期刊论文详细信息
BMC Evolutionary Biology
Self-pollination rate and floral-display size in Asclepias syriaca (Common Milkweed) with regard to floral-visitor taxa
Edward M Barrows1  Aaron F Howard2 
[1] Center for the Environment, Georgetown University, Box 571229, Washington, DC 20057-1229, USA;Department of Biology, Georgetown University, Box 571229, Washington, DC 20057-1229, USA
关键词: Self-pollination rate;    Mating system;    Geitonogamy;    Floral-display size;    Asclepias syriaca;    Insect pollinators;    Bombus;    Apocynaceae;    Apis mellifera;   
Others  :  848445
DOI  :  10.1186/1471-2148-14-144
 received in 2014-03-10, accepted in 2014-05-20,  发布年份 2014
PDF
【 摘 要 】

Background

Animals fertilize thousands of angiosperm species whose floral-display sizes can significantly influence pollinator behavior and plant reproductive success. Many studies have measured the interactions among pollinator behavior, floral-display size, and plant reproductive success, but few studies have been able to separate the effects of pollinator behavior and post-pollination processes on angiosperm sexual reproduction. In this study, we utilized the highly self-incompatible pollinium-pollination system of Asclepias syriaca (Common Milkweed) to quantify how insect visitors influenced male reproductive success measured as pollen removal, female reproductive success measured as pollen deposition, and self-pollination rate. We also determined how floral-display size impacts both visitor behavior and self-pollination rate.

Results

Four insect taxonomic orders visited A. syriaca: Coleoptera, Diptera, Hymenoptera, and Lepidoptera. We focused on three groups of visitor taxa within two orders (Hymenoptera and Lepidoptera) with sample sizes large enough for quantitative analysis: Apis mellifera (Western Honey Bee), Bombus spp. (bumble bees) and lepidopterans (butterflies and moths). Qualitatively, lepidopterans had the highest pollinator importance values, but the large variability in the lepidopteran data precluded meaningful interpretation of much of their behavior. The introduced A. mellifera was the most effective and most important diurnal pollinator with regard to both pollen removal and pollen deposition. However, when considering the self-incompatibility of A. syriaca, A. mellifera was not the most important pollinator because of its high self-pollination rate as compared to Bombus spp. Additionally, the rate of self-pollination increased more rapidly with the number of flowers per inflorescence in A. mellifera than in the native Bombus spp.

Conclusions

Apis mellifera’s high rate of self-pollination may have significant negative effects on both male and female reproductive successes in A. syriaca, causing different selection on floral-display size than native pollinators.

【 授权许可】

   
2014 Howard and Barrows; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20140718071900169.pdf 1468KB PDF download
Figure 7. 91KB Image download
Figure 6. 84KB Image download
Figure 5. 50KB Image download
Figure 4. 111KB Image download
Figure 3. 85KB Image download
Figure 2. 63KB Image download
Figure 1. 109KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】
  • [1]Broyles SB, Wyatt R: A reexamination of the pollen-donation hypothesis in an experimental population of Asclepias exaltata. Evolution 1995, 49:89-99.
  • [2]Beattie AJ: Pollination mechanisms in Viola. New Phytol 1971, 70:343-360.
  • [3]Herrera CM: Components of pollen “quality”: comparative analysis of a diverse insect assemblage. Oikos 1987, 50:79-90.
  • [4]Armbruster WS: Estimating and testing the shapes of adaptive surfaces: the morphology and pollination of Dalechampia blossoms. Am Nat 1990, 135:14-31.
  • [5]Shemske DW, Horovitz CC: Temporal variation in selection on floral character. Evolution 1989, 43:461-465.
  • [6]Stanton M, Young HJ, Ellstrand NC, Clegg JM: Consequences of floral variation for male and female reproduction in experimental populations of Wild Radish, Raphanus sativus L. Evolution 1991, 45:268-280.
  • [7]Ivey CT, Martinez P, Wyatt R: Variation in pollinator effectiveness in Swamp Milkweed, Asclepias incarnata (Apocynaceae). Am J Bot 2003, 90:214-225.
  • [8]Brunet J, Sweet HR: Impact of insect pollinator group and floral display size on outcrossing rate. Evolution 2006, 60:234-246.
  • [9]Harder LD, Barrett SCH: Mating cost of large floral displays in hermaphrodite plants. Nature 1995, 373:512-515.
  • [10]Karron JD, Holmquist KG, Flanagan RJ, Mitchell RJ: Pollinator visitation patterns strongly influence among-flower variation in selfing rate. Ann Bot-London 2009, 103:1379-1383.
  • [11]Herlihy CM, Eckert CG: Experimental dissection of inbreeding and its adaptive significance in a flowering plant, Aquilegia canadensis (Ranunculaceae). Evolution 2004, 58:2693-2703.
  • [12]Karron JD, Thumser NN, Tucker R, Hessenauer AJ: The influence of population density on outcrossing rates in Mimulus ringens. Heredity 1995, 75:175-180.
  • [13]Klinkhamer PGL, de Jong TJ: Attractiveness to pollinators: a plants’ dilemma. Oikos 1993, 66:180-184.
  • [14]Kunin WE: Sex and the single mustard: population density and pollinator behavior effects on seed-set. Ecology 1993, 74:2145-2160.
  • [15]Wyatt R, Ivey CT: Family outcrossing rates and neighborhood floral density in natural populations of Swamp Milkweed (Asclepias incarnata): potential statistical artifacts. Theo Appl Genet 1999, 98:1063-1071.
  • [16]Karron JD, Mitchell RJ, Holmquist KG, Bell JM, Funk B: The influence of floral display size on selfing rates in Mimulus ringens. Heredity 2004, 92:242-248.
  • [17]Wyatt R: Pollination and fruit-set in Asclepias: a reappraisal. Am J Bot 1976, 63:845-851.
  • [18]Fishbein M, Venable DL: Diversity and temporal change in the effective pollinators of Asclepias tuberosa. Ecology 1996, 77:1061-1073.
  • [19]Broyles SB, Wyatt R: Paternity analysis in a natural population of Asclepias exaltata — multiple paternity, functional gender, and the “Pollen-donation hypothesis”. Evolution 1990, 44:1454-1468.
  • [20]Willson MF: Adaptive design of the floral display in Asclepias syriaca L. Am Midl Nat 1974, 92:47-57.
  • [21]Broyles SB, Wyatt R: The pollen donation hypothesis revisited: a response to Queller. Am Nat 1997, 149:595-599.
  • [22]Fishbein M, Venables DL: Evolution of inflorescence design: theory and data. Evolution 1996, 50:2165-2177.
  • [23]Queller DC: Sexual selection in a hermaphroditic plant. Nature 1983, 305:706-707.
  • [24]Wyatt R, Broyles SB: Ecology and evolution of reproduction in milkweeds. Annu Rev Ecol Syst 1994, 25:423-441.
  • [25]Kephart SR: The partitioning of pollinators among three species of Asclepias. Ecology 1983, 64:120-133.
  • [26]Willson MF, Bertin RI: Flower-visitors, nectar production, and inflorescence size of Asclepias syriaca. Can J Bot 1979, 57:1380-1388.
  • [27]Goulson D: Effects of introduced bees on native ecosystems. Annu Rev Ecol Syst 2003, 34:1-26.
  • [28]Gross CL, Mackay D: Honeybees reduce fitness in the pioneer shrub Melastoma affine (Melastomataceae). Biol Conserv 1998, 86:169-178.
  • [29]Roubik DW: African honey bees as exotic pollinators in French Guinea. In The Conservation of Bees. Edited by Matheson A, Buchmann SL, O’Toole C, Westrich P, Williams IH. London: Academic; 1996:173-182.
  • [30]Paton DC: Budgets for the use of floral resources in mallee heath. In The Mallee Lands: A Conservation Perspective. Edited by Noble JC, Joss PJ, Jones GK. Melbourne: CSIRO; 1990:189-193.
  • [31]Paton DC: Honeybees in the Australian environment – does Apis mellifera disrupt or benefit the native biota? Bioscience 1993, 43:95-103.
  • [32]Thompson JD: How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system. Oecologia 2001, 126:386-394.
  • [33]Lipow SR, Wyatt R: Single gene control of postzygotic self-incompatibility in Poke Milkweed, Asclepias exaltata L. Genetics 2000, 154:893-907.
  • [34]Pleasants JM: Evidence for short-distance dispersal of pollinia in Asclepias syriaca L. Funct Ecol 1991, 5:75-82.
  • [35]Pleasants JM, Ng G: The relationship between inflorescence size and self-pollination in milkweed, Asclepias syriaca [abstract]. Iowa Acad Sci 1987.
  • [36]Shore JS: Pollination genetics of the Common Milkweed, Asclepias syriaca L. Heredity 1992, 70:101-108.
  • [37]Eckert CG: Contributions of autogamy and geitonogamy to self-fertilization in a mass-flowering, clonal plant. Ecology 2000, 81:532-542.
  • [38]Kropf M, Renner SS: Pollinator-mediated selfing in two deceptive orchids and a review of pollinium tracking studies addressing geitonogamy. Oecologia 2008, 155:497-508.
  • [39]Nishihiro J, Washitani I: Patterns and consequences of self-pollen deposition on stigmas in heterstylous Persicaria japonica (Polygonaceae). Am J Bot 1998, 85:352-359.
  • [40]Matsuki Y, Isagi Y, Suyama Y: The determination of multiple microsatellite genotypes and DNA sequence from a single pollen grain. Mol Ecol Notes 2007, 7:194-198.
  • [41]Morse DH: The role of self-pollen in the female reproductive success of Common Milkweed (Asclepias syriaca: Asclepiadaceae). Am J Bot 1994, 81:322-330.
  • [42]Wilbur HM: Life history evolution in seven milkweeds of the genus Asclepias. J Ecol 1976, 64:223-240.
  • [43]Kahn AP, Morse DH: Pollinium germination and putative ovule penetration in self- and cross-pollinated common milkweed Asclepias syriaca. Am Midl Nat 1991, 126:61-67.
  • [44]Kephart SR: Breeding Systems in Asclepias incarnata L., A. syriaca L., and A. verticillata L. Am J Bot 1981, 68:226-232.
  • [45]Kephart SR: Phenological variation in flowering and fruiting of Asclepias. Am Midl Nat 1987, 118:64-67.
  • [46]Liede S, Weberling F: On the inflorescence structure of Asclepiadaceae. Plant Syst Evol 1995, 197:99-109.
  • [47]Wyatt R, Broyles SB, Dedra GS: Environmental influences on nectar production in milkweeds (Asclepias syriaca and A. exaltata). Am J Bot 1992, 79:636-642.
  • [48]O’Quinn RL, Fishbein M: Isolation, characterization and cross-species amplification of polymorphic microsatellite loci in Asclepias (Apocynaceae). Conserv Genet 2009, 10:1437-1440.
  • [49]Shaw DV, Kohler AL, Allard RW: A multilocus estimator of mating system parameters in plant population. P Natl Acad Sci USA 1981, 78:1298-1302.
  • [50]Cruzan MB, Hamrick JL, Arnold ML, Bennett BD: Mating system variation in hybridizing irises: effects of phenology and floral densities on family outcrossing rates. Heredity 1994, 72:95-105.
  • [51]Park JC, Werth CR: A study of spatial features of clones in a population of Bracken Fern, Pteridium aquilinium (Dennstaedtiaceae). Am J Bot 1993, 80:537-544.
  • [52]Olsen KM: Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia 1997, 109:114-121.
  • [53]Ver Hoek JM, Boveng PL: Quasi-poisson vs. negative binomial regression: how should we model overdispersed count data? Ecology 2007, 88:2766-2772.
  • [54]Cameron A, Trevedi PK: Regression Analysis of Count Data. New York: Cambridge University Press; 1998.
  • [55]Eckert CG, Barrett SCH: Inbreeding depression in partially self-fertilizing Decodon verticillatus (Lythraceae): population-genetic and experimental analysis. Evolution 1994, 48:952-964.
  • [56]Reynolds RJ, Fenster CB: Point and interval estimation of pollinator importance: a study using pollination data of Silene caroliniana. Oecologia 2008, 156:325-332.
  • [57]Hollander M, Wolfe DA: Nonparametric Statistical Methods. New York: John Wiley & Sons; 1999.
  • [58]Wu J, Zhang L, Johnson WD: The permutation test as an ancillary procedure for compaing zero-inflated continuous distributions. Open J Stat 2012, 2:274-280.
  • [59]Development Core Team R: R: A language and environment for statistical computing. [http://www.R-project.org webcite]
  • [60]Morse DH, Fritz RS: Contributions of diurnal and nocturnal insects to the pollination of Common Milkweed (Asclepias syriaca L.) in a pollen-limited system. Oecologia 1983, 60:190-197.
  • [61]Southwick EE: Nectar biology and nectar feeders of Common Milkweed, Asclepias syriaca L. Bull Torrey Bot Club 1983, 110:324-334.
  • [62]Liede-Schumann S, Meve U: ASCLEPOL. [http://www.bio.uni-bayreuth.de/planta2/research/pollina/as_pol_t.html webcite]
  • [63]Bertin RI, Willson MF: Effectiveness of diurnal and nocturnal pollination of two milkweeds. Can J Bot 1980, 58:1744-1746.
  • [64]Morse DH: Modification of bumblebee foraging: the effect of milkweed pollinia. Ecology 1981, 62:89-97.
  • [65]Betz RF, Struven RD, Wall JE, Heitler FB: Insect pollinators of 12 milkweed (Asclepias) species. In Proceedings of the Thirteenth North American Prairie Conference: 1994; Windsor, Ontario. Edited by Wickett RG, Lewis PD, Woodliffe A, Pratt P. Windsor: Department of Parks and Recreation; 1994:45-60.
  • [66]Lynch SP: The floral ecology of Asclepias solanoano Woods. Madrono 1977, 24:159-177.
  • [67]Mitchell RJ, Karron JD, Holmquist KG, Bell JM: The influence of Mimulus ringens floral display size on pollinator visitation patterns. Funct Ecol 2004, 18:116-124.
  • [68]Kunin WE: Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber. J Ecol 1997, 85:225-234.
  • [69]Morris WF: Predicting the consequences of plant spacing and biased movement for pollen dispersal by Honey Bees. Ecology 1993, 74:493-500.
  • [70]De Jong TJ, Waser NM, Klinkhamer PGL: Geitonogamy: the neglected side of selfing. Trends Ecol Evol 1993, 8:321-325.
  • [71]Broyles SB, Wyatt R: The consequences of self-pollination in Asclepias exaltata, a self-incompatible milkweed. Am J Bot 1993, 80:41-44.
  • [72]Barrett SCH: Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Phil Trans R Soc Lond B 2003, 358:991-1004.
  • [73]Ashman TL, Morgan M: Explaining phenotypic selection on plant attractive characters: male function, gender balance or ecological context? P Roy Soc B-Biol Sci 2004, 271:553-559.
  • [74]Zimmerman M, Pyke GH: Reproduction in Pandemonium: assessing the factors limiting seed set. Am Nat 1988, 131:723-738.
  • [75]Sheppard WS: A history of the introduction of honey bee races into the United States, part 1. Amer Bee J 1989, 129:617-619.
  • [76]Bolstad GH, Armbruster WS, Pelabon C, Perez-Barrales R, Hansen TF: Direct selection at the blossom level on floral reward by pollinators in a natural population of Dalechampia schottii: full-disclosure honesty? New Phytol 2010, 188:370-384.
  • [77]Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD: Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 2004, 35:375-403.
  • [78]Wyatt R, Shannon TR: Nectar production and pollination of Asclepias exaltata. Syst Bot 1986, 11:326-334.
  • [79]Pleasant JM, Chaplin SJ: Nectar production rates of Asclepias quadrifolia: causes and consequences of individual variation. Oecologia 1983, 59:232-238.
  • [80]Biernaskie JM, Cartar RV: Variation in rate of nectar production depends on floral display size: a pollinator manipulation hypothesis. Funct Ecol 2004, 18:125-129.
  • [81]Iwasa Y, de Jong TJ, Klinkhamer PGL: Why pollinators visit only a fraction of the open flowers on a plant: the plant’s point of view. J Evolution Biol 1995, 8:439-453.
  • [82]Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhöffer JH, Freitas BM, Ghazoul J, Greenleaf S, Hipólito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka K, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, et al.: Wild pollinators enhance fruit set of crops regardless of Honey Bee abundance. Science 2013, 339:1608-1611.
  文献评价指标  
  下载次数:104次 浏览次数:58次