JM, Zamora R (2000) Spatial variation in the selective scenarios of Hormathophylla spinosa (Cruciferae). Am Nat 155:657–668

    PubMed  Google Scholar 

  • Gómez JM, Bosch J, Perfectti F et al (2008) Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators. Proc R Soc B Biol Sci 275:2241–2249

    Google Scholar 

  • Gómez JM, Abdelaziz M, Muñoz-Pujares J, Perfectti F (2009) Heritability and genetic correlation of corolla shape and size in Erysimum mediohispanicum. Evolution 63:1820–1831

    PubMed  Google Scholar 

  • Goodspeed TH (1954) The genus Nicotiana. Chronica Botanica Co, Massachusetts

    Google Scholar 

  • Gunz P, Mitteroecker P (2013) Semilandmarks: a method for quantifying curves and surfaces. Hystrix 24(1):103–109

    Google Scholar 

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

    Google Scholar 

  • Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 9:5–15

    Google Scholar 

  • Issaly EA, Sérsic AN, Pauw A et al (2020) Reproductive ecology of the bird-pollinated Nicotiana glauca across native and introduced ranges with contrasting pollination environments. Biol Invasions 22:485–498

    Google Scholar 

  • Jiménez-Lobato V, Martínez‐Borda E, Núñez‐Farfán J et al (2018) Changes in floral biology and inbreeding depression in native and invaded regions of Datura stramonium. Plant Biol 20:214–223

    PubMed  Google Scholar 

  • Kaczorowski RL, Seliger AR, Gaskett AC et al (2012) Corolla shape vs. size in flower choice by a nocturnal hawkmoth pollinator. Funct Ecol 26(3):577–587

    Google Scholar 

  • Kingsolver JG, Pfennig DW (2007) Patterns and power of phenotypic selection in nature. Bioscience 57(7):561–572

    Google Scholar 

  • Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357

    PubMed  Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    PubMed  Google Scholar 

  • Lloyd DG (1987) Allocations to pollen, seeds and pollination mechanisms in self-fertilizing plants. Funct Ecol 1:83–89

    Google Scholar 

  • Lloyd DG, Schoen DJ (1992) Self- and cross-fertilization in plants. I. Functional dimensions. Int J Plant Sci 153(3):358–369

    Google Scholar 

  • Maad J, Alexandersson R (2004) Variable selection in Platanthera bifolia (Orchidaceae): phenotypic selection differed between sex functions in a drought year. J Evol Biol 17(3):642–650

    CAS  PubMed  Google Scholar 

  • Mitchell-Olds T, Shaw R (1987) Regression analysis of natural selection: statistical inference and biological interpretations. Evolution 41(6):1149–1161

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Molina-Montenegro MA, Quiroz CL, Torres-Díaz C et al (2011) Functional differences in response to drought in the invasive Taraxacum officinale from native and introduced alpine habitat ranges. Plant Ecol Divers 4:37–44

    Google Scholar 

  • Moragues E, Rita J (2005) Els vegetals introduïts a les Illes Balears. Govern de les Illes Balears, Palma de Mallorca

    Google Scholar 

  • Murren CJ, Chang CC, Dudash MR (2009) Patterns of selection of two North American native and nonnative populations of monkeyflower (Phrymaceae). New Phytol 183:691–701

    PubMed  Google Scholar 

  • Nattero J, Cocucci AA (2007) Geographical variation in floral traits of the tree tobacco in relation to its hummingbird pollinator fauna. Biol J Linn Soc 90:657–667

    Google Scholar 

  • Nattero J, Sérsic AN, Cocucci AA (2010a) Patterns of contemporary phenotypic selection and flower integration in the hummingbird-pollinated Nicotiana glauca between populations with different flower-pollinator combinations. Oikos 119:852–863

    Google Scholar 

  • Nattero J, Cocucci AA, Medel R (2010b) Pollinator-mediated selection in a specialized pollination system: matches and mismatches across populations. J Evol Biol 23:1957–1968

    CAS  PubMed  Google Scholar 

  • Nattero J, Sérsic AN, Cocucci AA (2011) Geographic variation of floral traits in Nicotiana glauca: relationships with biotic and abiotic factors. Acta Oecol 37:503–511

    Google Scholar 

  • Núñez-Farfán J, Schlichting CD (2005) Natural selection in Potentilla glandulosa revisited. Evol Ecol Res 7(1):105–119

    Google Scholar 

  • Ollerton J, Watts S, Connerty S et al (2012) Pollination ecology of the invasive tree tobacco Nicotiana glauca: comparisons across native and non-native ranges. J Pollinat Ecol 9:85–95

    Google Scholar 

  • Palacio FX, Ordano M, Benitez-Vieyra S (2019) Measuring natural selection on multivariate phenotypic traits: a protocol for verifiable and reproducible analyses of natural selection. Israel J Ecol Evol 1(aop):1–7

    Google Scholar 

  • Paton DC, Collins BG (1989) Consequences of differences in body mass, wing length and leg morphology for nectar-feeding birds. Aust J Ecol 14:269–289

    Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed April 2020

  • Richardson DM, Allsopp N, D'Antonio CM et al (2000) Plant invasions: the role of mutualisms. Biol Rev 75:65–93

    CAS  PubMed  Google Scholar 

  • Rohlf FJ (2010) tpsDig v2. 16. Free software available. http://morphometrics.org/morphmet.html. Accessed May 2017

  • Sakai A, Allendorf F, Holt JS et al (2001) The population biology of invasive species. Ann Rev Ecol Evol Syst 32:305–332

    Google Scholar 

  • Schueller SK (2004) Self-pollination in island and mainland populations of the introduced hummingbird- pollinates. Am J Bot 91:672–681

    PubMed  Google Scholar 

  • Schueller SK (2007) Island–mainland difference in Nicotiana glauca (Solanaceae) corolla length: a product of pollinator mediated selection? Evol Ecol 21:81–98

    Google Scholar 

  • Sheets HD (2017) CoordGen 8. Department of Physics, Canisius College, Buffalo, USA.  http://www3.canisius.edu/~sheets/morphsoft.html. Accessed May 2017

  • Takebayashi N, Wolf DE, Delph LF (2006) Effect of variation in herkogamy on outcrossing within a population of Gilia achilleifolia. Heredity 96(2):159–165

    CAS  PubMed  Google Scholar 

  • Temeles EJ, Koulouris CR, Sander SE et al (2009) Effect of flower shape and size on foraging performance and trade-offs in a tropical hummingbird. Ecology 90:1147–1161

    PubMed  Google Scholar 

  • Traveset A, Richardson DM (2014) Mutualistic interactions and biological invasions. Ann Rev Ecol Evol Syst 45:89–113

    Google Scholar 

  • Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92(1):3–10

    Google Scholar 

  • Westerkamp C (1990) Bird-flowers hovering versus perching exploitation. Bot Acta 103:366–371

    Google Scholar 

  • Westley PA (2011) What invasive species reveal about the rate and form of contemporary phenotypic change in nature. Am Nat 177(4):496–509

    PubMed  Google Scholar 

  • Wood SN (2017) Generalized additive models: an introduction with R. CRC Press/Taylor & Francis Group, Boca Raton London

    Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets HD (2012) Geometric morphometrics for biologists: a primer. Academic Press, Cambridge

    Google Scholar 

  • Zuur A, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Google Scholar 

Download references

Acknowledgements

AAC, ANS, SBV and VP acknowledge the National Research Council of Argentina (CONICET) and the Universidad Nacional de Córdoba (UNC) as researchers. We thank the two anonymous reviewers, and associated editor for their valuable suggestions; we also thank MC Baranzelli, G Bertone, R Castro, A Coetzee, MC Díaz-Vélez, MC Maubecin, X Rotllán Puig, C Tur, and C Vignolo for assistance in the field work, and C Vignolo and F Gilles for assistance in the lab. This work was supported by FONCyT (PICT 2015-3089; PICT-2011-0837) to ANS, the Department of Science and Technology of South Africa (438 75946) and the Spanish Ministry of Economy and Competitiveness (CGL2013-44386-P)

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Authors and Affiliations

  1. Instituto Multidisciplinario de Biología Vegetal (IMBIV-CONICET), Universidad Nacional de Córdoba, Av. Vélez Sársfield 1611, C.C. 495, 5000, Córdoba, Argentina

    Macarena García, Santiago Benítez-Vieyra, Alicia Noemí Sérsic, Andrea Arístides Cocucci, Federico Sazatornil & Valeria Paiaro

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

    Anton Pauw

  3. Instituto Mediterráneo de Estudios Avanzados (CSI, CUIB), C/ Miquel Marquès, 21, 07190, Esporles, Mallorca, Balearic Islands, Spain

    Anna Traveset

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  1. Macarena García
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García, M., Benítez-Vieyra, S., Sérsic, A.N. et al. Is variation in flower shape and length among native and non-native populations of Nicotiana glauca a product of pollinator-mediated selection?. Evol Ecol 34, 893–913 (2020). https://doi.org/10.1007/s10682-020-10082-w

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