Greater number of pollen donors improves female reproductive success but not progeny vigour in Allium stellatum
DOI:
https://doi.org/10.26786/1920-7603(2025)847Keywords:
Pollen competition, pollen load, plant-pollinator interactions, population fitness, trade-offs, multiple matingAbstract
Plant-pollinator interactions affect the quantity and identity of pollen delivered to stigmas, influencing plant genetics and fitness. Here, we test the pollen competition hypothesis, which predicts that competition among pollen grains yields higher-quality offspring, by hand-pollinating Allium stellatum with pollen from one, two, or three donors while controlling pollen load size. We germinated seeds and assessed seed and seedling traits using generalised linear mixed-effects models. We found that flowers that received pollen loads with a greater number of donors had slower growing seedlings but also had a greater proportion of seeds that successfully germinated. These results provide mixed support for the pollen competition hypothesis, in that greater donor diversity leads to higher female reproductive success, but with a possible trade-off in progeny vigour. Pollen donor diversity thus affects reproductive outcomes and should be considered when examining how pollinators influence plant population dynamics.
References
Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281. DOI: https://doi.org/10.1890/06-1017
Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, D.R. Campbell, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421. DOI: https://doi.org/10.1890/03-8024
Baskin JM, Baskin CC (2015) Pollen (microgametophyte) competition: an assessment of its significance in the evolution of flowering plant diversity, with particular reference to seed germination. Seed Science Research 25:1-11. DOI: https://doi.org/10.1017/S0960258515000033
Baskin JM, Baskin CC (2019) How much influence does the paternal parent have on seed germination? Seed Science Research 29:1-11. https://www.doi.org/10.1017/S0960258518000417. DOI: https://doi.org/10.1017/S0960258518000417
Beaudry FEG, Rifkin JL, Barret SCH, Wright SI (2020) Evolutionary Genomics of Plant Gametophytic Selection. Plant Communications 1:100115. DOI: https://doi.org/10.1016/j.xplc.2020.100115
Bernasconi G (2003) Seed paternity in flowering plants: An evolutionary perspective. Perspectives in Plant Ecology, Evolution and Systematics 6:149–158. DOI: https://doi.org/10.1078/1433-8319-00075
Bertin RI (1990) Effects of Pollination Intensity in Campsis radicans. American Journal of Botany 77:178–187. DOI: https://doi.org/10.1002/j.1537-2197.1990.tb13544.x
Breed MF, Ottewell KM, Gardner MG, Marklund MHK, Dormontt EE, Lowe AJ (2015) Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics. Heredity 115:108–114. DOI: https://doi.org/10.1038/hdy.2013.48
Chae K, Lord EM (2011) Pollen tube growth and guidance: roles of small, secreted proteins. Annals of Botany 108:627–636. DOI: https://doi.org/10.1093/aob/mcr015
Dhole, S, Stern CA, Servedio MR (2018) Direct detection of male quality can facilitate the evolution of female choosiness and indicators of good genes: Evolution across a continuum of indicator mechanisms. Evolution 72:770-784. DOI: https://doi.org/10.1111/evo.13466
Ehrlén J (1992) Proximate limits to seed production in a herbaceous perennial legume, Lathyrus vernus. Ecology 73:1820–1831. DOI: https://doi.org/10.2307/1940033
Ellstrand NC (1984) Multiple Paternity within the Fruits of the Wild Radish, Raphanus sativus. The American Naturalist 123:819–828. DOI: https://doi.org/10.1086/284241
Goring DR (2018) Exocyst, exosomes, and autophagy in the regulation of Brassicaceae pollen-stigma interactions. Journal of Experimental Botany 69:69–78. DOI: https://doi.org/10.1093/jxb/erx340
Holland JN, Chamberlain SA, Waguespack AM, Kinyo AS (2009) Effects of pollen load and donor diversity on seed and fruit mass in the columnar cactus, Pachycereus schottii (Cactaceae). International Journal of Plant Sciences 170:467–475. DOI: https://doi.org/10.1086/597266
Honys D, Twell D (2003) Comparative Analysis of the Arabidopsis Pollen Transcriptome. Plant Physiology 132:640–652. DOI: https://doi.org/10.1104/pp.103.020925
Janzen DH (1977) A Note on Optimal Mate Selection by Plants. The American Naturalist 111:365–371. DOI: https://doi.org/10.1086/283166
Knight TM, Steets JA, Vamosi JC Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman TL (2005) Pollen limitation of plant reproduction: Pattern and process. Annual Review of Ecology, Evolution, and Systematics 36:467–497. DOI: https://doi.org/10.1146/annurev.ecolsys.36.102403.115320
Krauss SL, Phillips RD, Karron JD, Johnson SD, Robert DG, Hopper SD (2017) Novel Consequences of Bird Pollination for Plant Mating. Trends in Plant Science 22:395–410. DOI: https://doi.org/10.1016/j.tplants.2017.03.005
Lee TD (1984) Patterns of Fruit Maturation: A Gametophyte Competition Hypothesis. The American Naturalist 123:427–432. DOI: https://doi.org/10.1086/284213
Leishman MR, Wright IJ, Moles AT, Westoby M (2000) The evolutionary ecology of seed size. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. Oxford University Press, Oxford, pp 31–57. DOI: https://doi.org/10.1079/9780851994321.0031
Lind JL, Bönig I, Clarke AE, Anderson MA (1996) A style-specific 120-kDa glycoprotein enters pollen tubes of Nicotiana alata in vivo. Sexual Plant Reproduction 9:75–86. DOI: https://doi.org/10.1007/s004970050013
McCallum B, Chang SM (2016) Pollen competition in style: Effects of pollen size on siring success in the hermaphroditic common morning glory, Ipomoea purpurea. American Journal of Botany 103:460–470 DOI: https://doi.org/10.3732/ajb.1500211
McClure BA, Cruz-Garcia F, Beecher B, Sulaman W (2000) Factors affecting inter- and intra-specific pollen rejection in Nicotiana. Annals of Botany 85:113-123. DOI: https://doi.org/10.1006/anbo.1999.1061
Mckenna M (1983) Ecological aspects of gametophytic competition in Dianthus chinensis. In: Mulcahy D, Ottaviano E (eds) Pollen: Biology and Implications in Plant Breeding, Elsevier, New York, pp 419-424.
Milberg P, Lamont BB (1997) Seed/cotyledon size and nutrient content play a major role in early performance of species on nutrient-poor soils. New Phytologist 137:665–672. DOI: https://doi.org/10.1046/j.1469-8137.1997.00870.x
Minaar C, Anderson B, De Jager ML, Karron JD (2019) Plant-pollinator interactions along the pathway to paternity. Annals of Botany 123:225–245. DOI: https://doi.org/10.1093/aob/mcy167
Molano-Flores B, Hendrix SD, Heard SB (1999). The Effect of Population Size on Stigma Pollen Load, Fruit Set, and Seed Set in Allium. International Journal of Plant Sciences 160:753–757. DOI: https://doi.org/10.1086/314160
Montalvo AM (1992) Relative Success of Self and Outcross Pollen Comparing Mixed- and Single-Donor Pollinations in Aquilegia caerulea. Evolution 46:1181–1198. DOI: https://doi.org/10.1111/j.1558-5646.1992.tb00627.x
Mulcahy DL (1979) The Rise of the Angiosperms: A Genecological Factor. Science 206: 20–23. DOI: https://doi.org/10.1126/science.206.4414.20
Mulcahy DL, Mulcahy GB (1975) The influence of gametophytic competition on sporophytic quality in Dianthus chinensis. Theoretical and Applied Genetics 46:277–280. DOI: https://doi.org/10.1007/BF00281149
Mulcahy DL, Mulcahy GB (1987) The effects of pollen competition. American Scientist 75:44–50. https://www.jstor.org/stable/27854449.
Niesenbaum RA (1999) The effects of pollen load size and donor diversity on pollen performance, selective abortion, and progeny vigor in Mirabilis jalapa (Nyctaginaceae). American Journal of Botany 86: 261–268. DOI: https://doi.org/10.2307/2656941
Obeso JR (2002) The costs of reproduction in plants. New Phytologist 155:321–348. DOI: https://doi.org/10.1046/j.1469-8137.2002.00477.x
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. DOI: https://doi.org/10.1111/j.1600-0706.2010.18644.x
Palmer TM, Zimmerman M (1994) Pollen Competition and Sporophyte Fitness in Brassica campestris: Does Intense Pollen Competition Result in Individuals with Better Pollen? Oikos 69:80-86. DOI: https://doi.org/10.2307/3545286
Pannell JR, Labouche AM (2013) The incidence and selection of multiple mating in plants. Philosophical Transactions of the Royal Society B: Biological Sciences 368. DOI: https://doi.org/10.1098/rstb.2012.0051
Paschke M, Abs C, Schmid B (2002) Effects of population size and pollen diversity on reproductive success and offspring size in the narrow endemic Cochlearia bavarica (Brassicaceae). American Journal of Botany 89:1250–1259. DOI: https://doi.org/10.3732/ajb.89.8.1250
Pedersen S, Simonsen V, Loeschcke V (1987) Overlap of gametophytic and sporophytic gene expression in barley. Theoretical and Applied Genetics 75:200–206. DOI: https://doi.org/10.1007/BF00249164
Prokop ZM, L Michalczyk SM, Drobniak SM, Herdegen M, Radwan J (2012) Meta-analysis suggests choosy females get sexy sons more than “good genes”. Evolution 66:2665-2673 DOI: https://doi.org/10.1111/j.1558-5646.2012.01654.x
Quesada M, Stephenson AG, Winsor JA (1996) Effects of pollen competition on the reproductive performance in cucurbit hybrids (Cucurbitaceae): F1 and backcross generations. Canadian Journal of Botany 74:1113–1118. DOI: https://doi.org/10.1139/b96-136
Rejón, J, Delalande F, Schaeffer-Reiss C, Alché J, Rodríguez-García M, Van Dorsselaer A, Castro AJ (2016) The Pollen Coat Proteome: At the Cutting Edge of Plant Reproduction. Proteomes 4:5. DOI: https://doi.org/10.3390/proteomes4010005
Rhodes MK, Fant JB, Skogen KA (2017) Pollinator identity and spatial isolation influence multiple paternity in an annual plant. Molecular Ecology 26:4296–4308. DOI: https://doi.org/10.1111/mec.14115
Richardson TE, Stephenson AG (1992) Effects of parentage and size of the pollen load on progeny performance in Campanula americana. Evolution 46:1731–1739. DOI: https://doi.org/10.1111/j.1558-5646.1992.tb01165.x
Shipley B, Dion J (1992) The allometry of seed production in herbaceous angiosperms. The American Naturalist 139:467–483. DOI: https://doi.org/10.1086/285339
Smith CC, Fretwell SD (1974) The Optimal Balance between Size and Number of Offspring. The American Naturalist 108:499–506. DOI: https://doi.org/10.1086/282929
Snow AA (1990) Effects of Pollen-Load Size and Number of Donors on Sporophyte Fitness in Wild Radish (Raphanus raphanistrum). The American Naturalist 136:742–758. DOI: https://doi.org/10.1086/285129
Stephenson AG (1981) Flower and Fruit Abortion: Proximate Causes and Ultimate Functions. Annual Review of Ecology and Systematics 1:253–279. https://www.annualreviews.org/content/journals/10.1146/annurev.es.12.110181.001345. DOI: https://doi.org/10.1146/annurev.es.12.110181.001345
Stephenson AG, Bertin RI (1983) Male competition, female choice, and sexual selection in plants. In: Real L (ed) Pollination Biology. Academic Press Inc., New York, pp 110-149. DOI: https://doi.org/10.1016/B978-0-12-583980-8.50013-2
Torres-Vanegas F, Hadley AS, Kormann UG, Jones FA, Betts MG, Wagner HH (2021) Tropical deforestation reduces plant mating quality by shifting the functional composition of pollinator communities. Journal of Ecology 109:1730–1746. DOI: https://doi.org/10.1111/1365-2745.13594
Valdivia ER, Stepheson AG, Durachko DM, Cosgrove D (2009) Class B β-expansins are needed for pollen separation and stigma penetration. Sexual Plant Reproduction 22:141–152. DOI: https://doi.org/10.1007/s00497-009-0099-y
Walsh NE, Charlesworth D (1992) Evolutionary Interpretations of Differences in Pollen Tube Growth Rates. The Quarterly Review of Biology 67:19–37. DOI: https://doi.org/10.1086/417446
Warman C, Panda K, Vejlupkova Z, Hokin S, Unger-Wallace E, Cole RA, Chettoor AM, Jiang D, Vollbrecht E, Evans MMS, Slotkin RKK, Fowler JE (2020) High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements. PLoS Genetics 16:e1008462. DOI: https://doi.org/10.1371/journal.pgen.1008462
Weiherer D, Eckardt K, Bernhardt P (2020) Comparative floral ecology and breeding systems between sympatric populations of Nothoscordum bivalve and Allium stellatum (Amaryllidaceae). Journal of Pollination Ecology 26:16–31. DOI: https://doi.org/10.26786/1920-7603(2020)585
Westoby M, Jurado E, Leishman M (1992) Comparative evolutionary ecology of seed size. Trends in Ecology and Evolution 7:368–372. DOI: https://doi.org/10.1016/0169-5347(92)90006-W
Wheeler MJ, Franklin-Tong VE, Franklin FCH (2001) The molecular and genetic basis of pollen-pistil interactions. New Phytologist 151:565-584. DOI: https://doi.org/10.1046/j.0028-646x.2001.00229.x
Winsor JA, Davis LE, Stephenson AG (1987) The Relationship between Pollen Load and Fruit Maturation and the Effect of Pollen Load on Offspring Vigor in Cucurbita pepo. The American Naturalist 129:643–656. DOI: https://doi.org/10.1086/284664
Wu H, Wong E, Ogdahl J, Cheung AY (2000) A pollen tube growth-promoting arabinogalactan protein from Nicotiana alata is similar to the tobacco TTS protein. Plant Journal 22: 165–176. DOI: https://doi.org/10.1046/j.1365-313x.2000.00731.x
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2025 Rieka Yu, Nathan Muchhala

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



