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Stabilizing selection on nectar concentration in wild Petunia axillaris, as revealed by genetic analysis of pollen dispersal

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Abstract

Most animal-pollinated plants produce nectar as a pollinator reward. Despite the main role that nectar plays in plant-pollinator interactions, the impact of natural variation in nectar traits on realized male fitness is poorly known. Here, we assessed this relation for a wild Petunia axillaris population using paternity-based direct selection gradient analysis, which allowed us also to infer pollen dispersal patterns. Because male fecundity may depend on other traits which could be associated with nectar characteristics (i.e. volume and concentration), we also considered selection on other key reproductive traits. The analysis revealed that P. axillaris was a strict outcrosser, but that successful pollination occurred mainly among neighbours. Individual plants varied greatly in their male fecundity. Nectar concentration, a key feature of nectar that determines its profitability, was subjected to stabilizing selection. Selection through male function also affected corolla area (positive directional selection), corolla tube length (negative directional selection), and floral display size (stabilizing selection), but none of these traits were phenotypically correlated with nectar characteristics. Because nectar concentration affects the ability and foraging efficiency of different flower visitors to feed on nectar, stabilizing selection may reflect either the preference of the most effective pollinators, or antagonistic selection driven by pollinators and non-pollinating nectar consumers.

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References

  • Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42

    Google Scholar 

  • Adams WT, Birkes DS (1991) Estimating mating patterns in forest tree populations. In: Fineschi S, Mavolti ME, Cannata F, Hattemer HH (eds) Biochemical markers in the population genetics of forest trees. Academic Publishing, The Hague, pp 157–172

    Google Scholar 

  • Adler LS, Bronstein JL (2004) Attracting antagonists: Does floral nectar increase leaf herbivory? Ecology 85:1519–1526

    Article  Google Scholar 

  • Ando T, Nomura M, Tsukahara J, Watanabe H, Kokubun H, Tsukamoto T, Hashimoto G, Marchesi E, Kitching IJ (2001) Reproductive isolation in a native population of Petunia sensu Jussieu (Solanaceae). Ann Bot 88:403–413

    Article  Google Scholar 

  • Austerlitz F, Dick CW, Dutech C, Klein EK, Oddou-Muratorio S, Smouse PE, Sork VL (2004) Using genetic markers to estimate the pollen dispersal curve. Mol Ecol 13:937–954

    Article  PubMed  Google Scholar 

  • Austerlitz F, Gleiser G, Teixeira S, Bernasconi G (2012) The effects of inbreeding, genetic dissimilarity and phenotype on male reproductive success in a dioecious plant. Proc R Soc B Biol Sci 279:91–100

    Article  Google Scholar 

  • Bell G (1985) On the function of flowers. P Roy Soc B Biol Sci 224:223–265

    Article  Google Scholar 

  • Bernasconi G (2003) Seed paternity in flowering plants: an evolutionary perspective. Perspect Plant Ecol Evol Syst 6:149–158

    Article  Google Scholar 

  • Bossolini E, Klahre U, Brandenburg A, Reinhardt D, Kuhlemeier C (2011) High resolution linkage maps of the model organism Petunia reveal substantial synteny decay with the related genome of tomato. Genome 54:327–340

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Brandenburg A, Kuhlemeier C, Bshary R (2012) Hawkmoth pollinators decrease seed set of a low-nectar Petunia axillaris line through reduced probing time. Curr Biol 22:1635–1639

    Article  CAS  PubMed  Google Scholar 

  • Burczyk J, Adams WT, Moran GF, Griffin AR (2002) Complex patterns of mating revealed in a Eucalyptus regnans seed orchard using allozyme markers and the neighbourhood model. Mol Ecol 11:2379–2391

    Article  CAS  PubMed  Google Scholar 

  • Burczyk J, Adams WT, Birkes DS, Chybicki IJ (2006) Using genetic markers to directly estimate gene flow and reproductive success parameters in plants on the basis of naturally regenerated seedlings. Genetics 173:363–372

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Campbell DR (1989) Measurements of selection in a hermaphroditic plant: variation in male and female pollination success. Evolution 43:318–334

    Article  Google Scholar 

  • Carlson JE (2007) Male-biased nectar production in a protandrous herb matches predictions of sexual selection theory in plants. Am J Bot 94:674–682

    Article  PubMed  Google Scholar 

  • Conner JK (2002) Genetic mechanisms of floral trait correlations in a natural population. Nature 420:407–410

    Article  CAS  PubMed  Google Scholar 

  • Conner JK (2006) Ecological genetics of floral evolution. In: Harder LD, Barrett SCH (eds) The ecology and evolution of flowers. Oxford University Press, Oxford, pp 260–277

    Google Scholar 

  • Conner JK, Hartl DL (2004) A primer of ecological genetics. Sinauer Associates, Sunderland

    Google Scholar 

  • Conner JK, Rush S, Kercher S, Jennetten P (1996) Measurements of natural selection on floral traits in wild radish (Raphanus raphanistrum). II. Selection through lifetime male and total fitness. Evolution 50:1137–1146

    Article  Google Scholar 

  • Cuartas-Domínguez M, Medel R (2010) Pollinator-mediated selection and experimental manipulation of the flower phenotype in Chloraea bletioides. Funct Ecol 24:1219–1227

    Article  Google Scholar 

  • Dell’Olivo A, Hoballah ME, Gübitz T, Kuhlemeier C (2011) Isolation barriers between Petunia axillaris and Petunia integrifolia (Solanaceae). Evolution 65:1979–1991

    Article  PubMed  Google Scholar 

  • Elle E, Meagher TR (2000) Sex allocation and reproductive success in the andromonoecious perennial Solanum carolinense (Solanaceae). II. Paternity and functional gender. Am Nat 156:622–636

    Article  Google Scholar 

  • Endler J (1986) Natural selection in the wild. Princeton University Press, New Jersey

    Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed Central  Google Scholar 

  • Fénart S, Austerlitz F, Cuguen J, Arnaud J-F (2007) Long distance pollen-mediated gene flow at a landscape level: the weed beet as a case study. Mol Ecol 16:3801–3813

    Article  PubMed  Google Scholar 

  • Galen C, Butchart B (2003) Ants in your plants: effects of nectar-thieves on pollen fertility and seed siring capacity in the alpine wildflower, Polemonium viscosum. Oikos 101:521–528

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Galliot C, Stuurman J, Kuhlemeier C (2006) The genetic dissection of floral pollination syndromes. Curr Opin Plant Biol 9:78–82

    Article  CAS  PubMed  Google Scholar 

  • Gérard PR, Klein EK, Austerlitz F, Fernandez-Manjarres JF, Frascaria-Lacoste N (2006) Assortative mating and differential male mating success in an ash hybrid zone population. BMC Evol Biol 6:96

    Article  PubMed Central  PubMed  Google Scholar 

  • Gerats T, Vandenbussche M (2005) A model system for comparative research: Petunia. Trends Plant Sci 10:251–256

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT (vers. 1.2): A computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Harder LD (1986) Effects of nectar concentration and flower depth on flower handling efficiency of bumble bees. Oecologia 69:309–315

    Article  Google Scholar 

  • Harder LD, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature 373:512–515

    Article  CAS  Google Scholar 

  • Harder LD, Johnson SD (2009) Darwin’s beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol 183:530–545

    Article  PubMed  Google Scholar 

  • Harder LD, Routley MB (2006) Pollen and ovule fates and reproductive performance by flowering plants. In: Harder LD, Barrett SCH (eds) The ecology and evolution of flowers. Oxford University Press, Oxford, pp 61–80

    Google Scholar 

  • Heyneman AJ (1983) Optimal sugar concentrations of floral nectars. Dependence on sugar intake efficiency and foraging costs. Oecologia 60:198–213

    Article  Google Scholar 

  • Hoballah ME, Stuurman J, Turlings TC, Guerin PM, Connetable S, Kuhlemeier C (2005) The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta. Planta 222:141–150

    Article  CAS  PubMed  Google Scholar 

  • Hoballah ME, Gubitz T, Stuurman J, Broger L, Barone M, Mandel T, Dell’Olivo A, Arnold M, Kuhlemeier C (2007) Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19:779–790

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hodges SA (1995) The influence of nectar production on hawkmoth behaviour, self pollination, and seed production in Mirabilis multiflora (Nyctaginaceae). Am J Bot 82:197–204

    Article  Google Scholar 

  • Hodgins KA, Barrett SCH (2008) Natural selection on floral traits through male and female function in wild populations of the heterostylous daffodil Narcissus triandrus. Evolution 62:1751–1763

    Article  PubMed  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253

    Article  Google Scholar 

  • Iwaizumi MG, Takahashi M, Isoda K, Austerlitz F (2013) Consecutive multiple-year analysis of paternal and maternal gene flow and contributions of the gametic heterogeneities to overall genetic composition of Pinus densiflora dispersed seeds. Am J Bot 100:1896–1904

    Article  CAS  PubMed  Google Scholar 

  • Johnson SD, Peter CI, Ågren J (2004) The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio. Proc R Soc B Biol Sci 271:803–809

    Article  Google Scholar 

  • Jones AG, Ardren WR (2003) Methods of parentage analysis in natural populations. Mol Ecol 12:2511–2523

    Article  CAS  PubMed  Google Scholar 

  • Jones AG, Small CM, Paczolt KA, Ratterman NL (2010) A practical guide to methods of parentage analysis. Mol Ecol Resour 10:6–30

    Article  PubMed  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 

  • Karron JD, Mitchell RJ (2012) Effects of floral display size on male and female reproductive success in Mimulus ringens. Ann Bot 109:563–570

    Article  PubMed Central  PubMed  Google Scholar 

  • Kevan PG, Baker HG (1983) Insects as flower visitors and pollinators. Annu Rev Entomol 28:407–453

    Article  Google Scholar 

  • Kim S-H, Yi SV (2007) Understanding relationship between sequence and functional evolution in yeast proteins. Genetica 131:151–156

    Article  CAS  PubMed  Google Scholar 

  • Kim W, Gilet T, Bush JWM (2011) Optimal concentrations in nectar feeding. Proc Natl Acad Sci USA 108:16618–16621

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kingsolver JG, Diamond SE, Siepielski AM, Carlson SM (2012) Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. Evol Ecol 26:1101–1118

    Article  Google Scholar 

  • Klein EK, Desassis N, Oddou-Muratorio S (2008) Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. IV. Whole interindividual variance of male fecundity estimated jointly with the dispersal kernel. Mol Ecol 17:3323–3336

    Article  CAS  PubMed  Google Scholar 

  • Klein EK, Carpentier FH, Oddou-Muratorio S (2011) Estimating the variance of male fecundity from genotypes of progeny arrays: evaluation of the Bayesian forward approach. Methods Ecol Evol 2:349–361

    Article  Google Scholar 

  • Klinkhamer PGL, de Jong TJ, Metz JAJ (1994) Why plants can be too attractive—a discussion of measures to estimate male fitness. J Ecol 82:191–194

    Article  Google Scholar 

  • Kokubun H, Nakano M, Tsukamoto T, Watanabe H, Hashimoto G, Marchesi E, Bullrich L, Basualdo IL, Kao TH, Ando T (2006) Distribution of self-compatible and self-incompatible populations of Petunia axillaris (Solanaceae) outside Uruguay. J Plant Res 119:419–430

    Article  PubMed  Google Scholar 

  • Kulbaba MW, Worley AC (2012) Selection on floral design in Polemonium brandegeei (Polemoniaceae): female and male fitness under hawkmoth pollination. Evolution 66:1344–1359

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Lankinen A, Hellriegel B, Bernasconi G (2006) Sexual conflict over floral receptivity. Evolution 60:2454–2465

    Article  PubMed  Google Scholar 

  • Llaurens V, Castric V, Austerlitz F, Vekemans X (2008) High paternal diversity in the self-incompatible herb Arabidopsis halleri despite clonal reproduction and spatially restricted pollen dispersal. Mol Ecol 17:1577–1588

    Article  CAS  PubMed  Google Scholar 

  • Maloof JE, Inouye DW (2000) Are nectar robbers cheaters or mutualists? Ecology 81:2651–2661

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25:1982–1983

    Article  CAS  PubMed  Google Scholar 

  • Mazer SJ, Delesalle VA, Neal PR (1999) Responses of floral traits to selection on primary sexual investment in Spergularia marina: the battle between the sexes. Evolution 53:717–731

    Article  Google Scholar 

  • Meagher TR (1986) Analysis of paternity within a natural population of Chamaelirium luteum. 1. Identification of most-likely male parents. Am Nat 128:199–215

    Article  Google Scholar 

  • Mitchell RJ (1993) Adaptive significance of Ipomopsis aggregata nectar production: observation and experiment in the field. Evolution 47:25–35

    Article  Google Scholar 

  • Morgan MT, Conner JK (2001) Using genetic markers to directly estimate male selection gradients. Evolution 55:272–281

    Article  CAS  PubMed  Google Scholar 

  • Nielsen R, Mattila DK, Clapham PJ, Palsbøll PJ (2001) Statistical approaches to paternity analysis in natural populations and applications to the north Atlantic humpback whale. Genetics 157:1673–1682

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nilsson LA (1988) The evolution of flowers with deep corolla tubes. Nature 334:147–149

    Article  Google Scholar 

  • Oddou-Muratorio S, Klein EK, Austerlitz F (2005) Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. II. Pollen dispersal and heterogeneity in mating success inferred from parent-offspring analysis. Mol Ecol 14:4441–4452

    Article  CAS  PubMed  Google Scholar 

  • Oddou-Muratorio S, Klein EK, Demesure-Musch B, Austerlitz F (2006) Real time patterns if pollen flow in the wild-service tree, Sorbus torminalis (Rosaceae). III. Mating patterns and the ecological maternal neighbourhood. Am J Bot 93:1650–1659

    Article  PubMed  Google Scholar 

  • Ohashi K, Yahara T (1998) Effects of variation in flower number on pollinator visits in Cirsium purpuratum (Asteraceae). Am J Bot 85:219–224

    Article  CAS  PubMed  Google Scholar 

  • Ohashi K, Yahara T (2001) Behavioural responses of pollinators to variation in floral display size and their influences on the evolution of floral traits. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination. Cambridge University Press, Cambridge, pp 274–296

    Chapter  Google Scholar 

  • Oyama-Okubo N, Ando T, Watanabe N, Marchesi E, Uchida K, Nakayama M (2005) Emission mechanism of floral scent in Petunia axillaris. Biosci Biotechnol Biochem 69:773–777

    Article  CAS  PubMed  Google Scholar 

  • Paccini E, Nepi M (2007) Nectar production and presentation. In: Nicolson SW, Nepi N, Paccini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 167–214

    Chapter  Google Scholar 

  • Signorovitch J, Nielsen R (2002) PATRI—paternity inference using genetic data. Bioinformatics 18:341–342

    Article  CAS  PubMed  Google Scholar 

  • Sink KC (1984) Petunia. Monographs on theoretical and applied genetics, vol 9. Springer, Berlin

    Google Scholar 

  • Smouse PE, Meagher TR (1994) Genetic analysis of male reproductive contributions in Chamaelirium luteum (L.) Gray (Liliaceae). Genetics 136:313–322

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smouse PE, Meagher TR, Kobak CJ (1999) Parentage analysis in Chamaelirium luteum (L.) Gray (Liliaceae): Why do some males have higher reproductive contributions? J Evol Biol 12:1069–1077

    Article  Google Scholar 

  • Snow AA, Lewis PO (1993) Reproductive traits and male fertility in plants: empirical approaches. Annu Rev Ecol Syst 24:331–351

    Google Scholar 

  • Stinchcombe JR, Agrawal AF, Hohenlohe PA, Arnold SJ, Blows MW (2008) Estimating nonlinear selection gradients using quadratic coefficients: Double or nothing? Evolution 62:2435–2440

    Article  PubMed  Google Scholar 

  • Stuurman J, Hoballah ME, Broger L, Moore J, Basten C, Kuhlemeier C (2004) Dissection of floral pollination syndromes in Petunia. Genetics 168:1585–1599

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Teixeira S, Burkhardt A, Bernasconi G (2008) Genetic variation among females affects paternity in a dioecious plant. Oikos 117:1594–1600

    Article  Google Scholar 

  • Tsukamoto T, Ando T, Takahashi K, Omori T, Watanabe H, Kokubun H, Marchesi E, Kao TH (2003) Breakdown of self-incompatibility in a natural population of Petunia axillaris caused by loss of pollen function. Plant Physiol 131:1903–1912

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • van Kleunen M, Burczyk J (2008) Selection on floral traits through male fertility in a natural plant population. Evol Ecol 22:39–54

    Article  Google Scholar 

  • van Kleunen M, Ritland K (2004) Predicting evolution of floral traits associated with mating system in a natural plant population. J Evol Biol 17:1389–1399

    Article  CAS  PubMed  Google Scholar 

  • Venail J, Dell’Olivo A, Kuhlemeier C (2010) Speciation genes in the genus Petunia. Philos Trans R Soc B 365:461–468

    Article  Google Scholar 

  • Wright JW, Meagher TR (2004) Selection on floral characters in natural Spanish populations of Silene latifolia. J Evol Biol 17:382–395

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Marcelo Aizen, Redouan Bshary, Lawrence Harder, Cris Kuhlemeier, three anonymous reviewers and the editors for comments, Dessislava Savova-Bianchi, Eligio Bossolini, José Gabriel Segarra-Moragues, Leonardo Galetto, Portia Lloyd, Mariana Musicante and Denis Pernecker for practical help, and Lawrence Harder for access to the particle counter. This study was supported by the Swiss NSF (Grant No. 3100A0_122004/1 to GB, Grant No. IZK0Z3-125693 to FA and GB) and the Fondation Mercier pour la Science. GG is a member of the Consejo Nacional de Investigaciones Científicas y Técnicas from Argentina. This project benefitted intellectually from collaboration with Cris Kuhlemeier and Redouan Bshary within the framework of the National Centre of Competence in Research (NCCR) Plant Survival (Work package 2.2), a program of the Swiss NSF.

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Correspondence to Gabriela Gleiser.

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Gleiser, G., Internicola, A.I., Austerlitz, F. et al. Stabilizing selection on nectar concentration in wild Petunia axillaris, as revealed by genetic analysis of pollen dispersal. Evol Ecol 28, 869–884 (2014). https://doi.org/10.1007/s10682-014-9714-y

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