Impact of capitulum structure on reproductive success in the declining species Centaurea cyanus (Asteraceae): small to self and big to flirt?
DOI:
https://doi.org/10.26786/1920-7603(2012)7Abstract
Attracting pollinators and achieving successful reproduction is essential to flowering plant species, which evolved different strategies to cope with unpredictable pollination service. The ability of selfing is most widespread and represents a reproductive insurance under varying conditions. In this study, we investigated reproductive success in Centaurea cyanus, a self-incompatible declining Asteraceae species. We measured seed set under outcrossing and autonomous selfing and assessed the impact of capitulum structure (i.e., the number of disc florets) on reproductive success. We report that the incompatibility system is either flexible or evolving a breakdown in this species, since autonomous selfing often resulted in production of few seeds. We also show that capitulum structure has a strong impact on reproduction, with smaller inflorescences presenting a better ability to self than larger ones, while larger inflorescences performed better than smaller ones when cross-pollinated. Variable capitulum structure in this Asteraceae species may therefore represent a reproductive strategy to achieve efficient reproduction under diverse pollination environments. Our results also suggest that this declining species might be disrupting its auto-incompatibility system in response to reduced habitats and declining population sizes.
References
Ågren J (1996) Population size, pollinator limitation, and seed set in the self- incompatible herb Lythrum salicaria. Ecology 77:1779-1790. DOI: https://doi.org/10.2307/2265783
Angiosperm Phylogeny Group (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141:399-436. DOI: https://doi.org/10.1046/j.1095-8339.2003.t01-1-00158.x
Ashman T-L, Penet L (2007) Direct and indirect effects of a sex-biased antagonist on male and female fertility: Consequences for reproductive trait evolution in a gender-dimorphic plant. The American Naturalist 169:595-608. DOI: https://doi.org/10.1086/513150
Biesmeijer JC, Sorensen PB, Carvalheiro LG (2011) How pollination ecology research can help answer important questions. Journal of Pollination Ecology 4:68-73. DOI: https://doi.org/10.26786/1920-7603(2011)10
Boršic I, Susanna A, Bancheva S, Garcia-Jacas N (2011) Centaurea sect. Cyanus : nuclear phylogeny, biogeography, and life-form evolution. International Journal of Plant Sciences 172:238-249. DOI: https://doi.org/10.1086/657645
Busch JW, Delph LF (2011) The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Annals of Botany doi:10.1093/aob/mcr219. DOI: https://doi.org/10.1093/aob/mcr219
Busch JW, Joly S, Schoen DJ (2010) Does mate limitation in self-incompatible species promote the evolution of selfing? The case of Leavenworthia alabamica. Evolution 64:1657-1670. DOI: https://doi.org/10.1111/j.1558-5646.2009.00925.x
Busch JW, Schoen DJ (2008) The evolution of self-incompatibility when mates are limiting. Trends in Plant Science 13:128-136. DOI: https://doi.org/10.1016/j.tplants.2008.01.002
Busch JW, Urban L (2011) Insights gained from 50 years of studying the evolution of self-compatibility in Leavenworthia (Brassicaceae). Evolutionary Biology 38:15-27. DOI: https://doi.org/10.1007/s11692-010-9104-5
Carreck NL, Williams IH (2002) Food for insect pollinators on farmland: insect visits to flowers of annual seed mixtures. Journal of Insect Conservation 6:13-23. DOI: https://doi.org/10.1023/A:1015764925536
Charlesworth, D (1985) Distribution of dioecy and self-incompatibility in angiosperms. Pp 237-268 in JJ Greenwood and M Slatkin, eds. Evolution –essays in honor of John Maynard Smith. Harvard University Press, Cambridge, Massachusetts.
Collin CL, Penet L, Shykoff JA (2009) Early inbreeding depression in the sexually polymorphic plant Dianthus sylvestris (Caryophyllaceae): effects of selfing and biparental inbreeding among sex morphs. American Journal of Botany 96:2279-2287. DOI: https://doi.org/10.3732/ajb.0900073
Dai C, Galloway LF (2011) Do dichogamy and herkogamy reduce sexual interference in a self-incompatible species? Functional Ecology 25:271-278. DOI: https://doi.org/10.1111/j.1365-2435.2010.01795.x
Darwin CR (1876) The effects of cross- and self-fertilisation in the vegetable kingdom. Murray, London.
Elam DR, Ridley CE, Goodell K, Ellstrand NC (2007) Population size and relatedness affect fitness of a self-incompatible invasive plant. Proceedings of the National Academy of Sciences of the United States of America 104:549-552. DOI: https://doi.org/10.1073/pnas.0607306104
Fenner M, Cresswell JE, Hurley RA, Baldwin T (2002) Relationship between capitulum size and pre-dispersal seed predation by insect larvae in common Asteraceae. Oecologia 130:72-77. DOI: https://doi.org/10.1007/s004420100773
Fenster CB, Marten-Rodriguez S (2007) Reproductive assurance and the evolution of pollination specialization. International Journal of Plant Sciences 168:215-228. DOI: https://doi.org/10.1086/509647
Fontaine C, Collin CL, Dajoz I (2008) Generalist foraging of pollinators: diet expansion at high density. Journal of Ecology 96:1002-1010. DOI: https://doi.org/10.1111/j.1365-2745.2008.01405.x
Freeman DC, Doust JL, ElKeblawy A, Miglia KJ, McArthur ED (1997) Sexual specialization and inbreeding avoidance in the evolution of dioecy. Botanical Review 63:65-92. DOI: https://doi.org/10.1007/BF02857918
Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: Occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology Evolution and Systematics 36:47-79. DOI: https://doi.org/10.1146/annurev.ecolsys.36.091704.175539
Helenurm K, Schaal BA (1996) Genetic load, nutrient limitation, and seed production in Lupinus texensis (Fabaceae). American Journal of Botany 83:1585-1595. DOI: https://doi.org/10.1002/j.1537-2197.1996.tb12817.x
Hermann K, Kuhlemeier C (2011) The genetic architecture of natural variation in flower morphology. Current Opinion in Plant Biology 14:60-65. DOI: https://doi.org/10.1016/j.pbi.2010.09.012
Igic B, Lande R, Kohn JR (2008) Loss of self-incompatibility and its evolutionary consequences. International Journal of Plant Sciences 169:93-104. DOI: https://doi.org/10.1086/523362
Ivey CT, Carr DE (2005) Effects of herbivory and inbreeding on the pollinators and mating system of Mimulus guttatus (Phrymaceae). American Journal of Botany 92:1641-1649. DOI: https://doi.org/10.3732/ajb.92.10.1641
Jursik M, Holec J, Andr J (2009) Biology and control of another important weeds of the Czech Republic: Cornflower (Centaurea cyanus L.). Listy Cukrovarnicke A Reparske 125:90-93.
Kameyama Y, Kudo G (2009) Flowering phenology influences seed production and outcrossing rate in populations of an alpine snowbed shrub, Phyllodoce aleutica : effects of pollinators and self-incompatibility. Annals of Botany 103:1385-1394. DOI: https://doi.org/10.1093/aob/mcp037
Klinkhamer PGL, de Jong TJ, de Bruyn G-J (1989) Plant size and pollinator visitation in Cynoglossum officinale. Oikos 54:201-204. DOI: https://doi.org/10.2307/3565267
Leducq JB, Gosset CC, Poiret M, Hendoux F, Vekemans X, Billiard S (2010) An experimental study of the S-Allee effect in the self-incompatible plant Biscutella neustriaca. Conservation Genetics 11:497-508. DOI: https://doi.org/10.1007/s10592-010-0055-2
Levin DA (1996) The evolutionary significance of pseudo-self-fertility. American Naturalist 148:321-332. DOI: https://doi.org/10.1086/285927
Mayer C et al. (2011) Pollination ecology in the 21st Century: Key questions for future research. Journal of Pollination Ecology 3:8-23. DOI: https://doi.org/10.26786/1920-7603(2011)1
Mena-Ali JI, Stephenson AG (2007) Segregation analyses of partial self-incompatibility in self and cross progeny of Solanum carolinense reveal a leaky S-allele. Genetics 177:501-510. DOI: https://doi.org/10.1534/genetics.107.073775
Muth NZ, Pigliucci M (2007) Implementation of a novel framework for assessing species plasticity in biological invasions: responses of Centaurea and Crepis to phosphorus and water availability. Journal of Ecology 95:1001–1013. DOI: https://doi.org/10.1111/j.1365-2745.2007.01268.x
Narbona E, Ortiz PL, Montserrat A (2011) Linking self-incompatibility, dichogamy, and flowering synchrony in two Euphorbia species: alternative mechanisms for avoiding self-fertilization? PLoS ONE 6:e20668 EP. DOI: https://doi.org/10.1371/journal.pone.0020668
Navascués M, Stoeckel S, Mariette S (2010) Genetic diversity and fitness in small populations of partially asexual, self-incompatible plants. Heredity 104:482-492. DOI: https://doi.org/10.1038/hdy.2009.159
Nienhuis CM, Stout JC (2009) Effectiveness of native bumblebees as pollinators of the alien invasive plant Impatiens glandulifera (Balsaminaceae) in Ireland. Journal of Pollination Ecology 1:1-11. DOI: https://doi.org/10.26786/(2009)
Nishihiro J, Washitani I (2011) Post-pollination process in a partially self-compatible distylous plant, Primula sieboldii (Primulaceae). Plant Species Biology 26:213-220. DOI: https://doi.org/10.1111/j.1442-1984.2011.00318.x
Ostevik KL, Manson JS, Thomson JD (2010) Pollination potential of male bumble bees (Bombus impatiens ): Movement patterns and pollen-transfer efficiency. Journal of Pollination Ecology 2:21-26. DOI: https://doi.org/10.26786/1920-7603(2010)3
Pausic I, Skornik S, Culiberg M, Kaligaric M (2010) Weed diversity in cottage building material used in 19th century: Past and present of the plant occurence. Polish Journal of Ecology 58:577-583.
Penet L, Collin CL, Ashman T-L (2009) Florivory increases selfing: an experimental study in the wild strawberry, Fragaria virginiana. Plant Biology 11:38-45. DOI: https://doi.org/10.1111/j.1438-8677.2008.00141.x
Potts SG, Biesmeijer JC, Bommarco R, Felicioli A, Fischer M, Jokinen P, Kleijn D, Klein A-M, Kunin WE, Neumann P, Penev LD, Petanidou T, Rasmont P, Roberts SPM, Smith HG, Sørensen PB, Steffan-Dewenter I, Vaissière BE, Vilà M, Vujić A, Woyciechowski M, Zobel M, Settele J, Schweiger O (2011) Developing European conservation and mitigation tools for pollination services: approaches of the STEP (Status and Trends of European Pollinators) project. Journal of Apicultural Research 50:152-164. DOI: https://doi.org/10.3896/IBRA.1.50.2.07
Powell KI, Krakos KN, Knight TM (2011) Comparing the reproductive success and pollination biology of an invasive plant to its rare and common native congeners: a case study in the genus Cirsium (Asteraceae). Biological Invasions 13:905-917. DOI: https://doi.org/10.1007/s10530-010-9878-5
Reinartz JA, Les DH (1994) Bottleneck-induced dissolution of self-incompatibility and breeding system consequences in Aster furcatus (Asteraceae). American Journal of Botany 81:446-455. DOI: https://doi.org/10.1002/j.1537-2197.1994.tb15469.x
Sander J, Wardell-Johnson G (2011) Fine-scale patterns of species and phylogenetic turnover in a global biodiversity hotspot: Implications for climate change vulnerability. Journal of Vegetation Science 22:766-780. DOI: https://doi.org/10.1111/j.1654-1103.2011.01293.x
Schweiger O, Biesmeijer JC, Bommarco R, Hickler T, Hulme PE, Klotz S, Kühn I, Moora M, Nielsen A, Ohlemüller R, Petanidou T, Potts SG, Pyšek P, Stout JC, Sykes MT, Tscheulin T, Vilà M, Walther G-R, Westphal C, Winter M, Zobel M, Settele J (2010) Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biological Reviews 85:777-795. DOI: https://doi.org/10.1111/j.1469-185X.2010.00125.x
Stilma ESC, Keesman KJ, van derWerf W (2009) Recruitment and attrition of associated plants under a shading crop canopy: Model selection and calibration. Ecological Modelling 220:1113–1125. DOI: https://doi.org/10.1016/j.ecolmodel.2009.01.015
Sutcliffe OL, Kay QON (2000) Changes in the arable flora of central southern England since the 1960s. Biological Conservation 93:1-8. DOI: https://doi.org/10.1016/S0006-3207(99)00119-6
R Development Core Team (2011) R: a language and environment for statistical computing. In. R Foundation for Statistical Computing, Vienna, Austria.
Rösch M (1998) The history of crops and crop weeds in southwestern Germany from the Neolithic period to modern times, as shown by archaeobotanical evidence. Vegetation History and Archaeobotany 7:109-125. DOI: https://doi.org/10.1007/BF01373928
Ulber L, Steinmann HH, Klimek S (2010) Using selective herbicides to manage beneficial and rare weed species in winter wheat. Journal of Plant Diseases and Protection 117:233-239. DOI: https://doi.org/10.1007/BF03356366
Uyenoyama MK (1986) Inbreeding and the cost of meiosis: The evolution of selfing in populations practicing biparental inbreeding. Evolution 40:388-404. DOI: https://doi.org/10.1111/j.1558-5646.1986.tb00479.x
Wassmuth BE, Stoll P, Tscharntke T, Thies C (2009) Spatial aggregation facilitates coexistence and diversity of wild plant species in field margins. Perspectives in Plant Ecology, Evolution and Systematics 11:127–135 DOI: https://doi.org/10.1016/j.ppees.2009.02.001
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2012 Laurent Penet, Benoit Marion, Anne Bonis

This work is licensed under a Creative Commons Attribution 4.0 International License.



