Abstract
Pollinator-mediated selection might lead to among-trait differences in the degree and pattern of floral integration and intra-flower variation. To examine the patterns of intra-flower variation in floral traits, including nectar volume, we performed a field study using the zygomorphic flowers of Aconitum japonicum ssp. subcuneatum. We investigated (1) correlations between the sizes of the left and right sepals and petals, (2) variation in floral traits among plants, within plants and within flowers, (3) effects of sexual phases on floral integration variation in floral and nectar traits, and (4) the effect of size and intra-flower variation in traits of the left and right sepals and petals on pollen removal by pollinators. Lateral sepal area, but not lower sepal area, was highly correlated between the left and right sepals. Floral traits were more integrated during the male phase than during the female phase. Nectar standing crop in male-phase flowers correlated with helmet height and lateral and lower sepal area, but in female-phase flowers it only correlated with spur length. While intra-flower variance in lateral sepal area accounted for approximately 10% of the overall variance in these traits, the variance in lower sepal area accounted for 70% of the overall variance. Lateral sepal area had a negative effect on the number of pollen grains remaining after pollinator visits. Low variance in lateral sepals within flowers and measurements of pollen removal suggest that lateral sepals play a more important role in pollen export than the other traits. Left and right sepals may be the targets of selection for symmetry in zygomorphic flowers.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Armbruster WS, Schwaegerle KE (1996) Causes of covariation of phenotypic traits among populations. J Evol Biol 9:261–276. https://doi.org/10.1046/j.1420-9101.1996.9030261.x
Armbruster WS, Di Stilio VS, Tuxill JD, Flores TC, Velásquez Runk JL (1999) Covariance and decoupling of floral and vegetative traits in nine neotropical plants: a re-evaluation of Berg’s correlation-pleiades concept. Am J Bot 86:39–55. https://doi.org/10.2307/2656953
Bartkowska MP, Johnston MO (2015) Pollen limitation and its influence on natural selection through seed set. Evolut Biol 28:2097–2105. https://doi.org/10.1111/jeb.12741
Bell G (1985) On the function of flowers. Proc R Soc London Ser B Biol Sci 224:223–265
Berg RL (1960) The ecological significance of correlation pleiades. Evolution (N Y) 14:171–180
Biernaskie JM, Cartar RV (2004) Variation in rate of nectar production depends on floral display size : a pollinator manipulation hypothesis. Funct Ecol 18:125–129
Bissell EK, Diggle PK (2008) Floral morphology in Nicotiana : architectural and temporal effects on phenotypic integration. Int J Plant Sci 169:225–240. https://doi.org/10.1086/523875
Boberg E, Alexandersson R, Jonsson M, Maad J, Ågren J, Nilsson LA (2014) Pollinator shifts and the evolution of spur length in the moth-pollinated orchid Platanthera bifolia. Ann Bot 113:267–275. https://doi.org/10.1093/aob/mct217
Conner JK (2002) Genetic mechanisms of floral trait correlations in a natural population. Nature 420:407–410. https://doi.org/10.1038/nature01028.1
Cuartas-Domínguez M, Medel R (2010) Pollinator-mediated selection and experimental manipulation of the flower phenotype in Chloraea bletioides. Funct Ecol 24:1219–1227. https://doi.org/10.1111/j.1365-2435.2010.01737.x
Darwin CR (1862) On the various contrivances by which British and foreign orchids are fertilised by insects. Murray, London
Diggle PK (2014) Modularity and intra-floral integration in metameric organisms: plants are more than the sum of their parts. Philos Trans R Soc B Biol Sci 369:20130253. https://doi.org/10.1098/rstb.2013.0253
Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, Mcclean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography (Cop) 36:027–046. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Fægri K, Van der Pijl L (1966) Principles of pollination biology. Pergamon Press, Oxford
Fenster CB, Cheely G, Dudash MR, Reynolds RJ (2006) Nectar reward and advertisement in hummingbird. Am J Bot 93:1800
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347
Fukuda Y, Suzuki K, Murata J (2001) The function of each sepal in pollinator behavior and effective pollination in Aconitum japonicum var. montanum. Plant Species Biol 16:151–157. https://doi.org/10.1046/j.1442-1984.2001.00059.x
Gong YB, Huang SQ (2009) Floral symmetry: Pollinator-mediated stabilizing selection on flower size in bilateral species. Proc R Soc B 276:4013–4020. https://doi.org/10.1098/rspb.2009.1254
Heiberger RM (2018) Statistical analysis and data display: Heiberger and Holland. R Packag version, pp 31–35
Herrera CM (2001) Deconstructing a floral phenotype: do pollinators select for Corolla integration in Lavandula latifolia? J Evol Biol 14:574–584. https://doi.org/10.1046/j.1420-9101.2001.00314.x
Herrera CM, Cerda X, Garcia MB, Guitian J, Medrano M, Rey PJ, Sanchez-Lafuente AM (2002) Floral integration, phenotypic covariance structure and pollination variation in bumblebee-pollinated Helleborus foetidus. J Evol Biol 15:108–121
Heywood JS, Michalski JS, McCann BK, Russo AD, Andres KJ, Hall AR, Middleton TC (2017) Genetic and environmental integration of the hawkmoth pollination syndrome in Ruellia humilis (Acanthaceae). Ann Bot 119:1143–1155. https://doi.org/10.1093/aob/mcx003
Hiraga T, Sakai S (2007) The effects of inflorescence size and flower position on biomass and temporal sex allocation in Lobelia sessiliflora. Plant Ecol 188:205–214. https://doi.org/10.1007/s11258-006-9157-9
Hirabayashi Y, Ishii HS, Kudo G (2006) Significance of nectar distribution for bumblebee behaviour within inflorescences, with reference to inflorescence architecture and display size. Écoscience 13:351–359
Inoue K (1986) Experimental studies on male and female reproductive success: effects of variation in spur length and pollinator activity on Platanthera mandarinorum ssp. hachijoensis (Orchidaceae). Plant Species Biol 1:207–215. https://doi.org/10.1111/j.1442-1984.1986.tb00028.x
Ishii HS, Morinaga SI (2005) Intra- and inter-plant level correlations among floral traits in Iris gracilipes (Iridaceae). Evol Ecol 19:435–448. https://doi.org/10.1007/s10682-005-0896-1
Ishii HS, Harder LD (2012) Phenological associations of within- and among-plant variation in gender with floral morphology and integration in protandrous Delphinium glaucum. J Ecol 100:1029–1038. https://doi.org/10.1111/j.1365-2745.2012.01976.x
Ishii HS, Hirabayashi Y, Kudo G (2008) Combined effects of inflorescence architecture, display size, plant density and empty flowers on bumble bee behaviour: experimental study with artificial inflorescences. Oecologia 156:341–350. https://doi.org/10.1007/s00442-008-0991-4
Lázaro A, Santamaría L (2016) Flower-visitor selection on floral integration in three contrasting populations of Lonicera implexa. Am J Bot 103:325–336. https://doi.org/10.3732/ajb.1500336
Lu NN, Li XH, Li L, Zhao ZG (2015) Variation of nectar production in relation to plant characteristics in protandrous Aconitum gymnandrum. J Plant Ecol 8:122–129. https://doi.org/10.1093/jpe/rtv020
Makino TT, Sakai S (2007) Experience changes pollinator responses to floral display size: from size-based to reward-based foraging. Funct Ecol 21:854–863. https://doi.org/10.1111/j.1365-2435.2007.01293.x
McDonald JH (2014) Nested anova. In: McDonald JH (ed) Handbook of biological statistics, 3rd edn. Sparky House Publishing, Baltimore
Misaki A, Itagaki T, Matsubara Y, Sakai S (2018) Intraflower variation in nectar secretion: secretion patterns and pollinator behavior in male and female–phase flowers. Am J Bot 105:842–850. https://doi.org/10.1002/ajb2.1099
Mitchell RJ (1993) Adaptive significance of Ipomopsis aggregata nectar production: observation and experiment in the field. Evolution (N Y) 47:25–35
Morinaga S-I, Sakai S (2006) Functional differentiation in pollination processes between the outer and inner perianths in Iris gracilipes (Iridaceae). Can J Bot 84:164–171. https://doi.org/10.1139/b05-158
Nakamura S, Kudo G (2016) Foraging responses of bumble bees to rewardless floral patches: importance of within-plant variance in nectar presentation. AoB Plants 8:37. https://doi.org/10.1093/aobpla/plw037
Nikkeshi A, Kurimoto D, Ushimaru A (2015) Low flower-size variation in bilaterally symmetrical flowers: support for the pollination precision hypothesis. Am J Bot 102:2032–2040. https://doi.org/10.3732/ajb.1500371
Parachnowitsch AL, Manson JS, Sletvold N (2019) Evolutionary ecology of nectar. Ann Bot. https://doi.org/10.1093/aob/mcy132
Pérez-Barrales R, Arroyo J, Armbruster WS (2007) Differences in pollinator faunas may generate geographic differences in floral morphology and integration in Narcissus papyraceus (Amaryllidaceae). Oikos 116:1904–1918. https://doi.org/10.1111/j.0030-1299.2007.15994.x
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ramírez-Aguirre E, Martén-Rodríguez S, Ornelas JF (2016) Floral variation, nectar production, and reproductive success of two Drymonia (Gesneriaceae) species with mixed pollination syndromes. Int J Plant Sci 177:469–480. https://doi.org/10.1086/686584
Rosas-Guerrero V, Quesada M, Armbruster WS, Pérez-Barrales R, Smith SDW (2011) Influence of pollination specialization and breeding system on floral integration and phenotypic variation in ipomoea. Evolution (N Y) 65:350–364. https://doi.org/10.1111/j.1558-5646.2010.01140.x
Schneider C, Rasband W, Eliceiri K (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Smith SD (2016) Pleiotropy and the evolution of floral integration. New Phytol 209:80–85. https://doi.org/10.1111/nph.13583
Smith RA, Rausher MD (2008) Experimental evidence that selection favors character displacement in the ivyleaf morning glory. Am Nat 171:1–9. https://doi.org/10.1086/523948
Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annu Rev Ecol Syst 1:307–326
Ushimaru A, Itagaki T, Ishii HS (2003) Variation in floral organ size depends on function: a test with Commelina communis, an andromonoecious species. Evol Ecol Res 5:615–622
Ushimaru A, Kikuchi S, Yonekura R, Maruyama A, Yanagisawa N, Kagami M, Nakagawa M, Mahoro S, Kohmatsu Y, Hatada A, Kitamura S, Nakata K (2007) The influence of floral symmetry and pollination systems on flower size variation. Nord J Bot 24:593–598. https://doi.org/10.1111/j.1756-1051.2004.tb01644.x
Wagner GP (1984) On the eigenvalue distribution of genetic and phenotypic dispersion matrices: evidence for a nonrandom organization of quantitative character variation. J Math Biol 21:77–95
Zhao Z, Lu N, Conner JK (2016) Adaptive pattern of nectar volume within inflorescences: Bumblebee foraging behavior and pollinator-mediated natural selection. Sci Rep 6:1–8. https://doi.org/10.1038/srep34499
Acknowledgements
We thank K. Yonekura for support in locating the study site; M. Oguro and M. Nomura for statistical advice; all colleagues in our laboratory, especially K. Takano and T. Hasegawa, for various kinds of help; and Mt. Hakkoda Botanical Garden, Tohoku University, for providing a laboratory and accommodations. A grant-in-aid from the Japanese Ministry of Education, Culture, Sports, Science and Technology funded this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Philip Ladd.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Itagaki, T., Misaki, A. & Sakai, S. Selection for floral integration and trait variation in zygomorphic flowers of Aconitum japonicum ssp. subcuneatum (Ranunculaceae). Plant Ecol 221, 347–359 (2020). https://doi.org/10.1007/s11258-020-01017-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-020-01017-0