Section: Evolutionary Biology
Topic: Ecology, Evolution, Population biology

Interplay between fecundity, sexual and growth selection on the spring phenology of European beech (Fagus sylvatica L.).

10.24072/pcjournal.396 - Peer Community Journal, Volume 4 (2024), article no. e27.

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Background: Plant phenological traits such as the timing of budburst or flowering can evolve on ecological timescales through response to fecundity and viability selection. However, interference with sexual selection may arise from assortative mating. This study aims to investigate how these three components of selection on spring phenology may combine in European beech populations in contrasting environments (high versus low altitude). Methods: we monitored the timing of budburst (TBB) in 339 adult beech trees and estimated their fecundity using spatially explicit mating models. Fecundity selection was infered by regressing fecundities on TBB, while sexual selection was inferred by regressing fecundities on mating opportunities (i.e., TBB mismatch). The correlation between mates for flowering time (i.e., assortative mating) was estimated based on paternity analyses. Morever, TBB and growth were surveyed in 3261 seedlings from 40 families grown planted in a common garden, and viability selection was inferred by regressing growth on TBB. Results: Overall, directional fecundity selection on female fitness favored trees with earlier TBB. Sexual selection acted only on male fitness through assortative mating favoring trees with mean TBB value (stabilizing selection). In the common garden, early budburst was associated with higher seedling growth. The respective intensities of directional and stabilizing selection varied with the environment: at low altitude, directional selection for earlier phenology was modulated by strong assortative mating and by an interaction effect between TBB an size on female fecundity, whereas at high altitude, directional selection for earlier phenology was reinforced by selection through male fecundity. Discussion: This study showed that selection through female fecundity and seedlings growth predominantly selected for earlier TBB, while sexual selection on male fitness through assortative mating modulated this trend. This interplay between fecundity and sexual selection calls for an integrative approach to predict the evolution of spring phenology under a changing climate.

Published online:
DOI: 10.24072/pcjournal.396
Type: Research article
Keywords: budburst phenology, selection gradient, assortative mating, Bateman’s gradient, parentage/paternity analyses, Mixed-Effect Mating Model (MEMM), Fagus sylvatica
Oddou-Muratorio, Sylvie 1, 2; Bontemps, Aurore 1; Gauzere, Julie 1, 3; Klein, Etienne K 4

1 INRAE, URFM, Avignon, France
2 ECOBIOP Université de Pau et des Pays de l’Adour, E2S UPPA, INRAE, ECOBIOP, Saint-Pée-sur-Nivelle, France
3 Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, UK
4 INRAE, BioSp, Avignon, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Oddou-Muratorio, Sylvie and Bontemps, Aurore and Gauzere, Julie and Klein, Etienne K},
     title = {Interplay between fecundity, sexual and growth selection on the spring phenology of {European} beech {(\protect\emph{Fagus} sylvatica} {L.).}},
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Oddou-Muratorio, Sylvie; Bontemps, Aurore; Gauzere, Julie; Klein, Etienne K. Interplay between fecundity, sexual and growth selection on the spring phenology of European beech (Fagus sylvatica L.).. Peer Community Journal, Volume 4 (2024), article  no. e27. doi : 10.24072/pcjournal.396.

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100657

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] Akaike, H. Factor Analysis and AIC, Springer Series in Statistics, Springer New York, New York, NY, 1987, pp. 371-386 | DOI

[2] Alberto, F. J.; Aitken, S. N.; Alía, R.; González-Martínez, S. C.; Hänninen, H.; Kremer, A.; Lefèvre, F.; Lenormand, T.; Yeaman, S.; Whetten, R.; Savolainen, O. Potential for evolutionary responses to climate change - evidence from tree populations, Global Change Biology, Volume 19 (2013) no. 6, pp. 1645-1661 | DOI

[3] Alexandre, H.; Truffaut, L.; Klein, E.; Ducousso, A.; Chancerel, E.; Lesur, I.; Dencausse, B.; Louvet, J. M.; Nepveu, G.; Torres-Ruiz, J. M.; Lagane, F.; Musch, B.; Delzon, S.; Kremer, A. How does contemporary selection shape oak phenotypes?, Evolutionary Applications, Volume 13 (2020) no. 10, pp. 2772-2790 | DOI

[4] Augspurger, C. K. Reconstructing patterns of temperature, phenology, and frost damage over 124 years: Spring damage risk is increasing, Ecology, Volume 94 (2013) no. 1, pp. 41-50 | DOI

[5] Austen, E. J.; Rowe, L.; Stinchcombe, J. R.; Forrest, J. R. Explaining the apparent paradox of persistent selection for early flowering, New Phytologist, Volume 215 (2017) no. 3, pp. 929-934 | DOI

[6] Austen, E. J.; Weis, A. E. Estimating selection through male fitness: three complementary methods illuminate the nature and causes of selection on flowering time, Proceedings of the Royal Society B: Biological Sciences, Volume 283 (2016) no. 1825 | DOI

[7] Bateman, A. Intra-sexual selection in Drosophila, Heredity, Volume 2 (1948), pp. 349-368 | DOI

[8] Bates, D.; Mächler, M.; Bolker, B. M.; Walker, S. C. Fitting linear mixed-effects models using lme4, Journal of Statistical Software, Volume 67 (2015) no. 1 | DOI

[9] Bigler, C.; Bugmann, H. Climate-induced shifts in leaf unfolding and frost risk of European trees and shrubs, Scientific Reports, Volume 8 (2018) no. 1 | DOI

[10] Bontemps, A.; Davi, H.; Lefèvre, F.; Rozenberg, P.; Oddou-Muratorio, S. How do functional traits syndromes covary with growth and reproductive performance in a water-stressed population of Fagus sylvatica?, Oikos, Volume 126 (2017) no. 10, pp. 1472-1483 | DOI

[11] Burnham, K. P.; Anderson, D. R. Model Selection and Multimodel Inference, Springer New York, New York, NY, 2004 | DOI

[12] Cailleret, M.; Davi, H. Effects of climate on diameter growth of co-occurring Fagus sylvatica and Abies alba along an altitudinal gradient, Trees, Volume 25 (2011) no. 2, pp. 265-276 | DOI

[13] Chuine, I.; Beaubien, E. G. Phenology is a major determinant of tree species range, Ecology Letters, Volume 4 (2001) no. 5, pp. 500-510 | DOI

[14] Collet, C.; Le Moguedec, G. Individual seedling mortality as a function of size, growth and competition in naturally regenerated beech seedlings, Forestry, Volume 80 (2007) no. 4, pp. 359-370 | DOI

[15] Davi, H.; Gillmann, M.; Ibanez, T.; Cailleret, M.; Bontemps, A.; Fady, B.; Lefèvre, F. Diversity of leaf unfolding dynamics among tree species: New insights from a study along an altitudinal gradient, Agricultural and Forest Meteorology, Volume 151 (2011) no. 12, pp. 1504-1513 | DOI

[16] Davi, H.; Cailleret, M. Assessing drought-driven mortality trees with physiological process-based models, Agricultural and Forest Meteorology, Volume 232 (2017), pp. 279-290 | DOI

[17] Donohue, K.; Burghardt, L. T.; Runcie, D.; Bradford, K. J.; Schmitt, J. Applying developmental threshold models to evolutionary ecology, Trends in Ecology and Evolution, Volume 30 (2015) no. 2, pp. 66-77 | DOI

[18] Franjic, J.; Sever, K.; Bogdan, S.; Krstonosic, D.; Aleskovic, I. Phenological asynchronization as a restrictive factor of efficient pollination in clonal seed orchards of Pedunculate Oak (Quercus robur L.)., Croatian Journal of Forest Engineering, Volume 32 (2011), pp. 141-156

[19] Franks, S. J.; Sim, S.; Weis, A. E. Rapid evolution of flowering time by an annual plant in response to a climate fluctuation, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 4, pp. 1278-1282 | DOI

[20] Gauzere, J.; Klein, E. K.; Brendel, O.; Davi, H.; Oddou-Muratorio, S. Using partial genotyping to estimate the genetic and maternal determinants of adaptive traits in a progeny trial of Fagus sylvatica, Tree Genetics and Genomes, Volume 12 (2016) no. 6, pp. 1-13 | DOI

[21] Gauzere, J.; Klein, E. K.; Brendel, O.; Davi, H.; Oddou‐Muratorio, S. Microgeographic adaptation and the effect of pollen flow on the adaptive potential of a temperate tree species, New Phytologist, Volume 227 (2020) no. 2, pp. 641-653 | DOI

[22] Gauzere, J.; Teuf, B.; Davi, H.; Chevin, L.-M.; Caignard, T.; Leys, B.; Delzon, S.; Ronce, O.; Chuine, I. Where is the optimum? Predicting the variation of selection along climatic gradients and the adaptive value of plasticity. A case study on tree phenology, Evolution Letters, Volume 4 (2020) no. 2, pp. 109-123 | DOI

[23] Gauzere, J.; Klein, E. K.; Oddou-Muratorio, S. Ecological determinants of mating system within and between three Fagus sylvatica populations along an elevational gradient, Molecular Ecology, Volume 22 (2013) no. 19, pp. 5001-5015 | DOI

[24] Geber, M. A.; Griffen, L. R. Inheritance and Natural Selection on Functional Traits, International Journal of Plant Sciences, Volume 164 (2003) no. S3, p. S21-S42 | DOI

[25] Gerard, P. R.; Klein, E. K.; Austerlitz, F.; Fernandez-Manjarres, J. F.; Frascaria-Lacoste, N. Assortative mating and differential male mating success in an ash hybrid zone population, BMC Evolutionary Biology, Volume 6 (2006) no. 1 | DOI

[26] Gleiser, G.; Chybicki, I. J.; González-Martínez, S. C.; Aizen, M. A. Phenological match drives pollen-mediated gene flow in a temporally dimorphic tree, Plant Biology, Volume 20 (2018) no. 1, pp. 93-100 | DOI

[27] Godineau, C.; Ronce, O.; Devaux, C. Assortative mating can help adaptation of flowering time to a changing climate: Insights from a polygenic model, Journal of Evolutionary Biology (2021) no. March, pp. 1-18 | DOI

[28] Grime, J. P. Evidence for the Existence of Three Primary Strategies in Plants and Its Relevance to Ecological and Evolutionary Theory, The American Naturalist, Volume 111 (1977) no. 982, pp. 1169-1194 | DOI

[29] Grubb, P. J. A reassessment of the strategies of plants which cope with shortages of resources, Perspectives in Plant Ecology, Evolution and Systematics, Volume 1 (1998) no. 1, pp. 3-31 | DOI

[30] Hacket-Pain, A. J.; Ascoli, D.; Vacchiano, G.; Biondi, F.; Cavin, L.; Conedera, M.; Drobyshev, I.; Liñán, I. D.; Friend, A. D.; Grabner, M.; Hartl, C.; Kreyling, J.; Lebourgeois, F.; Levanič, T.; Menzel, A.; van der Maaten, E.; van der Maaten-Theunissen, M.; Muffler, L.; Motta, R.; Roibu, C. C.; Popa, I.; Scharnweber, T.; Weigel, R.; Wilmking, M.; Zang, C. S. Climatically controlled reproduction drives interannual growth variability in a temperate tree species, Ecology Letters, Volume 21 (2018) no. 12, pp. 1833-1844 | DOI

[31] Hamann, E.; Weis, A. E.; Franks, S. J. Two decades of evolutionary changes in Brassica rapa in response to fluctuations in precipitation and severe drought, Evolution (2018), pp. 2682-2696 | DOI

[32] Hardy, O. J.; Delaide, B.; Hainaut, H.; Gillet, J. F.; Gillet, P.; Kaymak, E.; Vankerckhove, N.; Duminil, J.; Doucet, J. L. Seed and pollen dispersal distances in two African legume timber trees and their reproductive potential under selective logging, Molecular Ecology, Volume 28 (2019) no. 12, pp. 3119-3134 | DOI

[33] Hartmann, H.; Bastos, A.; Das, A. J.; Esquivel-Muelbert, A.; Hammond, W. M.; Martínez-Vilalta, J.; Mcdowell, N. G.; Powers, J. S.; Pugh, T. A.; Ruthrof, K. X.; Allen, C. D. Climate Change Risks to Global Forest Health: Emergence of Unexpected Events of Elevated Tree Mortality Worldwide, Annual Review of Plant Biology, Volume 73 (2022), pp. 673-702 | DOI

[34] Ismail, S. A.; Kokko, H. An analysis of mating biases in trees, Molecular Ecology, Volume 29 (2020) no. 1, pp. 184-198 | DOI

[35] Jean, F.; Davi, H.; Oddou-Muratorio, S.; Fady, B.; Scotti, I.; Scotti-Saintagne, C.; Ruffault, J.; Journe, V.; Clastre, P.; Marloie, O.; Brunetto, W.; Correard, M.; Gilg, O.; Pringarbe, M.; Rei, F.; Thevenet, J.; Turion, N.; Pichot, C. A 14-year series of leaf phenological data collected for European beech (Fagus sylvatica L.) and silver fir (Abies alba Mill.) from their geographic range margins in south-eastern France, Annals of Forest Science, Volume 80 (2023) no. 1 | DOI

[36] Jiang, Y.; Bolnick, D. I.; Kirkpatrick, M. Assortative mating in animals, American Naturalist, Volume 181 (2013) no. 6 | DOI

[37] Keenan, T. F.; Gray, J.; Friedl, M. A.; Toomey, M.; Bohrer, G.; Hollinger, D. Y.; Munger, J. W.; O'Keefe, J.; Schmid, H. P.; Wing, I. S.; Yang, B.; Richardson, A. D. Net carbon uptake has increased through warming-induced changes in temperate forest phenology, Nature Climate Change, Volume 4 (2014) no. 7, pp. 598-604 | DOI

[38] Kingsolver, J. G.; Hoekstra, H. E.; Hoekstra, J. M.; Berrigan, D.; Vignieri, S. N.; Hill, C. E.; Hoang, A.; Gibert, P.; Beerli, P. The Strength of Phenotypic Selection in Natural Populations, The American Naturalist, Volume 157 (2001) no. 3, pp. 245-261 | DOI

[39] Kirkpatrick, M. Reinforcement and divergence under assortative mating, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 267 (2000) no. 1453, pp. 1649-1655 | DOI

[40] Lagache, L.; Klein, E. K.; Ducousso, A.; Petit, R. J. Distinct male reproductive strategies in two closely related oak species, Molecular Ecology, Volume 23 (2014) no. 17, pp. 4331-4343 | DOI

[41] Lamarins, A.; Fririon, V.; Folio, D.; Vernier, C.; Daupagne, L.; Labonne, J.; Buoro, M.; Lefèvre, F.; Piou, C.; Oddou-Muratorio, S. Importance of interindividual interactions in eco-evolutionary population dynamics: The rise of demo-genetic agent-based models, Evolutionary Applications, Volume 15 (2022) no. 12, pp. 1988-2001 | DOI

[42] Lande, R.; Arnold, S. J. The Measurement of Selection on Correlated Characters, Evolution, Volume 37 (1983) no. 6, p. 1210 | DOI

[43] Lander, T. A.; Oddou-Muratorio, S.; Prouillet-Leplat, H.; Klein, E. K. Reconstruction of a beech population bottleneck using archival demographic information and Bayesian analysis of genetic data, Molecular Ecology, Volume 20 (2011) no. 24, pp. 5182-5196 | DOI

[44] Larue, C.; Klein, E. K.; Petit, R. J. Sexual interference revealed by joint study of male and female pollination success in chestnut, Molecular Ecology (2022) no. October 2022, pp. 1211-1228 | DOI

[45] Lenz, A.; Hoch, G.; Vitasse, Y.; Körner, C. European deciduous trees exhibit similar safety margins against damage by spring freeze events along elevational gradients, New Phytologist, Volume 200 (2013) no. 4, pp. 1166-1175 | DOI

[46] Mazerolle, M. J. Package ‘AICcmodavg', R package, 2020 (

[47] Meier, M.; Vitasse, Y.; Bugmann, H.; Bigler, C. Phenological shifts induced by climate change amplify drought for broad-leaved trees at low elevations in Switzerland, Agricultural and Forest Meteorology, Volume 307 (2021) | DOI

[48] Menzel, A.; Sparks, T. H.; Estrella, N.; Koch, E.; Aaasa, A.; Ahas, R.; Alm-Kübler, K.; Bissolli, P.; Braslavská, O.; Briede, A.; Chmielewski, F. M.; Crepinsek, Z.; Curnel, Y.; Dahl, Å.; Defila, C.; Donnelly, A.; Filella, Y.; Jatczak, K.; Måge, F.; Mestre, A.; Nordli, Ø.; Peñuelas, J.; Pirinen, P.; Remišová, V.; Scheifinger, H.; Striz, M.; Susnik, A.; Van Vliet, A. J.; Wielgolaski, F. E.; Zach, S.; Zust, A. European phenological response to climate change matches the warming pattern, Global Change Biology, Volume 12 (2006) no. 10, pp. 1969-1976 | DOI

[49] Merilä, J.; Hendry, A. P. Climate change, adaptation, and phenotypic plasticity: The problem and the evidence, Evolutionary Applications, Volume 7 (2014) no. 1, pp. 1-14 | DOI

[50] Monthe, F. K.; Hardy, O. J.; Doucet, J. L.; Loo, J.; Duminil, J. Extensive seed and pollen dispersal and assortative mating in the rain forest tree Entandrophragma cylindricum (Meliaceae) inferred from indirect and direct analyses, Molecular Ecology, Volume 26 (2017) no. 19, pp. 5279-5291 | DOI

[51] Moore, J. C.; Pannell, J. R. Sexual selection in plants, Current Biology, Volume 21 (2011) no. 5, p. R176-R182 | DOI

[52] Munguía-Rosas, M. A.; Ollerton, J.; Parra-Tabla, V.; De-Nova, J. A. Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured, Ecology Letters, Volume 14 (2011) no. 5, pp. 511-521 | DOI

[53] Nielsen, P. C.; Schaffalitzky de Muckadell, M. Flower observations and controlled pollinations in Fagus, Silvae Genetica, Volume 3 (1954), pp. 6-17

[54] Nilsson, J. E. Genetic variation in the natural pollen cloud of pinus sylvestris: A study based on progeny testing, Scandinavian Journal of Forest Research, Volume 10 (1995) no. 1-4, pp. 140-148 | DOI

[55] Oddou-Muratorio, S.; Gauzere, J.; Angeli, N.; Brahic, P.; Brendel, O.; De Castro, M.; Gilg, O.; Hossann, C.; Jean, F.; Lingrand, M.; Pringarbe, M.; Rei, F.; Roig, A.; Thevenet, J.; Turion, N. Phenotypic and genotypic data of a European beech (Fagus sylvatica L.) progeny trial issued from three plots along an elevation gradient in Mont Ventoux, South-Eastern France, Annals of Forest Science, Volume 78 (2021) no. 4, p. 88 | DOI

[56] Oddou-Muratorio, S.; Houot, M. L.; Demesure-Musch, B.; Austerlitz, F. Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. I. Evaluating the paternity analysis procedure in continuous populations, Molecular Ecology, Volume 12 (2003) no. 12, pp. 3427-3439 | DOI

[57] Oddou-Muratorio, S.; Gauzere, J.; Bontemps, A.; Rey, J.; Klein, E. K. Tree, sex and size: Ecological determinants of male vs. female fecundity in three Fagus sylvatica stands, Molecular Ecology, Volume 27 (2018) no. 15, pp. 3131-3145 | DOI

[58] Oddou-Muratorio, S.; Davi, H. Simulating local adaptation to climate of forest trees with a Physio-Demo-Genetics model, Evolutionary Applications, Volume 7 (2014) no. 4, pp. 453-467 | DOI

[59] Oddou-Muratorio, S.; Bontemps, A.; Gauzere, J.; Klein, E. Data for the manuscript “Intertwining of fecundity, sexual and growth selection on spring phenology along an altitudinal gradient of European beech (Fagus sylvatica L.).”, Recherche Data Gouv, V1, UNF:6:lKz/a8jcVz3IK2n79tnAiA== [fileUNF], 2023 | DOI

[60] Packham, J. R.; Thomas, P. A.; Atkinson, M. D.; Degen, T. Biological Flora of the British Isles: Fagus sylvatica, Journal of Ecology, Volume 100 (2012) no. 6, pp. 1557-1608 | DOI

[61] Palacio-Lopez, K.; King, C. M.; Bloomberg, J.; Hovick, S. M. Natural selection on traits and trait plasticity in Arabidopsis thaliana varies across competitive environments, Scientific Reports, Volume 10 (2020) no. 1, pp. 1-14 | DOI

[62] Parmesan, C.; Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems, Nature, Volume 421 (2003) no. 6918, pp. 37-42 | DOI

[63] Richardson, A. D.; Bailey, A. S.; Denny, E. G.; Martin, C. W.; O'Keefe, J. Phenology of a northern hardwood forest canopy, Global Change Biology, Volume 12 (2006) no. 7, pp. 1174-1188 | DOI

[64] Servedio, M. R.; Doorn, G. S. V.; Kopp, M.; Frame, A. M.; Nosil, P. Magic traits in speciation: 'magic' but not rare?, Trends in Ecology and Evolution, Volume 26 (2011) no. 8, pp. 389-397 | DOI

[65] Soularue, J. P.; Firmat, C.; Caignard, T.; Thöni, A.; Arnoux, L.; Delzon, S.; Ronce, O.; Kremer, A. Antagonistic Effects of Assortative Mating on the Evolution of Phenotypic Plasticity along Environmental Gradients, American Naturalist, Volume 202 (2023) no. 1, pp. 18-39 | DOI

[66] Soularue, J.-P.; Kremer, A. Assortative mating and gene flow generate clinal phenological variation in trees, BMC Evolutionary Biology, Volume 12 (2012) no. 1 | DOI

[67] Soularue, J.-P.; Kremer, A. Evolutionary responses of tree phenology to the combined effects of assortative mating, gene flow and divergent selection, Heredity, Volume 113 (2014) no. 6, pp. 485-494 | DOI

[68] Tonnabel, J.; David, P.; Pannell, J. R. Do metrics of sexual selection conform to Bateman's principles in a wind-pollinated plant?, Proceedings of the Royal Society B: Biological Sciences, Volume 286 (2019) no. 1905 | DOI

[69] Vitasse, Y. Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier, New Phytologist, Volume 198 (2013) no. 1, pp. 149-155 | DOI

[70] Weis, A. E.; Nardone, E.; Fox, G. A. The strength of assortative mating for flowering date and its basis in individual variation in flowering schedule, Journal of Evolutionary Biology, Volume 27 (2014) no. 10, pp. 2138-2151 | DOI

[71] Weis, A. E.; Winterer, J.; Vacher, C.; Kossler, T. M.; Young, C. A.; LeBuhn, G. L. Phenological assortative mating in flowering plants: The nature and consequences of its frequency dependence, Evolutionary Ecology Research, Volume 7 (2005) no. 2, pp. 161-181

[72] Whittet, R.; Cavers, S.; Cottrell, J.; Rosique-Esplugas, C.; Ennos, R. Substantial variation in the timing of pollen production reduces reproductive synchrony between distant populations of Pinus sylvestris L. in Scotland, Ecology and Evolution, Volume 7 (2017) no. 15, pp. 5754-5765 | DOI

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