Conclusion and future directions
In virtually all communities, species vary widely in their abundance. In this article, I demonstrate that this variability could explain a part of the angiosperms’ remarkable floral diversity. The model presented here offers a potential framework to understand the evolution toward different pollination systems. According to this model, the optimal pollination system is a function of the pollinator assemblage (which varies geographically according to the Grant-Stebbins model), the plant community in which a species is embedded, and its floral abundance. This more holistic view integrating the plant community context with selection exerted by different pollinators promises to improve our understanding of the ecological processes involved in flower diversification.
Future studies should investigate how this mechanism operates in natural systems. In support of the model, some studies have shown that the strength of selection on floral traits can be affected by floral density (see Eisen et al. 2020 and references therein). An important next step would be to investigate how floral abundance affects the strength and direction of selection exerted by different pollinators. Such studies should be performed at the scale of whole populations to encompass representative variation in the pollination processes affected by floral abundance. Studies investigating how different pollination systems are associated with distinct floral abundances could also be very informative, although such studies would require careful consideration of historical contingency and spatiotemporal variation in species’ abundances.
ACKNOWLEDGMENTS
I thank Jessica Forrest, Colleen Smith, Lydia Wong and the members of the Forrest laboratory for valuable comments on the manuscript. Financial support was provided through a doctoral scholarship from the Natural Sciences and Engineering Research Council of Canada.
REFERENCES
Aigner, P.A. (2001). Optimality modeling and fitness trade-offs: when should plants become pollinator specialists? Oikos , 95, 177–184.
Amaya-Márque, M. (2009). Floral constancy in bees: a revision of theories and a comparison with other pollinators. Rev. Colomb. Entomol. , 35, 206–216.
Armbruster, S.W. (2011). Evolution and ecological implications of “specialized” pollinator rewards. In: Evolution of plant-pollinator relationships (ed. Patiny, S.). Cambridge University Press, New York., pp. 44–67.
Armbruster, W.S. (2014). Floral specialization and angiosperm diversity: phenotypic divergence, fitness trade-offs and realized pollination accuracy. AoB Plants , 6, plu003.
Armbruster, W.S. (2017). The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Funct. Ecol. , 31, 88–100.
Baldridge, E., Harris, D.J., Xiao, X. & White, E.P. (2016). An extensive comparison of species-abundance distribution models.PeerJ , 2016, e2823.
Bascompte, J., Jordano, P., Melián, C.J. & Olesen, J.M. (2003). The nested assembly of plant-animal mutualistic networks. Proc. Natl. Acad. Sci. U. S. A. , 100, 9383–9387.
Benadi, G. & Pauw, A. (2018). Frequency dependence of pollinator visitation rates suggests that pollination niches can allow plant species coexistence. J. Ecol. , 106, 1892–1901.
Bergamo, P.J., Susin Streher, N., Traveset, A., Wolowski, M. & Sazima, M. (2020). Pollination outcomes reveal negative density‐dependence coupled with interspecific facilitation among plants. Ecol. Lett. , 23, 129–139.
Bobrowiec, P.E.D. & Oliveira, P.E. (2012). Removal effects on nectar production in bat-pollinated flowers of the Brazilian Cerrado.Biotropica , 44, 1–5.
Burd, M. (1995). Pollinator behavioural responses to reward size inLobelia Deckenii : no escape from pollen limitation of seed set.J. Ecol. , 83, 865.
Campbell, D.R. (1985). Pollen and gene dispersal: the influences of competition for pollination. Evolution. , 39, 418–431.
Caruso, C.M. (2000). Competition for pollination influences selection on floral traits of ipomopsis aggregata. Evolution. , 54, 1546–1557.
Caruso, C.M. (2002). Influence of plant abundance on pollination and selection on floral traits of ipomopsis aggregata .Ecology , 83, 241–254.
Castellanos, M.C., Wilson, P. & Thomson, J.D. (2002). Dynamic nectar replenishment in flowers of Penstemon (Scrophulariaceae).Am. J. Bot. , 89, 111–118.
Castellanos, M.C., Wilson, P. & Thomson, J.D. (2004). “Anti-bee” and “pro-bird” changes during the evolution of hummingbird pollination inPenstemon flowers. J. Evol. Biol. , 17, 876–885.
Culley, T.M., Weller, S.G. & Sakai, A.K. (2002). The evolution of wind pollination in angiosperms. Trends Ecol. Evol. , 17, 361–369.
Darwin, C. (1877). The various contrivances by which orchids are fertilised by insects . John Murray, London, UK.
Dorado, J., Vázquez, D.P., Stevani, E.L. & Chacoff, N.P. (2011). Rareness and specialization in plant–pollinator networks.Ecology , 92, 19–25.
Dormann, C.F., Fruend, J. & Gruber, B. (2020). Package bipartite: visualising bipartite networks and calculating some (ecological) indices. https://CRAN.R-project.org/package=bipartite.
Duffy, K.J. & Stout, J.C. (2008). The effects of plant density and nectar reward on bee visitation to the endangered orchidSpiranthes romanzoffiana . Acta Oecologica , 34, 131–138.
Eisen, K.E., Wruck, A.C. & Geber, M.A. (2020). Floral density and co-occurring congeners alter patterns of selection in annual plant communities. Evolution. , in press.
Essenberg, C.J. (2012). Explaining variation in the effect of floral density on pollinator visitation. Am. Nat. , 180, 153–66.
Fattorini, R. & Glover, B.J. (2020). Molecular Mechanisms of Pollination Biology. Annu. Rev. Plant Biol. , 71, 487–515.
Feinsinger, P. (1983). Coevolution and pollination. In:Coevolution (eds. Futuyma, D.J. & Slatkin, M.). Sinauer Associates, Sunderland, MA, pp. 282–310.
Feinsinger, P., Tiebout, H.M. & Young, B.E. (1991). Do tropical bird-pollinated plants exhibit density-dependent interactions? Field experiments. Ecology , 72, 1953–1963.
Fenster, C.B., Armbruster, W.S., Wilson, P., Dudash, M.R. & Thomson, J.D. (2004). Pollination syndromes and floral specialization.Annu. Rev. Ecol. Evol. Syst. , 35, 375–403.
Ferreiro, G., Baranzelli, M.C., Sérsic, A.N. & Cocucci, A.A. (2017). Patterns of phenotypic selection for oil and nectar in Monttea aphylla (Plantaginaceae) in a geographic mosaic of interactions with pollinators. Flora , 232, 47–55.
Fort, H., Vázquez, D.P. & Lan, B.L. (2016). Abundance and generalisation in mutualistic networks: solving the chicken-and-egg dilemma. Ecol. Lett. , 19, 4–11.
Friedman, J. & Barrett, S.C. (2009). Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Ann. Bot. , 103, 1515–1527.
García-Ramos, G. & Kirkpatrick, M. (1997). Genetic models of adaptation and gene flow in peripheral populations. Evolution. , 51, 21–28.
Geber, M.A. & Moeller, D.A. (2006). Pollinator responses to plant communities and implications for reproductive character evolution. In:Ecology and evolution of flowers (eds. Harder, L.D. & Barrett, S.C.H.). Oxford University Press, New York, NY, pp. 102–119.
Ghazoul, J. (2005). Pollen and seed dispersal among dispersed plants.Biol. Rev. , 80, 413–443.
Gómez, J.M. & Regino, Z. (2006). Ecological factors that promote the evolution of generalization in pollination systems. In:Plant–pollinator interactions: from specialization to generalization (eds. Waser, N.M. & Ollerton, J.). University of Chicago University Press, Chicago, IL, pp. 145–166.
Goulson, D. (1999). Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution.Perspect. Plant Ecol. Evol. Syst. , 2, 185–209.
Grant, V. & Grant, K. (1965). Flower pollination in the Phlox family . Columbia University Press, New York, NY.
Harder, L.D. (1990). Pollen removal by bumble bees and its implications for pollen dispersal. Ecology , 71, 1110–1125.
Harder, L.D. & Johnson, S.D. (2009). Darwin’s beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol. , 183, 530–545.
Hegland, S.J. (2014). Floral neighbourhood effects on pollination success in red clover are scale‐dependent. Funct. Ecol. , 28, 561–568.
Hernández-Hernández, T. & Wiens, J.J. (2020). Why are there so many flowering plants? A multi-scale analysis of plant diversification.Am. Nat. , 195, 000–000.
Herrera, C.M., Castellanos, C. & Nica Medrano, M. (2006). Geographical context of floral evolution: towards an improved research programme in floral diversification. In: Ecology and Evolution of Flowers(eds. Harder, L.D. & Barrett, S.C.H.). Oxford University Press, New York, NY, pp. 278–294.
Holmquist, K.G., Mitchell, R.J. & Karron, J.D. (2012). Influence of pollinator grooming on pollen-mediated gene dispersal in Mimulus ringens (Phrymaceae). Plant Species Biol. , 27, 77–85.
Johnson, S. (2006). Pollinator-driven speciation in plants. In:Ecology and Evolution of Flowers (eds. Harder, L.D. & Barrett, S.C.H.). Oxford University Press, New York, NY, pp. 295–306.
Johnson, S.D. (2010). The pollination niche and its role in the diversification and maintenance of the southern African flora.Philos. Trans. R. Soc. B Biol. Sci. , 365, 499–516.
Johnson, S.D. & Steiner, K.E. (2000). Generalization versus specialization in plant pollination systems. Trends Ecol. Evol. , 15, 140–143.
Jordano, P., Bascompte, J. & Olesen, J.M. (2002). Invariant properties in coevolutionary networks of plant-animal interactions. Ecol. Lett. , 6, 69–81.
Juan, M.O. & Ornelas, F. (2004). PLANT ANIMAL INTERACTIONS Generous-like flowers: nectar production in two epiphytic bromeliads and a meta-analysis of removal effects. Oecologia , 140, 495–505.
Kay, K.M. & Sargent, R.D. (2009). The role of animal pollination in plant speciation: integrating ecology, geography, and genetics.Annu. Rev. Ecol. Evol. Syst. , 40, 637–656.
Kirkpatrick, M. & Barton, N.H. (1997). Evolution of a species’ range.Am. Nat. , 150, 1–23.
Koski, M.H. (2020). The role of sensory drive in floral evolution.New Phytol. , 227, 1012–1024.
Lertzman, K. & Gass, C. (1983). Alternative models of pollen transfer. In: Handbook of experimental pollination biology . Scientific and Academic Editions, New York, NY, pp. 474–489.
Loza, M.I., Jiménez, I., Jørgensen, P.M., Arellano, G., Macía, M.J., Torrez, V.W., et al. (2017). Phylogenetic patterns of rarity in a regional species pool of tropical woody plants. Glob. Ecol. Biogeogr. , 26, 1043–1054.
Mersmann, O., Trautmann, H., Steuer, D. & Bornkamp, B. (2018). truncnorm: truncated normal distribution. https://CRAN.R-project.org/package=truncnorm.
Minnaar, C., Anderson, B., L de Jager, M. & Karron, J.D. (2019). Plant–pollinator interactions along the pathway to paternity.Ann. Bot. , 123, 225–245.
Mitchell, R.J., Flanagan, R.J., Brown, B.J., Waser, N.M. & Karron, J.D. (2009). New frontiers in competition for pollination. Ann. Bot. , 103, 1403–1413.
Morales, C.L. & Traveset, A. (2008). Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. CRC. Crit. Rev. Plant Sci. , 27, 221–238.
Moreira-Hernández, J.I. & Muchhala, N. (2019). Importance of pollinator-mediated interspecific pollen transfer for angiosperm evolution. Annu. Rev. Ecol. Evol. Syst. , 50, 191–217.
Morris, W.F., Price, M. V., Waser, N.M., Thomson, J.D., Thomson, B. & Stratton, D.A. (1994). Systematic increase in pollen carryover and its consequences for geitonogamy in plant populations. Oikos , 71, 431.
Moyroud, E. & Glover, B.J. (2017). The evolution of diverse floral morphologies. Curr. Biol. , 27, R941–R951.
Muchhala, N. (2007). Adaptive trade-off in floral morphology mediates specialization for flowers pollinated by bats and hummingbirds.Am. Nat. , 169, 494–504.
Muchhala, N., Brown, Z., Armbruster, W.S. & Potts, M.D. (2010). Competition drives specialization in pollination systems through costs to male fitness. Am. Nat. , 176, 732–43.
Van der Niet, T. & Johnson, S.D. (2012). Phylogenetic evidence for pollinator-driven diversification of angiosperms. Trends Ecol. Evol. , 27, 353–361.
Van Der Niet, T., Pirie, M.D., Shuttleworth, A., Johnson, S.D. & Midgley, J.J. (2014). Do pollinator distributions underlie the evolution of pollination ecotypes in the Cape shrub Erica plukenetii ?Ann. Bot. , 113, 301–315.
Ogilvie, J.E., Thomson, J.D., Luo, E.Y. & Ogilvie, J.E. (2014). Stimulation of flower nectar replenishment by removal: a survey of eleven animal-pollinated plant species. Artic. J. Pollinat. Ecol. , 12, 52–62.
Olesen, J.M. & Jordano, P. (2002). Geographic patterns in plant-pollinator mutualistic networks. Ecology , 83, 2416–2424.
Palmer, T.M., Stanton, M.L. & Young, T.P. (2003). Competition and coexistence: exploring mechanisms that restrict and maintain diversity within mutualist guilds. Am. Nat. , 162, S63–S79.
Pauw, A. (2007). Collapse of a pollination web in small conservation areas. Ecology , 88, 1759–1769.
Pauw, A. (2013). Can pollination niches facilitate plant coexistence?Trends Ecol. Evol. , 28, 30–37.
Prado, P.I., Miranda, D. & Maintainer, A.C. (2018). sads: maximum likelihood models for species abundance distributions. R package version 0.4.2. https://cran.r-project.org/package=sads.
R core team (2020). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
Rathcke, B. (1983). Competition and facilitation among plants for pollination. In: Pollination Biology (ed. Real, L.). Academic Press, New York, pp. 305–329.
Ricklefs, R.E. (2010). Evolutionary diversification, coevolution between populations and their antagonists, and the filling of niche space.Proc. Natl. Acad. Sci. U. S. A. , 107, 1265–1272.
Robertson, A.W. (1992). The relationship between floral display size, pollen carryover and geitonogamy in Myosotis colensoi (Kirk) Macbride (Boraginaceae). Biol. J. Linn. Soc. , 46, 333–349.
Robertson, A.W. & Lloyd, D.G. (1993). Rates of pollen deposition and removal in Myosotis colonsoi . Funct. Ecol. , 7, 549.
Runquist, R.B. & Stanton, M.L. (2013). Asymmetric and frequency-dependent pollinator-mediated interactions may influence competitive displacement in two vernal pool plants. Ecol. Lett. , 16, 183–190.
Sargent, R.D. (2004). Floral symmetry affects speciation rates in angiosperms. Proc. R. Soc. London. Ser. B Biol. Sci. , 271, 603–608.
Sargent, R.D. & Ackerly, D.D. (2008). Plant-pollinator interactions and the assembly of plant communities. Trends Ecol. Evol. , 23, 123–130.
Sargent, R.D. & Otto, S.P. (2006). The role of local species abundance in the evolution of pollinator attraction in flowering plants. Am. Nat. , 167, 67–80.
Shan, H., Cheng, J., Zhang, R., Yao, X. & Kong, H. (2019). Developmental mechanisms involved in the diversification of flowers.Nat. Plants , 5, 917–923.
Stebbins, G.L. (1970). Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annu. Rev. Ecol. Syst. , 1, 307–326.
Steven, J.C., Rooney, T.P., Boyle, O.D. & Waller, D.M. (2003). Density-dependent pollinator visitation and self-incompatibility in upper Great Lakes populations of Trillium grandiflorum . J. Torrey Bot. Soc. , 130, 23.
Thomson, J. (2003). When Is It Mutualism? Am. Nat. , 162, S1–S9.
Thomson, J.D., Wilson, P., Valenzuela, M. & Malzone, M. (2000). Pollen presentation and pollination syndromes, with special reference toPenstemon . Plant Species Biol. , 15, 11–29.
Thorp, R.W. (2000). The collection of pollen by bees. Plant Syst. Evol. , 222, 211–223.
Thostesen, A.M. & Olesen, J.M. (1996). Pollen removal and deposition by specialist and generalist bumblebees in Aconitum septentrionale .Oikos , 77, 77–84.
Valdovinos, F.S., Brosi, B.J., Briggs, H.M., Moisset de Espanés, P., Ramos-Jiliberto, R. & Martinez, N.D. (2016). Niche partitioning due to adaptive foraging reverses effects of nestedness and connectance on pollination network stability. Ecol. Lett. , 19, 1277–1286.
Vamosi, J.C., Knight, T.M., Steets, J.A., Mazer, S.J., Burd, M. & Ashman, T.L. (2006). Pollination decays in biodiversity hotspots.Proc. Natl. Acad. Sci. U. S. A. , 103, 956–961.
Vázquez, D.P. & Aizen, M.A. (2003). Null model analyses of specialization in plant–pollinator interactions. Ecology , 84, 2493–2501.
Waser, N.M. (1986). Flower constancy: definition, cause, and measurement. Am. Nat. , 127, 593–603.
Waser, N.M., Chittka, L., Price, M. V., Williams, N.M. & Ollerton, J. (1996). Generalization in pollination systems, and why it matters.Ecology , 77, 1043–1060.
Wolfe, L.M. & Barrett, S.C.H. (1989). Patterns of pollen removal and deposition in tristylous Pontederia cordata L. (Pontederiaceae).Biol. J. Linn. Soc. , 36, 317–329.
Ye, Z.M., Jin, X.F., Wang, Q.F., Yang, C.F. & Inouye, D.W. (2017). Nectar replenishment maintains the neutral effects of nectar robbing on female reproductive success of Salvia przewalskii (Lamiaceae), a plant pollinated and robbed by bumble bees. Ann. Bot. , 119, 1053–1059.
Young, H.J. & Stanton, M.L. (1990). Influences of floral variation on pollen removal and seed production in wild radish. Ecology , 71, 536–547.
Table 1. Description of the parameters and parameter values used in the mathematical model