Section: Ecology
Topic:
Ecology,
Evolution
Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off
Corresponding author(s): Yacine, Youssef (youssef-yacine@hotmail.fr)
10.24072/pcjournal.433 - Peer Community Journal, Volume 4 (2024), article no. e60.
Get full text PDF Peer reviewed and recommended by PCIMany plant traits are subject to an ecological trade-off between attracting pollinators and escaping herbivores. The interplay of both plant-animal interaction types determines their evolution. As most studies focus on either pollination or herbivory, how they jointly affect the eco-evolutionary dynamics of plant-animal communities is often left unknown. Within a plant-pollinator-herbivore community where interaction strengths depend on trait matching, we consider the evolution of a plant trait involved in both plant-animal interactions. Using adaptive dynamics, we uncover when stabilizing, runaway (i.e. directional) or disruptive selection emerges and its consequences for multispecies coexistence. We find that strong pollination relative to herbivory favors stabilizing selection and coexistence. Strong herbivory relative to pollination fosters runaway selection and threatens coexistence. Importantly, given balanced interactions, joint effects may lead to disruptive selection, allowing the emergence of plant dimorphism. The strength of the ecological trade-off largely explains the occurrence of these contrasting eco-evolutionary dynamics. In particular, plant diversification requires strong trade-offs, with the strongest trade-offs allowing long-term polymorphism. We discuss how our results relate to various empirical cases where the interplay of pollination and herbivory maintains plant polymorphism. Beyond maintenance, our work suggests that it might also have fueled the diversification process itself.
Type: Research article
Yacine, Youssef 1, 2; Loeuille, Nicolas 1
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TY - JOUR AU - Yacine, Youssef AU - Loeuille, Nicolas TI - Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off JO - Peer Community Journal PY - 2024 VL - 4 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.433/ DO - 10.24072/pcjournal.433 LA - en ID - 10_24072_pcjournal_433 ER -
%0 Journal Article %A Yacine, Youssef %A Loeuille, Nicolas %T Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off %J Peer Community Journal %D 2024 %V 4 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.433/ %R 10.24072/pcjournal.433 %G en %F 10_24072_pcjournal_433
Yacine, Youssef; Loeuille, Nicolas. Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off. Peer Community Journal, Volume 4 (2024), article no. e60. doi : 10.24072/pcjournal.433. https://peercommunityjournal.org/articles/10.24072/pcjournal.433/
PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.ecology.100530
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] Attracting antagonists: Does floral nectar increase leaf herbivory?, Ecology, Volume 85 (2004) no. 6, pp. 1519-1526 | DOI
[2] Reliance on pollinators predicts defensive chemistry across tobacco species, Ecology Letters, Volume 15 (2012) no. 10, pp. 1140-1148 | DOI
[3] Exaptations Link Evolution of Plant-Herbivore and Plant-Pollinator Interactions: A Phylogenetic Inquiry, Ecology, Volume 78 (1997) no. 6, p. 1661 | DOI
[4] Herbivores at the highest risk of extinction among mammals, birds, and reptiles, Science Advances, Volume 6 (2020) no. 32, p. eabb8458 | DOI
[5] The origins of reproductive isolation in plants, New Phytologist, Volume 207 (2015) no. 4, pp. 968-984 | DOI
[6] Macroevolutionary chemical escalation in an ancient plant-herbivore arms race, Proceedings of the National Academy of Sciences of the United States of America, Volume 106 (2009) no. 43, pp. 18062-18066 | DOI
[7] Chemical phenotype matching between a plant and its insect herbivore, Proceedings of the National Academy of Sciences of the United States of America, Volume 95 (1998) no. 23, pp. 13743-13748 | DOI
[8] Plant-herbivore-pollinator ménage-à-trois: tell me how well they match, and I'll tell you if it's made to last, Peer Community in Ecology, 2024 | DOI
[9] Rapid evolution caused by pollinator loss in Mimulus guttatus, Evolution, Volume 65 (2011) no. 9, pp. 2541-2552 | DOI
[10] Effects of Pollinators , Herbivores , and Seed Predators on Flowering Phenology, Ecology, Volume 78 (2008) no. 6, pp. 1624-1631 | DOI
[11] Plant traits that predict resistance to herbivores, Functional Ecology, Volume 25 (2011) no. 2, pp. 358-367 | DOI
[12] How context dependent are species interactions?, Ecology Letters, Volume 17 (2014) no. 7, pp. 881-890 | DOI
[13] Mechanisms of plant competition for nutrients, water and light, Functional Ecology, Volume 27 (2013) no. 4, pp. 833-840 | DOI
[14] Arms races between and within species, Proceedings of the Royal Society B: Biological Sciences, Volume 205 (1979), pp. 489-511 | DOI
[15] Experimental examination of pollinator-mediated selection in a sexually deceptive orchid, Annals of Botany, Volume 123 (2019) no. 2, pp. 347-354 | DOI
[16] Multidimensional (Co)evolutionary stability, American Naturalist, Volume 184 (2014) no. 2, pp. 158-171 | DOI
[17] The dynamical theory of coevolution: a derivation from stochastic ecological processes, Journal of Mathematical Biology, Volume 34 (1996) no. 5-6, pp. 579-612 | DOI
[18] Pollen limitation, seed predation and scape length in Primula farinosa, Oikos, Volume 97 (2002) no. 1, pp. 45-51 | DOI
[19] Timing of flowering: Opposed selection on different fitness components and trait covariation, American Naturalist, Volume 173 (2009) no. 6, pp. 819-830 | DOI
[20] Butterflies and Plants: A Study in Coevolution, Evolution, Volume 18 (1964) no. 4, p. 586 | DOI
[21] Evolutionary and continuous stability, Journal of Theoretical Biology, Volume 103 (1983) no. 1, pp. 99-111 | DOI
[22] Escalation of plant defense: do latex and resin canals spur plant diversification?, American Naturalist, Volume 138 (1991) no. 4, pp. 881-900 | DOI
[23] Plant apparency and chemical defense, Biochemical interaction between plants and insects, Springer, Boston, MA, 1976, pp. 1-40 | DOI
[24] The ecological and evolutionary implications of merging different types of networks, Ecology Letters, Volume 14 (2011) no. 11, pp. 1170-1181 | DOI
[25] Opposing natural selection from herbivores and pathogens may maintain floral-color variation in Claytonia virginica (Portulacaceae), Evolution, Volume 58 (2004) no. 11, pp. 2426-2437 | DOI
[26] Down the tube: Pollinators, predators, and the evolution of flower shape in the alpine skypilot, Polemonium viscosum, Evolution, Volume 55 (2001) no. 10, pp. 1963-1971 | DOI
[27] Dynamics of adaptation and evolutionary branching, Physical Review Letters, Volume 78 (1997) no. 10, pp. 2024-2027 | DOI
[28] Non-additive effects of herbivores and pollinators on Erysimum mediohispanicum (Cruciferae) fitness, Oecologia, Volume 143 (2005) no. 3, pp. 412-418 | DOI
[29] Modeling the continua in the outcomes of biotic interactions, Ecology, Volume 104 (2023) no. 4, p. e3995 | DOI
[30] When does Evolution by Natural Selection Prevent Extinction?, Evolution, Volume 49 (1995) no. 1, pp. 201-207 | DOI
[31] Pollination Systems as Isolating Mechanisms in Angiosperms, Evolution, Volume 3 (1949) no. 1, pp. 82-97 | DOI
[32] Insect egg-killing: a new front on the evolutionary arms-race between brassicaceous plants and pierid butterflies, New Phytologist, Volume 230 (2021) no. 1, pp. 341-353 | DOI
[33] The secret pollinators: an overview of moth pollination with a focus on Europe and North America, Arthropod-Plant Interactions, Volume 10 (2016) no. 1, pp. 21-28 | DOI
[34] More than 75 percent decline over 27 years in total flying insect biomass in protected areas, PLoS ONE, Volume 12 (2017) no. 10 | DOI
[35] Why are there so many flowering plants? A multiscale analysis of plant diversification, American Naturalist, Volume 195 (2020) no. 6, pp. 948-963 | DOI
[36] Spurring plant diversification: Are floral nectar spurs a key innovation?, Proceedings of the Royal Society B: Biological Sciences, Volume 262 (1995) no. 1365, pp. 343-348 | DOI
[37] Predation, apparent competition, and the structure of prey communities, Theoretical Population Biology, Volume 12 (1977) no. 2, pp. 197-229 | DOI
[38] Permanent coexistence in general models of three interacting species, Journal of Mathematical Biology, Volume 21 (1985) no. 3, pp. 285-298 | DOI
[39] The Role of Herbivores in the Maintenance of a Flower Color Polymorphism in Wild Radish, Ecology, Volume 84 (2003) no. 7, pp. 1733-1743 | DOI
[40] Herbivory-mediated pollinator limitation: Negative impacts of induced volatiles on plant-pollinator interactions, Ecology, Volume 92 (2011) no. 9, pp. 1769-1780 | DOI
[41] Models of coevolution and speciation in plants and their pollinators., American Naturalist, Volume 124 (1984) no. 2, pp. 220-243 | DOI
[42] Trade-off geometries and the adaptive dynamics of two co-evolving species, Evolutionary Ecology Research, Volume 8 (2006) no. 6, pp. 959-973
[43] Multilocus genetics and the coevolution of quantitative traits, Evolution, Volume 60 (2006) no. 7, pp. 1321-1336 | DOI
[44] The Limiting Similarity, Convergence, and Divergence of Coexisting Species, The American Naturalist, Volume 101 (1967) no. 921, pp. 377-385 | DOI
[45] An individual-based model for the eco-evolutionary emergence of bipartite interaction networks, Ecology Letters, Volume 23 (2020) no. 11, pp. 1623-1634 | DOI
[46] Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense, Evolution, Volume 51 (1997) no. 5, pp. 1435-1444 | DOI
[47] The logic of animal conflict, Nature, Volume 246 (1973) no. 5427, pp. 15-18 | DOI
[48] Diversity in a complex ecological network with two interaction types, Oikos, Volume 118 (2009) no. 1, pp. 122-130 | DOI
[49] How should we define 'fitness' for general ecological scenarios?, Trends in Ecology and Evolution, Volume 7 (1992) no. 6, pp. 198-202 | DOI
[50] New frontiers in competition for pollination, Annals of Botany, Volume 103 (2009) no. 9, pp. 1403-1413 | DOI
[51] Interspecific pollen transfer: Magnitude, prevalence and consequences for plant fitness, Critical Reviews in Plant Sciences, Volume 27 (2008) no. 4, pp. 221-238 | DOI
[52] Instability of a hybrid module of antagonistic and mutualistic interactions, Population Ecology, Volume 56 (2014) no. 2, pp. 257-263 | DOI
[53] Nectar bat stows huge tongue in its rib cage, Nature, Volume 444 (2006) no. 7120, pp. 701-702 | DOI
[54] How many flowering plants are pollinated by animals?, Oikos, Volume 120 (2011) no. 3, pp. 321-326 | DOI
[55] Agriculture and climate change are reshaping insect biodiversity worldwide, Nature, Volume 605 (2022) no. 7908, pp. 97-102 | DOI
[56] Pollinators exert natural selection on flower size and floral display in Penstemon digitalis, New Phytologist, Volume 188 (2010) no. 2, pp. 393-402 | DOI
[57] Global pollinator declines: Trends, impacts and drivers, Trends in Ecology and Evolution, Volume 25 (2010) no. 6, pp. 345-353 | DOI
[58] Rapid plant evolution driven by the interaction of pollination and herbivory, Science, Volume 364 (2019) no. 6436, pp. 193-196 | DOI
[59] Trait multi-functionality in plant stress response, Integrative and Comparative Biology, Volume 60 (2020) no. 1, pp. 98-112 | DOI
[60] Testing for conflicting and nonadditive selection: Floral adaptation to multiple pollinators through male and female fitness, Evolution, Volume 65 (2011) no. 5, pp. 1457-1473 | DOI
[61] Worldwide decline of the entomofauna: A review of its drivers, Biological Conservation, Volume 232 (2019), pp. 8-27 | DOI
[62] Floral symmetry affects speciation rates in angiosperms, Proceedings of the Royal Society B: Biological Sciences, Volume 271 (2004) no. 1539, pp. 603-608 | DOI
[63] Structure-stability relationships in networks combining mutualistic and antagonistic interactions, Oikos, Volume 123 (2014) no. 3, pp. 378-384 | DOI
[64] Stability of a diamond-shaped module with multiple interaction types, Theoretical Ecology, Volume 9 (2016) no. 1, pp. 27-37 | DOI
[65] How plants connect pollination and herbivory networks and their contribution to community stability, Ecology, Volume 97 (2016) no. 4, pp. 908-917 | DOI
[66] Plant competition, temporal niches and implications for productivity and adaptability to climate change in water-limited environments, Functional Ecology, Volume 27 (2013) no. 4, pp. 886-897 | DOI
[67] Ecological and Evolutionary Consequences of Multispecies Plant-Animal Interactions, Annual Review of Ecology, Evolution, and Systematics, Volume 35 (2004) no. 1, pp. 435-466 | DOI
[68] Direct and ecological costs of resistance to herbivory, Trends in Ecology and Evolution, Volume 17 (2002) no. 6, pp. 278-285 | DOI
[69] Non-pollinator agents of selection on floral traits, Ecology and evolution of flowers, Oxford University Press on Demand, New York, NY, USA, 2006, pp. 120-138 | DOI
[70] Optimal defence theory and flower petal colour predict variation in the secondary chemistry of wild radish, Journal of Ecology, Volume 92 (2004) no. 1, pp. 132-141 | DOI
[71] Stability of ecological communities and the architecture of mutualistic and trophic networks, Science, Volume 329 (2010) no. 5993, pp. 853-856 | DOI
[72] Attracting mutualists and antagonists: Plant trait variation explains the distribution of specialist floral herbivores and pollinators on crops and wild gourds, American Journal of Botany, Volume 101 (2014) no. 8, pp. 1314-1322 | DOI
[73] Variation in interspecific interactions, Annual review of ecology and systematics. Vol. 19, Volume 19 (1988), pp. 65-87 | DOI
[74] The coevolving web of life, American Naturalist, Volume 173 (2009) no. 2, pp. 125-140 | DOI
[75] Eco-evolutionary dynamics further weakens mutualistic interaction and coexistence under population decline, Evolutionary Ecology, Volume 36 (2022) no. 3, pp. 373-387 | DOI
[76] Pollinator shifts drive increasingly long nectar spurs in columbine flowers, Nature, Volume 447 (2007) no. 7145, pp. 706-709 | DOI
[77] Stable coexistence in plant-pollinator-herbivore communities requires balanced mutualistic vs antagonistic interactions, Ecological Modelling, Volume 465 (2022) no. June 2021, p. 109857 | DOI
[78] Codes and supplementary information related to the manuscript "Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off", Zenodo, 2024 | DOI
[79] When Does Coevolution Promote Diversification?, The American Naturalist, Volume 176 (2010) no. 6, pp. 802-817 | DOI
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