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Within-carpel and among-carpel competition during seed development, and selection on carpel number, in the apocarpous perennial herb Helleborus foetidus L. (Ranunculaceae)

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Abstract

Apocarpous flowers share opportunities for post-fertilization ovule selection among more functional levels than syncarpous flowers, because the occurrence of a variable number of unfused carpels adds a new source of variation to the likelihood of successful female reproduction. The extent to which post-fertilization events might differ among these unfused carpels may promote variations in the reproductive strategies of plants. We report a study of the variation, within and among carpels and flowers, in seed production and mass in the apocarpous Helleborus foetidus (Ranunculaceae), in relation to the number of carpels per flower. Differences within and among carpels in female reproductive success were affected by carpel number and pollination environment. When analysing whole flowers as functional units we also found that the magnitude of the differences related to carpel number and pollination treatment actually depended on the “distribution” of pollen types within flowers. Thus, variable within-flower pollination environments, more likely to occur in apocarpous than in syncarpous flowers, may affect the strategies of resource allocation for fruit development at different stages of the reproductive process. Regarding seed production, we found that producing more flowers with four carpels was under directional; however, when mean diaspore mass was considered as a measure of fitness, directional selection was found on producing flowers with two and three carpels (the modal carpel number found in wild populations). We discuss ecological and developmental reasons which could explain the observed pattern, and conclude that selection on an optimum carpel number may be very variable across the species range, as the discussed reasons may impose constraints on eventual evolutionary response, thus contributing to the maintenance of the intra-individual variability in carpel number.

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References

  • Acosta FJ, Delgado JA, Lopez F, Serrano JM (1997) Functional features and ontogenetic changes in reproductive allocation and partitioning strategies of plant modules. Pl Ecol 132:71–76

    Article  Google Scholar 

  • Arathi HS, Ganeshaiah KN, Uma Shaanker R, Hedge SG (1999) Seed abortion in Pongamia pinnata (Fabaceae). Am J Bot 86:659–662

    Article  PubMed  Google Scholar 

  • Armbruster WS, Gobeille Rogers D (2004) Does pollen competition reduce the cost of inbreeding? Am J Bot 91:1939–1943

    Article  Google Scholar 

  • Armbruster WS, Debevec EM, Willson MF (2002) Evolution of syncarpy in angiosperms: theoretical and phylogenetic analyses of the effects of carpel fusion on offspring quantity and quality. J Evol Biol 15:657–672

    Article  Google Scholar 

  • Arnold SJ, Wade MJ (1984) On the measurement of natural and sexual selection: theory. Evolution 38:709–719

    Article  Google Scholar 

  • Bañuelos MJ, Obeso JR (2003) Maternal provisioning, sibling rivalry and seed mass variability in the dioecious shrub Rhamnus alpinus. Evol Ecol 17:19–31

    Article  Google Scholar 

  • Bates DM (2005) Fitting linear mixed models in R. R News 5:27–30

    Google Scholar 

  • Bates DM, Maechler M (2009) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-32. http://CRAN.R-project.org/package=lme4

  • Burd M (1998) “Excess” flower production and selective fruit abortion: a model of potential benefits. Ecology 79:2123–2132

    Google Scholar 

  • Canty A, Ripley B (2009) Boot: Bootstrap R (S-Plus) functions. R package version 1.2-41

  • Carr SGM, Carr DJ (1961) The functional significance of syncarpy. Phytomorphology 11:249–256

    Google Scholar 

  • Castellanos MC, Medrano M, Herrera CM (2008) Subindividual variation and genetic versus environmental effects on seed traits in a European Aquilegia. Botany 86:1125–1132

    Article  Google Scholar 

  • Castro J (1999) Seed mass versus seedling performance in Scots pine: a maternally dependent trait. New Phytol 144:153–161

    Article  Google Scholar 

  • Cooke TJ (2006) Do Fibonacci numbers reveal the involvement of geometrical imperatives or biological interactions in phyllotaxis? Bot J Linn Soc 150:3–24

    Article  Google Scholar 

  • Craine JM (2005) Reconciling plant strategy theories of Grime and Tilman. J Ecol 93:1041–1052

    Article  Google Scholar 

  • Davidson AC, Hinkley DV (1997) Bootstrap methods and their applications. Cambridge University Press, Cambridge

    Google Scholar 

  • Ehrlen J (1991) Why do plants produce surplus flowers? A reserve-ovary model. Am Nat 138:918–933

    Article  Google Scholar 

  • Ehrlen J (1993) Ultimate functions of non-fruiting flowers in Lathyrus vernus. Oikos 68: 45–52

    Article  Google Scholar 

  • Endress PK (1982) Syncarpy and alternative modes of scaping disadvantages of apocarpy in primitive angiosperms. Taxon 31:48–52

    Article  Google Scholar 

  • Endress PK (1987) Floral phyllotaxis and floral evolution. Bot Jahrb Syst Pflanzengesch Pflanzengeogr 108:417–438

    Google Scholar 

  • Endress PK, Doyle JA (2007) Floral phyllotaxis in basal angiosperms: development and evolution. Curr Opin Plant Biol 10:52–57

    Article  PubMed  Google Scholar 

  • Fedriani JM, Rey PJ, Garrido JL, Guitián J, Herrera CM, Medrano M, Sánchez-Lafuente AM, Cerdá X (2004) Geographical variation in the potential of mice to constrain an ant-seed dispersal mutualism. Oikos 105:181–191

    Article  Google Scholar 

  • Garrido JL (2003) Semillas y plántulas de Helleborus foetidus L. (Ranunculaceae): variación geográfica, ecología y Evolución. Dissertation, Universidad de Jaén, Jaén, Spain

  • Garrido JL, Rey PJ, Cerdá X, Herrera CM (2002) Geographical variation in diaspore traits of an ant-dispersed plant (Helleborus foetidus): are ant community composition and diaspore traits correlated? J Ecol 90:446–455

    Article  Google Scholar 

  • Garrido JL, Rey PJ, Herrera CM (2005) Fuentes de variación en el tamaño de la semilla de la herbácea perenne Helleborus foetidus L (Ranunculaceae). An J Bot Mad 62:115–125

    Google Scholar 

  • Guitián J, Medrano M, Herrera CM, Sánchez-Lafuente AM (2003) Variation in structural gender in the hermaphrodite Helleborus foetidus (Ranunculaceae): within and among-population patterns. Pl Syst Evol 241:139–151

    Article  Google Scholar 

  • Herrera CM (1991) Dissecting factors responsible for individual variation in plant fecundity. Ecology 72:1448–1463

    Article  Google Scholar 

  • Herrera CM (2000) Flower-to-seedling consequences of different pollination regimes in an insect-pollinated shrub. Ecology 81:15–29

    Article  Google Scholar 

  • Herrera CM (2002) Censusing natural microgametophyte populations: variable spatial mosaics and extreme fine-graininess in winter-flowering Helleborus foetidus L (Ranunculaceae). Am J Bot 89:1570–1578

    Article  Google Scholar 

  • Herrera CM (2005) Post-floral perianth functionality: contribution of persistent sepals to seed development in Helleborus foetidus (Ranunculaceae). Am J Bot 92:1486–1491

    Article  Google Scholar 

  • Herrera CM, Sánchez-Lafuente AM, Medrano M, Guitián J, Cerdá X, Rey PJ (2001) Geographical variation in autonomous self-pollination levels unrelated to pollinator service in Helleborus foetidus (Ranunculaceae). Am J Bot 88:1025–1032

    Article  PubMed  Google Scholar 

  • Herrera CM, Medrano M, Rey PJ, Sanchez-Lafuente AM, Garcia MB, Guitian J, Manzaneda AJ (2002) Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. PNAS 99:16823–16828

    Article  CAS  PubMed  Google Scholar 

  • Hossaert M, Valero M (1988) Effect of ovule position in the pod on patterns of seed formation in two species of Lathyrus (Leguminosae: Papilionoideae). Am J Bot 75:1714–1731

    Article  Google Scholar 

  • Huang SQ (2003) Reproductive success by unusual growth of pollen tubes to ovules. New Phytol 158:232–234

    Article  Google Scholar 

  • Klinkhamer PGL, de Jong TJ (1993) Phenotypic gender in plants: effects of plant size and environment on allocation to seeds in Cynoglossum officinale. Oikos 67:81–86

    Article  Google Scholar 

  • Klinkhamer PGL, Meelis E, de Jong TJ, Weiner J (1992) On the analysis of size-dependent reproductive output in plants. Funct Ecol 6:308–316

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lemon J (2006) Plotrix: a package in the red light district of R. R-News 6:8–12

    Google Scholar 

  • Luzuriaga AL, Escudero A, Pérez-Garcia F (2006) Environmental maternal effects on seed morphology and germination in Sinapis arvensis (Cruciferae). Weed Res 46:163–174

    Article  Google Scholar 

  • Mark S, Olesen JM (1996) Importance of elaiosome size to removal of ant-dispersed seeds. Oecologia 107:95–101

    Article  Google Scholar 

  • Marshall DL, Ellstrand C (1986) Sexual selection in Raphanus sativus: experimental data on non-random fertilization, maternal choice and consequences of multiple paternity. Am Nat 131:739–756

    Article  Google Scholar 

  • Marshall DL, Folsom MW (1991) Mate choice in plants: an anatomical to population perspective. Annu Rev Ecol Syst 22:37–63

    Article  Google Scholar 

  • Mazer SJ, Snow AA, Stanton ML (1986) Fertilization dynamics and parental effects upon fruit development in Raphanus raphanistrum: consequences for seed size variation. Am J Bot 73:500–511

    Article  Google Scholar 

  • Mena-Ali JI, Rocha OJ (2005) Effect of ovule position within the pod on the probability of seed production in Bauhinia ungulata (Fabaceae). Ann Bot 95:449–455

    Article  PubMed  Google Scholar 

  • Mustajarvi K, Siikamaki P, Rytkonen S, Lammi A (2001) Consequences of plant population size and density for plant–pollinator interactions and plant performance. J Ecol 89:80–87

    Article  Google Scholar 

  • Niesenbaum RA, Casper BB (1994) Pollen tube numbers and selective fruit maturation in Lindera benzoin. Am Nat 144:184–191

    Article  Google Scholar 

  • Padien DJ, Lajtha K (1992) Plant spatial pattern and nutrient distribution in pinyon-juniper woodlands along an elevational gradient in northern New-Mexico. Int J Pl Sci 153:425–433

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  • Pinheiro JC, Bates DM, DebRoy S, Sarkar D, R Core team (2009). nlme: linear and nonlinear mixed effects models. R package version 3.1-96

  • Quesada M, Winsor JA, Stephenson AG (1993) Effects of pollen competition on progeny performance in a heterozygous cucurbit. Am Nat 142:694–706

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org

  • Ramírez JM, Rey PJ, Alcántara JM, Sánchez-Lafuente AM (2006) Altitude and woody cover control recruitment of Helleborus foetidus in a Mediterranean mountain area. Ecography 29:375–384

    Article  Google Scholar 

  • Rey PJ, Ramírez JM, Sánchez-Lafuente AM (2006a) Seed- vs. microsite-limited recruitment in a myrmecochorous herb. Plant Ecol 184:213–222

    Article  Google Scholar 

  • Rey PJ, Herrera CM, Guitian J, Cerdá X, Sánchez-Lafuente AM, Medrano M, Garrido JL (2006b) The geographic mosaic of predispersal interactions and selection on Helleborus foetidus (Ranunculaceae). J Evol Biol 19:21–34

    Article  CAS  PubMed  Google Scholar 

  • Rigney LP (1995) Postfertilization causes of differential success of pollen donors in Erythronium grandiflorum (Liliaceae): nonrandom ovule abortion. Am J Bot 82:578–584

    Article  Google Scholar 

  • Rocha OJ, Stephenson AG (1990) Effect of ovule position on seed production, seed weight, and progeny performance in Phaseolus coccineus (Leguminosae). Am J Bot 77:1320–1329

    Article  Google Scholar 

  • Sakai S (2007) A new hypothesis for the evolution of overproduction of ovules: an advantage of selective abortion for females not associated with variation in genetic quality of the resulting seeds. Evolution 61:984–993

    Article  PubMed  Google Scholar 

  • Salopek-Sondi B, Kovac M, Ljubesic N, Magnus V (2000) Fruit initiation in Helleborus niger L. triggers chloroplast formation and photosynthesis in the perianth. J Plant Phys 157:357–364

    CAS  Google Scholar 

  • Sánchez-Lafuente AM, Parra R (2009) Implications of a long-term, pollinator-mediated selection on floral traits in a generalist herb. Ann Bot 104:689–701

    Article  PubMed  Google Scholar 

  • Sánchez-Lafuente AM, Guitian J, Medrano M, Herrera CM, Rey PJ, Cerda X (2005) Plant traits, environmental factors, and pollinator visitation in winter-flowering Helleborus foetidus (Ranunculaceae). Ann Bot 96:845–852

    Article  PubMed  Google Scholar 

  • Shaw RG, Waser NM (1994) Quantitative genetic interpretation of postpollination reproductive traits in plants. Am Nat 143:617–635

    Article  Google Scholar 

  • Snow AA, Spira TP (1996) Pollen-tube competition and male fitness in Hibiscus moscheutos. Evolution 50:1866–1870

    Article  Google Scholar 

  • Susko DJ (2006) Effect of ovule position on patterns of seed maturation and abortion in Robinia pseudoacacia (Fabaceae). Can J Bot 84:1259–1265

    Article  Google Scholar 

  • Susko DJ, Lovett-Doust L (1999) Effects of resource availability, and fruit and ovule position on components of fecundity in Alliaria petiolata (Brassicaceae). New Phytol 144:295–306

    Article  Google Scholar 

  • Susko DJ, Lovett-Doust L (2000) Patterns of seed mass variation and their effects on seedling traits in Alliaria petiolata (Brassicaceae). Am J Bot 87:56–66

    Article  PubMed  Google Scholar 

  • Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16

    Article  Google Scholar 

  • Uma Shaanker R, Ganeshaiah KN, Bawa KS (1988) Parent-offspring conflict, sibling rivalry, and brood-size patterns in plants. Annu Rev Ecol Syst 19:177–205

    Article  Google Scholar 

  • Vaughton G, Ramsey M (1998) Sources and consequences of seed mass variation in Banksia marginata (Proteaceae). J Ecol 86:563–573

    Article  Google Scholar 

  • Vila M, Sardans J (1999) Plant competition in Mediterranean-type vegetation. J Veg Sci 10:281–294

    Article  Google Scholar 

  • Wang XF, Tan YY, Chen JH, Lu YT (2006) Pollen tube reallocation in two preanthesis cleistogamous species, Ranalisma rostratum and Sagittaria guyanensis ssp. lappula (Alismataceae). Aquatic Bot 85:233–240

    Article  Google Scholar 

  • Werner K, Ebel F (1994) Zur Lebensgeschichte der Gattung Helleborus L. (Ranunculaceae). Flora 189:97–130

    Google Scholar 

  • Williams EG, Sage TL, Thien LB (1993) Functional syncarpy by intercarpellary growth of pollen tubes in a primitive apocarpous angiosperm, Illicium floridanum (Illiciaceae). Am J Bot 80:137–142

    Article  Google Scholar 

  • Wise MJ, Cummins JJ (2002) Nonfruiting hermaphroditic flowers as reserve ovaries in Solanum carolinense. Am Mid Nat 148:236–245

    Article  Google Scholar 

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Acknowledgments

The authors thank Francisco Javier Jiménez for laboratory assistance, and three anonymous reviewers for helpful comments that improved an earlier version of this manuscript. This research was conducted without any kind of financial support.

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  1. Departamento de Biología Vegetal y Ecología, Facultad de Biología, Universidad de Sevilla, Avd, Reina Mercedes 9, 41012, Sevilla, Spain

    Raquel Parra & Alfonso M. Sánchez-Lafuente

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  1. Raquel Parra
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  2. Alfonso M. Sánchez-Lafuente
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Correspondence to Alfonso M. Sánchez-Lafuente.

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Parra, R., Sánchez-Lafuente, A.M. Within-carpel and among-carpel competition during seed development, and selection on carpel number, in the apocarpous perennial herb Helleborus foetidus L. (Ranunculaceae). Plant Syst Evol 290, 225–237 (2010). https://doi.org/10.1007/s00606-010-0363-5

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