Plasticity versus phylogenetic restrictions in flowering time of coexisting species in experimental annual plant assemblages

Plasticity versus phylogenetic restrictions in flowering time of coexisting species in experimental annual plant assemblages | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Plasticity versus phylogenetic restrictions in flowering time of coexisting species in experimental annual plant assemblages Rocío Chaves, Alicia Montesinos-Navarro, Pablo Ferrandis, Arantzazu L. Luzuriaga This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5980745/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 24 Jul, 2025 Read the published version in Scientific Reports → Version 1 posted 10 You are reading this latest preprint version Abstract Flowering timing is a critical event in the lifetime of angiosperms, being particularly sensitive to environmental conditions, although the range of flowering response should be ultimately constrained by evolutionary history. We hypothesized that a) if phylogenetic constraints prevail over phenotypic plasticity in the expression of flowering phenology, flowering peaks would be more segregated in diverse assemblages than in assemblages composed of close relatives; b) conversely, if flowering time is mainly a plastic trait, drought would induce significant flowering overlap, irrespective of the phylogenetic diversity in the assemblage. We designed assemblages with annual plants of semiarid systems of Spain, considering two contrasted levels of phylogenetic diversity (PD) and two water availability treatments in a common garden experiment, where we analysed the flowering segregation among species. High PD assemblages resulted in greater flowering overlap, while assemblages composed of close relatives segregated more their flowering peaks. Water stress triggered flowering synchronization both in neighborhoods with high and low phylogenetic diversity. Our findings corroborate that in the very diverse Iberian gypsophilous annual plant communities, it is phenotypic plasticity in response to water availability, rather than phylogenetic constraints what modulates species segregation of flowering phenology, potentially affecting species coexistence. Earth and environmental sciences/Ecology/Community ecology Earth and environmental sciences/Ecology/Biodiversity Earth and environmental sciences/Ecology/Climate change ecology/Phenology Common garden drought flowering phenology gypsum niche complementarity phenotipic plasticity phylogenetic diversity species assembly species coexistence Figures Figure 1 Introduction Flowering time is a crucial event in the lifetime of angiosperms that has critical impacts on plant fitness. If flowering occurs too early in the growing season, late frosts could damage floral tissues, or pollinators may not yet be abundant enough to ensure fertilization, or plant size may constrain total flower production. However, if flowering occurs too late, environmental conditions may not be favorable for seed maturation or dispersal or may leave the offspring in harsh conditions to survive (Bernal et al., 2011 ; Montesinos-Navarro et al., 2011 , Bucher & Romermann 2020). Flowering time is determined by a trade-off among water availability (Shavrukov et al., 2017 ) temperature (Cleland et al., 2012; Jagadish et al., 2016 ), photoperiod (Johanson, 2014), and the moment of germination (Rathcke & Lacey, 1985 ). External environmental conditions are linked to a complex set of endogenous molecular pathways that trigger flowering time (Lee et al., 2023 ). In arid and semiarid systems, where unpredictable droughts occur, soil water availability is known to be a critical driver of plant growth and plant community dynamics (Peñuelas et al., 2004 , Peralta et al., 2019 ; Luzuriaga et al., 2012 , 2020 ; Sánchez et al., 2022 ). Low water availability has been linked to acceleration in flowering timing, especially in annual plants (Fitter & Fitter, 2002 ; Kigel et al., 2011 ), which has been interpreted as a drought escape response to complete phenology prior to environment becoming too harsh for plant survival (Franks, 2011 ). Flowering time is associated with the period of maximum vegetative biomass (Mooney et al., 1986 ; Cleland et al., 2006 ; Sun & Frelich, 2011 ), indicating high resource uptake. Indeed, several studies suggest that phenology can serve as a proxy for temporal resource use in plants (Davies et al., 2010; Craine et al., 2012 ; Montesinos-Navarro, 2023 ). It is expected that co-occurring species are more likely to coexist if their phenology is segregated because of a reduction of interspecific competition (Chase & Laibold, 2003 ; Chesson et al., 2004 ). Furthermore, phenological segregation has recently been demonstrated to be a plausible driver of community structure by enabling nitrogen transfer between plants in different phenological stages (Montesinos-Navarro, 2023 ). In communities where coexisting species flower concurrently, species performance may benefit from overlapping flowering periods due to the attraction of a larger number and greater diversity of pollinators (Moeller, 2004 ; Ricketts et al., 2008 ; Lázaro et al., 2009 ). However, co-flowering species might also face increased competition for pollinators, potentially reducing the frequency of pollinator visits (Elzinga et al., 2007 ; Mitchell et al., 2009 ; Pauw, 2013 ), as well as competition for shared abiotic resources. Consequently, the aggregation versus segregation of flowering phenology can alter plant-plant interactions among coexisting species (Strauss et al., 2021 ), ultimately influencing the species assembly process. In the last two decades, community ecologists have focused their attention on phylogenetic patterns in order to unveil ecological processes underlying coexistence (Webb et al., 2002 ). Phylogenetic diversity (PD, hereinafter) measures the degree of evolutionary relatedness among species of a community (Faith, 1992 ). It provides a valuable measure of biodiversity because it integrates the evolutionary history of species with their ecological requirements (Ackerly, 2003 ; Cavender-Bares et al., 2009 ; Srivastava et al., 2012 ; Gerhold et al., 2015 ) and it can inform on the main ecological processes involved in the species assembly (Webb et al., 2002 ; Emerson & Gillespie, 2008 ; Lemos-Costa et al., 2024 ). Many authors have analyzed phylogenetic relatedness observed in local communities to infer ecological processes that can influence the community structure ( i. e. , phylogenetic response) (Godoy et al., 2014 ; López-Angulo et al., 2018 ; Luzuriaga et al., 2020 ). Phylogenetic convergence is usually related to habitat filtering processes (Webb et al., 2002 ) and to competitive exclusion processes when a phylogenetically conserved trait promoting survival is selected by environmental constraints (Mayfield & Levine, 2010 ). Phylogenetic overdispersion in assemblages (phylogenetic divergence) is usually associated with nurse-mediated facilitation (Valiente-Banuet & Verdú, 2007 ), and competitive exclusion interactions between close relatives with the same niche-use (Webb et al., 2002 ; Slinghsby & Verboom, 2006). Phylogenetic divergence, however, also occurs when distantly related taxa converge on similar niche-use (Cavender-Bares et al., 2004 ; Kembel & Hubbell, 2006 ; Swenson et al., 2006 ; Kraft et al., 2007 ). Integrating knowledge on how flowering timing is influenced by community-level patterns, such as phylogenetic diversity, and how flowering timing, in turn, affects species coexistence within the community, is crucial for understanding the assembly of plant communities and for predicting how they will respond to ongoing climate change. Although flowering timing is a ductile trait particularly sensitive to both abiotic and biotic environmental signals, plant species have a range in the flowering response which should be ultimately determined by their evolutionary history. To what extent plasticity vs. phylogeny determines phenological segregation is a key question to understand assembly mechanisms organizing plant communities. From a community perspective, few studies have manipulated the phylogenetic diversity of experimental assemblages (see Feng et al., 2019 , and Galland et al., 2019 ) and even fewer have done so to evaluate the causal effect of phylogenetic diversity of assemblages as driver of the assembly processes (see Chaves et al., 2021 ; Ortiz et al., 2023 ). We build on our previous study (Chaves et al., 2021 ), that established that under drought conditions, phylogenetically diverse assemblages of Iberian gypsophilous annual plants resulted in higher plant survival and fitness than neighborhoods composed of closely related species, to explore potential mechanisms driven by plant phenology. The phylogenetic diversity of species assemblages seems to be a driving force of the assembly process, being the niche complementarity among species a central process organizing the community (Webb et al., 2002 ; Pausas & Verdú, 2010 ; Chaves et al., 2021 ), however a better understanding of the underlying mechanisms is required to improve our predictions on how communities will change under different conditions. In this study, we aimed to evaluate if differences in flowering time of coexisting species could be a key driver of niche complementarity in the communities of annual plants growing in gypsum soils. To pursue this aim, we monitored the flowering phenology of plants in a common garden experiment, where the initial phylogenetic diversity of species assemblages together with water availability were manipulated. We hypothesize that, in a scenario where flowering time is, to some extent, evolutionarily conserved, flowering segregation will be higher in phylogenetically diverse assemblages compared to assemblages with close relatives, especially under drought conditions in which competition avoidance might be even more relevant for succeeding. However, in the opposite scenario, where flowering time of species is highly plastic, we expect a reduction of the temporal segregation (i.e., greater flowering overlap) under drought conditions, both in high and low PD assemblages, thus flowering acceleration can be a response to escape from water stress in unpredictable systems. Materials and methods The target annual plant community of this study grows on gypsum soils in the Tagus valley, central Spain. The climate in the area is semiarid Mediterranean with mean annual temperatures around 14.5°C and mean annual precipitation of 400 mm, specially distributed in the late autumn and early spring (Aranjuez weather station, 40°4′2′′N; 3°32′46′′W, 540 m). The habitat comprises a gypsum steppe, where gypsophilous dwarf shrubs (e.g., Lepidium subulatum L., Centaurea hyssopifolia Vahl, Gypsophila struthium L., Helianthemum squamatum (L.) Dum. Cours., Thymus lacaitae Pau, Herniaria fruticosa L., and Frankenia thymifolia Desf.) are patchily scattered along with Macrochloa tenacissima (L.) Kunth grass tussocks on a matrix of bare soil with a well-developed biological crust dominated by lichens (e.g., Diploschistes diacapsis (Ach.) Lumbsch, Squamarina lentigera (G.H. Weber) Poelt, Fulgensia subbracteata (Nyl.) Poelt, and Psora decipiens (Hedw.) Hoffm). From October to July a seasonally dynamic, rich community of annual plants proliferates. They remain in seed form the rest of the year by accumulating dense and well-structured seed banks in the soil (Caballero et al., 2008 ; Martínez-Duro et al., 2012 ; Peralta et al., 2016 ). The regional species pool is composed of nearly 120 species (Luzuriaga et al 2018 ), with up to 38 plant species/0.25 m 2 in rainy years (Luzuriaga et al., 2012 ; 2015 ). Relevant examples are Campanula fastigiata Dufour ex A. DC., Chaenorhinum reyesii (C. Vicioso & Pau) Benedí, Asterolinon linum-stellatum (L.) Duby in DC., Campanula erinus L., Galium parisiense L., Helianthemum salicifolium (L.) Miller., Micropyrum tenellum (L.) Link, Bromus rubens L., Lomelosia stellata (L.) Raf. and Pistorinia hispanica (L.) DC. We used data collected from the experiment described in Chaves et al. ( 2021 ) in which we manipulated the initial phylogenetic diversity of experimental assemblages in a common garden approach in the greenhouse. We aimed to evaluate the causal effect of phylogenetic diversity on flowering phenology of annual plant assemblages. This approach has rarely been attempted with vascular plants to the best of our knowledge (but see Feng et al., 2019 ; Galland et al., 2019 ). To determine the initial levels of phylogenetic diversity of each assemblage, we prepared a phylogenetic tree (see Chaves et al., 2021 ) using phylo.maker function of “V.Phylomaker” package (Jin & Qian, 2019 ), and to calculate indices we used the packages “ape” (Paradis & Schliep, 2018 ) and “picante” (Kembel et al., 2010 ) in software R ( http://www.R-project.org ). We calculated the phylogenetic species variability (PSV) index (Helmus et al., 2007 ) and the standardized effect size of mean pairwise distances in communities index (SES.MPD). The PSV index, bounded between 0 and 1, indicates the degree of relatedness among different species in a community. Values close to zero imply very low PD, while values close to one represent maximum PD. The SES.MPD index measures the mean phylogenetic distance between pairs of species and contrasts it to 1000 null species assemblages from the phylogenetic community tree. High positive values imply larger mean phylogenetic distance than the null model, thus phylogenetic dispersal, while high negative values indicate lower mean phylogenetic distance than the null model, thus phylogenetic convergence. To create species assemblages, we collected seeds of annual plants along the Tagus valley during the springs of 2016 and 2017. Annual plant communities from Mediterranean gypsum soils provide a useful model system to conduct manipulative experiments to determine mechanisms involved in the assembly of communities, because they comprise a rich regional species pool (over 120 taxa) of ephemeral, small-sized species, with short and highly synchronized life cycles (October-early June), which overall allow to perform, handle, and complete common garden experiments in small spaces and short time lapses ( see Luzuriaga et al., 2012 ; 2015 ; 2018 ; Peralta et al., 2016 ; 2019 ; Chaves et al., 2021 ; Sánchez et al., 2022 ). Experimental assemblages were formed by four combinations of seven different species: two combinations with low PD and two with high PD. Two taxonomic scenarios with high phylogenetic diversity were composed of Poaceae, Crassulaceae, Apiaceae and Caryophylaceae families (PSV = 0.82 and 0.85; SES.MPD = 0.53 and 0.17) and two taxonomic scenarios with low PD, one composed of Asteraceae species (PSV = 0.24; SES.MPD = − 9.6; p < 0.001) and another one made up of Brassicales and Malvales (PSV = 0.64; SES.MPD = − 2.5; p < 0.05). Replication of taxonomic scenarios allows to control for the effects of taxonomic identity. Two irrigation treatments were applied, differing in the amount of water applied. We calculated the average monthly precipitation recorded between 1981 and 2010 in the area of our study system (Getafe weather station, 40°18.0′ N, 3° 43.2′ W, 620 masl) and we applied it to pots manually, distributing the corresponding amount twice a week, being this the average irrigation treatment. To simulate an intense drought, we reduced the watering to 33% of that in the Average treatment (Drought treatment). We established a fully crossed factorial design with two phylogenetic diversity levels × two taxonomic combinations of species × two water availability treatments (eight experimental scenarios). Each experimental scenario was replicated in 10 to 16 units, thereby resulting in 110 experimental assemblages (pots). The experiment was set up in October 2017, thus synchronized with the natural life cycle of annual plants, at the Rey Juan Carlos University greenhouse ( https://urjc-cultive.webnode.es ; Móstoles, Madrid, Spain: 40°20′2′′N, 3°52′00′′W, 650 masl). We filled round plastic pots with a diameter of 30 cm and depth of 10 cm with 5 kg of seed-free gypsum soil from a gypsum quarry near to the natural habitat of the study species. Seventy seeds per species were sown in each pot and excess seedlings were removed until we obtained 10 stablished individuals per each of the seven species per pot. Plants persisted as seedlings during all winter, as naturally occurs in the field, and in February, the experimental irrigation and periodic monitoring of plants started. Between February and June (the natural growing season for annual plants in gypsum systems; Luzuriaga et al., 2012 ; 2015 ), we monitored the number of flowering plants per species and pot weekly. We calculated the time of flowering peak for each species in each pot by assigning the ordinal number of the week in which we censed the highest number of flowering plants of that species in that pot. We evaluated the floral phenology at the community level based on the flowering segregation index per pot. Each pot was characterized by a single value of the flowering segregation index. This index consists of the mean pairwise distances of the flowering peaks between every species in each pot (measured in number of days). Flowering segregation informs on the degree of flowering overlap among species in each species assemblage (de Avila & Pinheiro, 2021 ). High values of segregation imply large temporal differences in flowering peaks among co-occurring species in each pot and low values imply synchronized or aggregated flowering peaks among coexisting species. Statistical analyses We performed a nested linear model to analyze whether the flowering segregation index (dependent variable), was influenced by the experimentally manipulated initial phylogenetic diversity (two levels, high and low PD), taxonomic composition (two taxonomic compositions per level of PD) and water irrigation (two levels, Average and Drought treatments) (explanatory variables). The variable taxonomic composition was nested within the phylogenetic diversity treatment to control differences associated with species identities. Following recommendations of Zuur et al. ( 2009 ), taxonomic composition was considered as a fixed factor in our statistical models because we had two levels of taxonomic compositions per treatment ( i. e. , far from the minimum 5 levels required for considering a variable to be random). We used the lm function in the “stats” package in R (4.0.3 version) (R Core Team, 2020). Differences in the number of surviving plants in the drought treatments could affect the flowering segregation index. Thus, in order to statistically control for the differences in the number of surviving individuals, we conducted a bootstrap procedure to standardize the number of species used to calculate this index in each pot. Specifically, we randomly selected four of the coexisting species since most pots had at least four species during the flowering peak even in drought conditions (n = 107) and bootstrapped 100 times to calculate the average value for the flowering segregation index for each specific pot. The average value obtained by this bootstrap procedure was analyzed with the same nested linear model explained above. Results In high phylogenetic diversity experimental scenarios, the peak flowering time averaged among coexisting species occurred at 8.9 weeks (± 0.18 SE) under average water availability and at 7.6 weeks (± 0.22 SE) under drought conditions. In low PD scenarios, the peak flowering time was observed at 7.7 weeks (± 0.3 SE) with average water availability and at 5.95 weeks (± 0.29 SE) under drought conditions. Overall, drought conditions accelerated the flowering time in high and low phylogenetic diversity experimental scenarios. The initial phylogenetic diversity of species assemblages significantly influenced flowering segregation in pots, irrespective of irrigation treatment (Table 1 , Fig. 1 ). Specifically, flowering phenology was more segregated in assemblages with low phylogenetic diversity compared to those with high phylogenetic diversity. Conversely, assemblages composed of phylogenetically distant species tended to have overlapping flowering peaks. Additionally, drought treatment increased flowering overlap, regardless of the initial phylogenetic diversity of the assemblage. Similar results were obtained when the number of species per pot was standardized using the bootstrap procedure. In this case, we found that the initial phylogenetic diversity was significant 100% of the time, irrigation was significant 95% of the time, and the interaction between them was not significant 92% of the time. Table 1 Linear models (LMs) for the analyses of flowering segregation among coexisting species per pot. Taxonomic composition (TC) nested within phylogenetic diversity (PD), irrigation treatment (I) and their interaction were included as fixed factors. Sum of squares and F values are presented. df: degrees of freedom. *: p < 0.05; **: p < 0.01; ***: p < 0.001. df Sum sq F value Phylogenetic diversity (PD) 1 41.9 137.5 *** Irrigation (I) 1 14.8 48.7 *** PD x Taxonomic composition (TC) 2 63.4 103.9 *** PD x I 1 1.1 3.6 PD x TC x I 2 5.6 9.2 *** Residuals 102 31.1 Discussion In a previous study, we demonstrated that niche complementarity was the primary assembly process in phylogenetically diverse Iberian gypsophilous annual plant neighborhoods (Chaves et al., 2021 ). We provided evidence that plants had a higher probability of survival and reproduction when growing in phylogenetically diverse assemblages, especially under drought conditions. In the present study, we use the same experiment to further analyze flowering time as a potential mechanism underlying the previous results, considering flowering segregation among coexisting plants as a proxi for temporal segregation in soil resource uptake (Davies et al., 2010; Craine et al., 2012 ; Montesinos-Navarro, 2023 ). With this in mind, we anticipated that flowering would be more segregated in phylogenetically diverse assemblages and more synchronized in those with closely related species, given the phylogenetic conservation of flowering phenology (Swenson & Enquist, 2007 ; Willis et al., 2008 ; Kraft & Ackerly, 2010 ; Simon et al., 2021 ) and the divergence of strategies required for niche complementarity (Webb et al., 2002 ). However, contrary to our expectations, our results revealed the opposite trend, with flowering being more overlapped in phylogenetically more diverse assemblages than in less diverse ones. This is a remarkable result that suggests that flowering time is not particularly relevant as a niche complementarity mechanism organizing our community. Instead, the community assembly is more likely driven by differences in other functional strategies and mechanisms rather than flowering time. Phylogenetically distant species may exhibit differences in functional traits related, for instance, to water use efficiency, photosynthetic efficiency, or resistance to desiccation (Webb et al., 2002 ; Kraft et al., 2007 ; Cavender-Bares et al., 2009 ). In our experimental setup, species with contrasting strategies to withstand water restriction successfully coexisted in phylogenetically diverse assemblages (e.g., the water accumulator Pistorinia hispanica , Crassulaceae, and the almost leafless Echinaria capitata , Poaceae) (Appendix 1). Therefore, species in phylogenetically diverse assemblages may attenuate interspecific competition by means of differences in functional traits, allowing them to allocate resources to flower production during the optimal period (in terms of temperature, soil moisture, photoperiod, etc.; Lee et al., 2023 ), that resulted in the overlap of species flowering peaks and presumably of their maximum development and resource uptake periods (Cleland et al., 2006 ). Drought conditions accelerated flowering time regardless of the phylogenetic diversity of the assemblage (see phenological data in Chaves et al., 2021 ). Other studies have observed that drought triggers the acceleration of flowering when days are long (Kigel et al., 2011 ; Lee et al., 2023 ). This drought escape response seems to be an adaptive strategy of many annual species to complete their life cycles and produce seeds when environmental conditions become challenging to survive (Franks, 2011 ). The earlier flowering as a response to drought conditions has likely contributed to the greater overlap in flowering phenology among coexisting species shown in this study. Remarkably, this temporal flowering synchronization under drought conditions was greater in high-diversity neighborhoods, which nevertheless showed higher reproductive success than low phylogenetic diversity ones (see fitness data in Chaves et al., 2021 ). This finding aligns with Ferguson et al. ( 2019 ), who observed that flowering time acceleration did not penalize reproductive performance. Unexpectedly, temporal flowering segregation was observed in assemblages of closely related species. Flowering segregation has been extensively studied in coflowering species that share pollinators (Moeller, 2004 ; Cozzolino et al., 2005 ; Aizen & Vázquez, 2006 ; Fantinato et al., 2018 ), potentially explaining the coexistence of shrub species within the same genus due to reduced deposition of heterospecific pollen (de Avila & Pinheiro, 2021 ). However, in our study, pollinators could not have induced this response, as the experiment was conducted in a greenhouse. We propose that the likely intense competition for belowground resources among closely related plants may have influenced the timing of full development and flowering of plants, resulting in a hierarchical flowering pattern among the coexisting species. Altering flowering time is an evolutionary strategy adopted by plants to maximize the chances of reproduction under stressful conditions (Kazan & Lyons 2016; Gaudinier & Blackman 2020). Thus, our results suggest that selective pressure for high plasticity in flowering phenology is particularly crucial in gypsum annual plant communities in semiarid systems. In conclusion, our findings corroborate the hypotheses that phenotypic plasticity in flowering time, rather than phylogenetic constraints, is a crucial property for species coexistence within our ecological system. When coexisting species undergo niche segregation mediated by non-phenological traits, their flowering periods can overlap, enabling them to flower at the time of optimal environmental conditions. This observation aligns with the significant overlap in flowering times reported in other Mediterranean dry grasslands (Fantinato et al., 2018 ). Conversely, when coexisting related species compete for resources, temporal segregation of flowering times may emerge as an adaptive strategy to mitigate stressful conditions. Moreover, the significant plasticity in flowering time observed in our target community indicates that it may adapt more successfully to future climate change, which will be particularly severe in the Iberian gypsum drylands, compared to systems with lower levels of phenotypic plasticity (Cleland et al., 2012), provided that environmental conditions remain within certain thresholds that permit this response. Declarations Author contributions: ALL conceived the idea; ALL, RC and PF collected seeds for the experimental set-up; ALL and RC designed methodology; RC collected the data; AMN and RC analysed the data; ALL and RC led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication. Data availability statement Dryad. https://doi.org/10.5061/dryad.98sf7m0tq Data could be also provided by Arantzazu L. Luzuriaga (corresponding author): [email protected] Ethical statement Authors assure that legislation on seed collection has been accomplished. Permission obtained from responsible authority to collect seeds. Acknowledgments We thank Carlos Díaz and José Margalet for experiment assistance. Roberto López Rubio for his help with the experimental setup. We thank the Spanish Meteorological Agency (AEMET) for providing climatic data and Yesos Ibéricos-Algiss for providing gypsum soil. Financial support was provided by the PHYLOFUNKEY project (PID2023-149999NB-I00 - Spanish Government) and NITOFLOW project (CNS2023-144743, Consolidacion investigadora, Ministerio de Ciencia, Innovación y Universidades – Spanish Government). References Ackerly, D. D. Community assembly, niche conservatism, and adaptive evolution in changing environments. Int. J. Plant Sci. 164 , 165–184 (2003). Aizen, M. A. & Vázquez, D. P. 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AoB Plants . 12 , 1–8 (2020). Luzuriaga, A. L., González, J. M. & Escudero, A. Annual plant community assembly in edaphically heterogeneous environments. J. Veg. Sci. 26 , 866–875 (2015). Luzuriaga, A. L., Sánchez, A. M., López-Angulo, J. & Escudero, A. Habitat fragmentation determines diversity of annual plant communities at landscape and fine spatial scales. Basic Appl. Ecol. 29 , 12–19 (2018). Luzuriaga, A. L., Sánchez, A. M., Maestre, F. T. & Escudero, A. Assemblage of a semi-arid annual plant community: abiotic and biotic filters act hierarchically. PLoS ONE . 7 , 1–9 (2012). Martínez-Duro, E., Luzuriaga, A. L., Ferrandis, P., Escudero, A. & Herranz, J. M. Does aboveground vegetation composition resemble soil seed bank during succession in specialized vegetation on gypsum soil? Ecol. Res. 27 , 43–51 (2012). Mayfield, M. M. & Levine, J. M. Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol. Lett. 13 , 1085–1093 (2010). Mitchell, R. J., Flanagan, R. J., Brown, B. J., Waser, N. M. & Karron, J. D. New frontiers in competition for pollination. Ann. Botany . 103 , 1403–1413 (2009). Moeller, D. A. Facilitative interactions among plants via shared pollinators. Ecology 85 , 3289–3301 (2004). Montesinos-Navarro, A. Nitrogen transfer between plant species with different temporal N‐demand. Ecol. Lett. 26 , 1676–1686 (2023). Montesinos-Navarro, A., Wig, J., Xavier Pico, F. & Tonsor, S. J. Arabidopsis thaliana populations show clinal variation in a climatic gradient associated with altitude. New Phytol. 189 (1), 282–294 (2011). Mooney, H. A., Hobbs, R. J., Gorham, J. & Williams, K. Biomass accumulation and resource utilization in co-occurring grassland annuals. Oecologia 70 , 555–558 (1986). Ortiz, L., Luzuriaga, A. L. & Ferrandis, P. Functional diversity of experimental annual plant assemblages drives plant responses to biological soil crusts in gypsum systems. Funct. Ecol. 37 , 488–503. https://doi.org/10.1111/1365-2435.14234 (2023). Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35 , 526–528 (2018). Pausas, J. G. & Verdú, M. The jungle of methods for evaluating phenotypic and phylogenetic structure of communities. BioScience 60 , 614–625 (2010). Pauw, A. Can pollination niches facilitate plant coexistence? Trends ecology evolution . 28 , 30–37 (2013). Peñuelas, J. et al. Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytol. 161 , 837–846 (2004). Peralta, A. M. L., Sánchez, A. M., Luzuriaga, A. L. & Escudero, A. Factors driving species assemblage in Mediterranean soil seed banks: from the large to the fine scale. Ann. Botany . 117 , 1221–1228 (2016). Peralta, A. M., Sánchez, A. M., Luzuriaga, A. L., de Bello, F. & Escudero, A. Evidence of functional species sorting by rainfall and biotic interactions: A community monolith experimental approach. J. Ecol. 107 , 2772–2788 (2019). Rathcke, B. & Lacey, E. P. Phenological patterns of terrestrial plants. Annu. Rev. Ecol. Syst. 16 , 179–214 (1985). Ricketts, T. H. et al. Landscape effects on crop pollination services: are there general patterns? Ecol. Lett. 11 , 499–515 (2008). Sánchez, A. M., Peralta, A. M., Luzuriaga, A. L., Prieto, M. & Escudero, A. Climate change and biocrust disturbance synergistically decreased taxonomic, functional and phylogenetic diversity in annual communities on gypsiferous soils. Oikos 3:e08809. (2022). Shavrukov, Y. et al. Early flowering as a drought escape mechanism in plants: How can it aid wheat production? Front. Plant Sci ., 8, 1950. (2017). Simon, A. D., Marx, H. E. & Starzomski, B. M. Phylogenetic restriction of plant invasion in drought-stressed environments: Implications for insect‐pollinated plant communities in water‐limited ecosystems. Ecol. Evol. 11 , 10042–10053 (2021). Slingsby, J. A. & Verboom, G. A. Phylogenetic relatedness limits co-occurrence at fine spatial scales: evidence from the schoenoid sedges (Cyperaceae: Schoeneae) of the Cape Floristic Region, South Africa. Am. Nat. 168 , 14–27 (2006). Srivastava, D. S., Cadotte, M. W., MacDonald, A. A. M., Marushia, R. G. & Mirotchnick, N. Phylogenetic diversity and the functioning of ecosystems. Ecol. Lett. 15 , 637–648 (2012). Strauss, S. Y., Truszczinski, A. M. & Anacker, B. L. Do habitat shifts alter flowering phenology overlap in close relatives? Implications for local coexistence. Madroño 68 , 406–415 (2021). Sun, S. & Frelich, L. E. Flowering phenology and height growth pattern are associated with maximum plant height, relative growth rate and stem tissue mass density in herbaceous grassland species. J. Ecol. 99 , 991–1000 (2011). Swenson, N. G. & Enquist, B. J. Ecological and evolutionary determinants of a key plant functional trait: wood density and its community-wide variation across latitude and elevation. Am. J. Bot. 94 , 451–459 (2007). Swenson, N. G., Enquist, B. J., Pither, J., Thompson, J. & Zimmerman, J. K. The problem and promise of scale dependency in community phylogenetics. Ecology 87 , 2418–2424 (2006). Valiente-Banuet, A. & Verdú, M. Facilitation can increase the phylogenetic diversity of plant communities. Ecol. Lett. 10 , 1029–1036 (2007). Webb, C. O., Ackerly, D. D., McPeek, M. A. & Donoghue, M. J. Phylogenies and community ecology . Annu. Rev. Ecol. Syst. 33 , 475–505 (2002). Willis, C. G., Ruhfel, B., Primack, R. B., Miller-Rushing, A. J. & Davis, C. C. Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proceedings of the National Academy of Sciences 105: 17029–17033. (2008). Zuur, A. F., Ieno, E. N. & Meesters, E. H. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-5980745","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":414086359,"identity":"0739c9fe-f9c1-45df-bed8-04c56f0a4c67","order_by":0,"name":"Rocío Chaves","email":"","orcid":"","institution":"Departamento de Biología y Geología, Física y Química Inorgánica, Universidad Rey Juan Carlos","correspondingAuthor":false,"prefix":"","firstName":"Rocío","middleName":"","lastName":"Chaves","suffix":""},{"id":414086360,"identity":"1eb5cfe8-5aab-45dc-b0e5-69a332a36a12","order_by":1,"name":"Alicia Montesinos-Navarro","email":"","orcid":"","institution":"Centro de Investigaciones sobre Desertificación (CIDE, CSIC-UV-GV)","correspondingAuthor":false,"prefix":"","firstName":"Alicia","middleName":"","lastName":"Montesinos-Navarro","suffix":""},{"id":414086362,"identity":"37f096dc-bfd0-4562-b490-6c6dd86985be","order_by":2,"name":"Pablo Ferrandis","email":"","orcid":"","institution":"Jardín Botánico de Castilla-La Mancha, Universidad de Castilla-La Mancha","correspondingAuthor":false,"prefix":"","firstName":"Pablo","middleName":"","lastName":"Ferrandis","suffix":""},{"id":414086363,"identity":"41791e94-17cb-4305-ad56-cbb52285afb1","order_by":3,"name":"Arantzazu L. Luzuriaga","email":"data:image/png;base64,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","orcid":"","institution":"Instituto de Investigación en Cambio Global (IICG-URJC), Universidad Rey Juan Carlos","correspondingAuthor":true,"prefix":"","firstName":"Arantzazu","middleName":"L.","lastName":"Luzuriaga","suffix":""}],"badges":[],"createdAt":"2025-02-07 11:38:21","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-5980745/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-5980745/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1038/s41598-025-12414-8","type":"published","date":"2025-07-24T15:57:50+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":76078703,"identity":"68108cdf-a5ac-4cf7-b807-fd494150c57d","added_by":"auto","created_at":"2025-02-12 06:12:55","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":30681,"visible":true,"origin":"","legend":"\u003cp\u003eMean flowering segregation (weeks) in high vs. low phylogenetic diversity (PD) of the plant neighborhood under two irrigation treatments (average precipitation vs. drought). Vertical bars represent standard errors.\u003c/p\u003e","description":"","filename":"floatimage114.png","url":"https://assets-eu.researchsquare.com/files/rs-5980745/v1/ac7fcf80b04892c96e65f7e0.png"},{"id":87756867,"identity":"f7e878cd-2919-4e1c-9d34-acc307c0a1b0","added_by":"auto","created_at":"2025-07-28 16:09:55","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":640181,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5980745/v1/65b37433-09e4-4740-b526-812ecfc71f49.pdf"},{"id":76077728,"identity":"34e8752a-33f2-482a-9570-4cf1054f6a84","added_by":"auto","created_at":"2025-02-12 06:04:55","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":17797,"visible":true,"origin":"","legend":"","description":"","filename":"Appendix1.docx","url":"https://assets-eu.researchsquare.com/files/rs-5980745/v1/e6461eb73e883e5ae99e345a.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Plasticity versus phylogenetic restrictions in flowering time of coexisting species in experimental annual plant assemblages","fulltext":[{"header":"Introduction","content":"\u003cp\u003eFlowering time is a crucial event in the lifetime of angiosperms that has critical impacts on plant fitness. If flowering occurs too early in the growing season, late frosts could damage floral tissues, or pollinators may not yet be abundant enough to ensure fertilization, or plant size may constrain total flower production. However, if flowering occurs too late, environmental conditions may not be favorable for seed maturation or dispersal or may leave the offspring in harsh conditions to survive (Bernal et al., \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Montesinos-Navarro et al., \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2011\u003c/span\u003e, Bucher \u0026amp; Romermann 2020). Flowering time is determined by a trade-off among water availability (Shavrukov et al., \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2017\u003c/span\u003e) temperature (Cleland et al., 2012; Jagadish et al., \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2016\u003c/span\u003e), photoperiod (Johanson, 2014), and the moment of germination (Rathcke \u0026amp; Lacey, \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e1985\u003c/span\u003e). External environmental conditions are linked to a complex set of endogenous molecular pathways that trigger flowering time (Lee et al., \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). In arid and semiarid systems, where unpredictable droughts occur, soil water availability is known to be a critical driver of plant growth and plant community dynamics (Pe\u0026ntilde;uelas et al., \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2004\u003c/span\u003e, Peralta et al., \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Luzuriaga et al., \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2012\u003c/span\u003e, \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; S\u0026aacute;nchez et al., \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Low water availability has been linked to acceleration in flowering timing, especially in annual plants (Fitter \u0026amp; Fitter, \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Kigel et al., \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), which has been interpreted as a drought escape response to complete phenology prior to environment becoming too harsh for plant survival (Franks, \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Flowering time is associated with the period of maximum vegetative biomass (Mooney et al., \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e1986\u003c/span\u003e; Cleland et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Sun \u0026amp; Frelich, \u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), indicating high resource uptake. Indeed, several studies suggest that phenology can serve as a proxy for temporal resource use in plants (Davies et al., 2010; Craine et al., \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Montesinos-Navarro, \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2023\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIt is expected that co-occurring species are more likely to coexist if their phenology is segregated because of a reduction of interspecific competition (Chase \u0026amp; Laibold, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Chesson et al., \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). Furthermore, phenological segregation has recently been demonstrated to be a plausible driver of community structure by enabling nitrogen transfer between plants in different phenological stages (Montesinos-Navarro, \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). In communities where coexisting species flower concurrently, species performance may benefit from overlapping flowering periods due to the attraction of a larger number and greater diversity of pollinators (Moeller, \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Ricketts et al., \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; L\u0026aacute;zaro et al., \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). However, co-flowering species might also face increased competition for pollinators, potentially reducing the frequency of pollinator visits (Elzinga et al., \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Mitchell et al., \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Pauw, \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2013\u003c/span\u003e), as well as competition for shared abiotic resources. Consequently, the aggregation versus segregation of flowering phenology can alter plant-plant interactions among coexisting species (Strauss et al., \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), ultimately influencing the species assembly process.\u003c/p\u003e \u003cp\u003eIn the last two decades, community ecologists have focused their attention on phylogenetic patterns in order to unveil ecological processes underlying coexistence (Webb et al., \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2002\u003c/span\u003e). Phylogenetic diversity (PD, hereinafter) measures the degree of evolutionary relatedness among species of a community (Faith, \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e1992\u003c/span\u003e). It provides a valuable measure of biodiversity because it integrates the evolutionary history of species with their ecological requirements (Ackerly, \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Cavender-Bares et al., \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Srivastava et al., \u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Gerhold et al., \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2015\u003c/span\u003e) and it can inform on the main ecological processes involved in the species assembly (Webb et al., \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Emerson \u0026amp; Gillespie, \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; Lemos-Costa et al., \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). Many authors have analyzed phylogenetic relatedness observed in local communities to infer ecological processes that can influence the community structure (\u003cem\u003ei. e.\u003c/em\u003e, phylogenetic response) (Godoy et al., \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; L\u0026oacute;pez-Angulo et al., \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Luzuriaga et al., \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Phylogenetic convergence is usually related to habitat filtering processes (Webb et al., \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2002\u003c/span\u003e) and to competitive exclusion processes when a phylogenetically conserved trait promoting survival is selected by environmental constraints (Mayfield \u0026amp; Levine, \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). Phylogenetic overdispersion in assemblages (phylogenetic divergence) is usually associated with nurse-mediated facilitation (Valiente-Banuet \u0026amp; Verd\u0026uacute;, \u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e2007\u003c/span\u003e), and competitive exclusion interactions between close relatives with the same niche-use (Webb et al., \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Slinghsby \u0026amp; Verboom, 2006). Phylogenetic divergence, however, also occurs when distantly related taxa converge on similar niche-use (Cavender-Bares et al., \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Kembel \u0026amp; Hubbell, \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Swenson et al., \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Kraft et al., \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2007\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIntegrating knowledge on how flowering timing is influenced by community-level patterns, such as phylogenetic diversity, and how flowering timing, in turn, affects species coexistence within the community, is crucial for understanding the assembly of plant communities and for predicting how they will respond to ongoing climate change. Although flowering timing is a ductile trait particularly sensitive to both abiotic and biotic environmental signals, plant species have a range in the flowering response which should be ultimately determined by their evolutionary history. To what extent plasticity vs. phylogeny determines phenological segregation is a key question to understand assembly mechanisms organizing plant communities. From a community perspective, few studies have manipulated the phylogenetic diversity of experimental assemblages (see Feng et al., \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2019\u003c/span\u003e, and Galland et al., \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2019\u003c/span\u003e) and even fewer have done so to evaluate the causal effect of phylogenetic diversity of assemblages as driver of the assembly processes (see Chaves et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Ortiz et al., \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). We build on our previous study (Chaves et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), that established that under drought conditions, phylogenetically diverse assemblages of Iberian gypsophilous annual plants resulted in higher plant survival and fitness than neighborhoods composed of closely related species, to explore potential mechanisms driven by plant phenology. The phylogenetic diversity of species assemblages seems to be a driving force of the assembly process, being the niche complementarity among species a central process organizing the community (Webb et al., \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Pausas \u0026amp; Verd\u0026uacute;, \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Chaves et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), however a better understanding of the underlying mechanisms is required to improve our predictions on how communities will change under different conditions.\u003c/p\u003e \u003cp\u003eIn this study, we aimed to evaluate if differences in flowering time of coexisting species could be a key driver of niche complementarity in the communities of annual plants growing in gypsum soils. To pursue this aim, we monitored the flowering phenology of plants in a common garden experiment, where the initial phylogenetic diversity of species assemblages together with water availability were manipulated. We hypothesize that, in a scenario where flowering time is, to some extent, evolutionarily conserved, flowering segregation will be higher in phylogenetically diverse assemblages compared to assemblages with close relatives, especially under drought conditions in which competition avoidance might be even more relevant for succeeding. However, in the opposite scenario, where flowering time of species is highly plastic, we expect a reduction of the temporal segregation (i.e., greater flowering overlap) under drought conditions, both in high and low PD assemblages, thus flowering acceleration can be a response to escape from water stress in unpredictable systems.\u003c/p\u003e"},{"header":"Materials and methods","content":"\u003cp\u003eThe target annual plant community of this study grows on gypsum soils in the Tagus valley, central Spain. The climate in the area is semiarid Mediterranean with mean annual temperatures around 14.5\u0026deg;C and mean annual precipitation of 400 mm, specially distributed in the late autumn and early spring (Aranjuez weather station, 40\u0026deg;4\u0026prime;2\u0026prime;\u0026prime;N; 3\u0026deg;32\u0026prime;46\u0026prime;\u0026prime;W, 540 m). The habitat comprises a gypsum steppe, where gypsophilous dwarf shrubs (e.g., \u003cem\u003eLepidium subulatum\u003c/em\u003e L., \u003cem\u003eCentaurea hyssopifolia\u003c/em\u003e Vahl, \u003cem\u003eGypsophila struthium\u003c/em\u003e L., \u003cem\u003eHelianthemum squamatum\u003c/em\u003e (L.) Dum. Cours., \u003cem\u003eThymus lacaitae\u003c/em\u003e Pau, \u003cem\u003eHerniaria fruticosa\u003c/em\u003e L., and \u003cem\u003eFrankenia thymifolia\u003c/em\u003e Desf.) are patchily scattered along with \u003cem\u003eMacrochloa tenacissima\u003c/em\u003e (L.) Kunth grass tussocks on a matrix of bare soil with a well-developed biological crust dominated by lichens (e.g., \u003cem\u003eDiploschistes diacapsis\u003c/em\u003e (Ach.) Lumbsch, \u003cem\u003eSquamarina lentigera\u003c/em\u003e (G.H. Weber) Poelt, \u003cem\u003eFulgensia subbracteata\u003c/em\u003e (Nyl.) Poelt, and \u003cem\u003ePsora decipiens\u003c/em\u003e (Hedw.) Hoffm). From October to July a seasonally dynamic, rich community of annual plants proliferates. They remain in seed form the rest of the year by accumulating dense and well-structured seed banks in the soil (Caballero et al., \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; Mart\u0026iacute;nez-Duro et al., \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Peralta et al., \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). The regional species pool is composed of nearly 120 species (Luzuriaga et al \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2018\u003c/span\u003e), with up to 38 plant species/0.25 m\u003csup\u003e2\u003c/sup\u003e in rainy years (Luzuriaga et al., \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Relevant examples are \u003cem\u003eCampanula fastigiata\u003c/em\u003e Dufour ex A. DC., \u003cem\u003eChaenorhinum reyesii\u003c/em\u003e (C. Vicioso \u0026amp; Pau) Bened\u0026iacute;, \u003cem\u003eAsterolinon linum-stellatum\u003c/em\u003e (L.) Duby in DC., \u003cem\u003eCampanula erinus\u003c/em\u003e L., \u003cem\u003eGalium parisiense\u003c/em\u003e L., \u003cem\u003eHelianthemum salicifolium\u003c/em\u003e (L.) Miller., \u003cem\u003eMicropyrum tenellum\u003c/em\u003e (L.) Link, \u003cem\u003eBromus rubens\u003c/em\u003e L., \u003cem\u003eLomelosia stellata\u003c/em\u003e (L.) Raf. and \u003cem\u003ePistorinia hispanica\u003c/em\u003e (L.) DC.\u003c/p\u003e \u003cp\u003eWe used data collected from the experiment described in Chaves et al. (\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e) in which we manipulated the initial phylogenetic diversity of experimental assemblages in a common garden approach in the greenhouse. We aimed to evaluate the causal effect of phylogenetic diversity on flowering phenology of annual plant assemblages. This approach has rarely been attempted with vascular plants to the best of our knowledge (but see Feng et al., \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Galland et al., \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). To determine the initial levels of phylogenetic diversity of each assemblage, we prepared a phylogenetic tree (see Chaves et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e) using \u003cem\u003ephylo.maker\u003c/em\u003e function of \u0026ldquo;V.Phylomaker\u0026rdquo; package (Jin \u0026amp; Qian, \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), and to calculate indices we used the packages \u0026ldquo;ape\u0026rdquo; (Paradis \u0026amp; Schliep, \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2018\u003c/span\u003e) and \u0026ldquo;picante\u0026rdquo; (Kembel et al., \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2010\u003c/span\u003e) in software R (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://www.R-project.org\u003c/span\u003e\u003cspan address=\"http://www.R-project.org\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e). We calculated the phylogenetic species variability (PSV) index (Helmus et al., \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2007\u003c/span\u003e) and the standardized effect size of mean pairwise distances in communities index (SES.MPD). The PSV index, bounded between 0 and 1, indicates the degree of relatedness among different species in a community. Values close to zero imply very low PD, while values close to one represent maximum PD. The SES.MPD index measures the mean phylogenetic distance between pairs of species and contrasts it to 1000 null species assemblages from the phylogenetic community tree. High positive values imply larger mean phylogenetic distance than the null model, thus phylogenetic dispersal, while high negative values indicate lower mean phylogenetic distance than the null model, thus phylogenetic convergence.\u003c/p\u003e \u003cp\u003eTo create species assemblages, we collected seeds of annual plants along the Tagus valley during the springs of 2016 and 2017. Annual plant communities from Mediterranean gypsum soils provide a useful model system to conduct manipulative experiments to determine mechanisms involved in the assembly of communities, because they comprise a rich regional species pool (over 120 taxa) of ephemeral, small-sized species, with short and highly synchronized life cycles (October-early June), which overall allow to perform, handle, and complete common garden experiments in small spaces and short time lapses ( see Luzuriaga et al., \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Peralta et al., \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Chaves et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; S\u0026aacute;nchez et al., \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Experimental assemblages were formed by four combinations of seven different species: two combinations with low PD and two with high PD. Two taxonomic scenarios with high phylogenetic diversity were composed of Poaceae, Crassulaceae, Apiaceae and Caryophylaceae families (PSV\u0026thinsp;=\u0026thinsp;0.82 and 0.85; SES.MPD\u0026thinsp;=\u0026thinsp;0.53 and 0.17) and two taxonomic scenarios with low PD, one composed of Asteraceae species (PSV\u0026thinsp;=\u0026thinsp;0.24; SES.MPD\u0026thinsp;=\u0026thinsp;\u0026minus;\u0026thinsp;9.6; p\u0026thinsp;\u0026lt;\u0026thinsp;0.001) and another one made up of Brassicales and Malvales (PSV\u0026thinsp;=\u0026thinsp;0.64; SES.MPD\u0026thinsp;=\u0026thinsp;\u0026minus;\u0026thinsp;2.5; p\u0026thinsp;\u0026lt;\u0026thinsp;0.05). Replication of taxonomic scenarios allows to control for the effects of taxonomic identity.\u003c/p\u003e \u003cp\u003eTwo irrigation treatments were applied, differing in the amount of water applied. We calculated the average monthly precipitation recorded between 1981 and 2010 in the area of our study system (Getafe weather station, 40\u0026deg;18.0\u0026prime; N, 3\u0026deg; 43.2\u0026prime; W, 620 masl) and we applied it to pots manually, distributing the corresponding amount twice a week, being this the average irrigation treatment. To simulate an intense drought, we reduced the watering to 33% of that in the Average treatment (Drought treatment). We established a fully crossed factorial design with two phylogenetic diversity levels \u0026times; two taxonomic combinations of species \u0026times; two water availability treatments (eight experimental scenarios). Each experimental scenario was replicated in 10 to 16 units, thereby resulting in 110 experimental assemblages (pots).\u003c/p\u003e \u003cp\u003eThe experiment was set up in October 2017, thus synchronized with the natural life cycle of annual plants, at the Rey Juan Carlos University greenhouse (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://urjc-cultive.webnode.es\u003c/span\u003e\u003cspan address=\"https://urjc-cultive.webnode.es\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e; M\u0026oacute;stoles, Madrid, Spain: 40\u0026deg;20\u0026prime;2\u0026prime;\u0026prime;N, 3\u0026deg;52\u0026prime;00\u0026prime;\u0026prime;W, 650 masl). We filled round plastic pots with a diameter of 30 cm and depth of 10 cm with 5 kg of seed-free gypsum soil from a gypsum quarry near to the natural habitat of the study species. Seventy seeds per species were sown in each pot and excess seedlings were removed until we obtained 10 stablished individuals per each of the seven species per pot. Plants persisted as seedlings during all winter, as naturally occurs in the field, and in February, the experimental irrigation and periodic monitoring of plants started. Between February and June (the natural growing season for annual plants in gypsum systems; Luzuriaga et al., \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), we monitored the number of flowering plants per species and pot weekly. We calculated the \u003cem\u003etime of flowering peak\u003c/em\u003e for each species in each pot by assigning the ordinal number of the week in which we censed the highest number of flowering plants of that species in that pot.\u003c/p\u003e \u003cp\u003eWe evaluated the floral phenology at the community level based on the flowering segregation index per pot. Each pot was characterized by a single value of the flowering segregation index. This index consists of the mean pairwise distances of the flowering peaks between every species in each pot (measured in number of days). Flowering segregation informs on the degree of flowering overlap among species in each species assemblage (de Avila \u0026amp; Pinheiro, \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). High values of segregation imply large temporal differences in flowering peaks among co-occurring species in each pot and low values imply synchronized or aggregated flowering peaks among coexisting species.\u003c/p\u003e \u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analyses\u003c/h2\u003e \u003cp\u003eWe performed a nested linear model to analyze whether the flowering segregation index (dependent variable), was influenced by the experimentally manipulated initial phylogenetic diversity (two levels, high and low PD), taxonomic composition (two taxonomic compositions per level of PD) and water irrigation (two levels, Average and Drought treatments) (explanatory variables). The variable taxonomic composition was nested within the phylogenetic diversity treatment to control differences associated with species identities. Following recommendations of Zuur et al. (\u003cspan citationid=\"CR74\" class=\"CitationRef\"\u003e2009\u003c/span\u003e), taxonomic composition was considered as a fixed factor in our statistical models because we had two levels of taxonomic compositions per treatment (\u003cem\u003ei. e.\u003c/em\u003e, far from the minimum 5 levels required for considering a variable to be random). We used the \u003cem\u003elm\u003c/em\u003e function in the \u0026ldquo;stats\u0026rdquo; package in R (4.0.3 version) (R Core Team, 2020).\u003c/p\u003e \u003cp\u003eDifferences in the number of surviving plants in the drought treatments could affect the flowering segregation index. Thus, in order to statistically control for the differences in the number of surviving individuals, we conducted a bootstrap procedure to standardize the number of species used to calculate this index in each pot. Specifically, we randomly selected four of the coexisting species since most pots had at least four species during the flowering peak even in drought conditions (n\u0026thinsp;=\u0026thinsp;107) and bootstrapped 100 times to calculate the average value for the flowering segregation index for each specific pot. The average value obtained by this bootstrap procedure was analyzed with the same nested linear model explained above.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cp\u003eIn high phylogenetic diversity experimental scenarios, the peak flowering time averaged among coexisting species occurred at 8.9 weeks (\u0026plusmn;\u0026thinsp;0.18 SE) under average water availability and at 7.6 weeks (\u0026plusmn;\u0026thinsp;0.22 SE) under drought conditions. In low PD scenarios, the peak flowering time was observed at 7.7 weeks (\u0026plusmn;\u0026thinsp;0.3 SE) with average water availability and at 5.95 weeks (\u0026plusmn;\u0026thinsp;0.29 SE) under drought conditions. Overall, drought conditions accelerated the flowering time in high and low phylogenetic diversity experimental scenarios. The initial phylogenetic diversity of species assemblages significantly influenced flowering segregation in pots, irrespective of irrigation treatment (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e, Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Specifically, flowering phenology was more segregated in assemblages with low phylogenetic diversity compared to those with high phylogenetic diversity. Conversely, assemblages composed of phylogenetically distant species tended to have overlapping flowering peaks. Additionally, drought treatment increased flowering overlap, regardless of the initial phylogenetic diversity of the assemblage. Similar results were obtained when the number of species per pot was standardized using the bootstrap procedure. In this case, we found that the initial phylogenetic diversity was significant 100% of the time, irrigation was significant 95% of the time, and the interaction between them was not significant 92% of the time.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eLinear models (LMs) for the analyses of flowering segregation among coexisting species per pot. Taxonomic composition (TC) nested within phylogenetic diversity (PD), irrigation treatment (I) and their interaction were included as fixed factors. Sum of squares and F values are presented. df: degrees of freedom. *: \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05; **: \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.01; ***: \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003edf\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSum sq\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eF value\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePhylogenetic diversity (PD)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e41.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e137.5 ***\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eIrrigation (I)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e14.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e48.7 ***\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePD x Taxonomic composition (TC)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e63.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e103.9 ***\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePD x I\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e1.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e3.6\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePD x TC x I\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e5.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e9.2 ***\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eResiduals\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e102\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e31.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eIn a previous study, we demonstrated that niche complementarity was the primary assembly process in phylogenetically diverse Iberian gypsophilous annual plant neighborhoods (Chaves et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). We provided evidence that plants had a higher probability of survival and reproduction when growing in phylogenetically diverse assemblages, especially under drought conditions. In the present study, we use the same experiment to further analyze flowering time as a potential mechanism underlying the previous results, considering flowering segregation among coexisting plants as a proxi for temporal segregation in soil resource uptake (Davies et al., 2010; Craine et al., \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Montesinos-Navarro, \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). With this in mind, we anticipated that flowering would be more segregated in phylogenetically diverse assemblages and more synchronized in those with closely related species, given the phylogenetic conservation of flowering phenology (Swenson \u0026amp; Enquist, \u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Willis et al., \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; Kraft \u0026amp; Ackerly, \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Simon et al., \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2021\u003c/span\u003e) and the divergence of strategies required for niche complementarity (Webb et al., \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2002\u003c/span\u003e). However, contrary to our expectations, our results revealed the opposite trend, with flowering being more overlapped in phylogenetically more diverse assemblages than in less diverse ones. This is a remarkable result that suggests that flowering time is not particularly relevant as a niche complementarity mechanism organizing our community. Instead, the community assembly is more likely driven by differences in other functional strategies and mechanisms rather than flowering time. Phylogenetically distant species may exhibit differences in functional traits related, for instance, to water use efficiency, photosynthetic efficiency, or resistance to desiccation (Webb et al., \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Kraft et al., \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Cavender-Bares et al., \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). In our experimental setup, species with contrasting strategies to withstand water restriction successfully coexisted in phylogenetically diverse assemblages (e.g., the water accumulator \u003cem\u003ePistorinia hispanica\u003c/em\u003e, Crassulaceae, and the almost leafless \u003cem\u003eEchinaria capitata\u003c/em\u003e, Poaceae) (Appendix 1). Therefore, species in phylogenetically diverse assemblages may attenuate interspecific competition by means of differences in functional traits, allowing them to allocate resources to flower production during the optimal period (in terms of temperature, soil moisture, photoperiod, etc.; Lee et al., \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2023\u003c/span\u003e), that resulted in the overlap of species flowering peaks and presumably of their maximum development and resource uptake periods (Cleland et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2006\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eDrought conditions accelerated flowering time regardless of the phylogenetic diversity of the assemblage (see phenological data in Chaves et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Other studies have observed that drought triggers the acceleration of flowering when days are long (Kigel et al., \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Lee et al., \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). This drought escape response seems to be an adaptive strategy of many annual species to complete their life cycles and produce seeds when environmental conditions become challenging to survive (Franks, \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). The earlier flowering as a response to drought conditions has likely contributed to the greater overlap in flowering phenology among coexisting species shown in this study. Remarkably, this temporal flowering synchronization under drought conditions was greater in high-diversity neighborhoods, which nevertheless showed higher reproductive success than low phylogenetic diversity ones (see fitness data in Chaves et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). This finding aligns with Ferguson et al. (\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), who observed that flowering time acceleration did not penalize reproductive performance.\u003c/p\u003e \u003cp\u003eUnexpectedly, temporal flowering segregation was observed in assemblages of closely related species. Flowering segregation has been extensively studied in coflowering species that share pollinators (Moeller, \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Cozzolino et al., \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Aizen \u0026amp; V\u0026aacute;zquez, \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Fantinato et al., \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2018\u003c/span\u003e), potentially explaining the coexistence of shrub species within the same genus due to reduced deposition of heterospecific pollen (de Avila \u0026amp; Pinheiro, \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). However, in our study, pollinators could not have induced this response, as the experiment was conducted in a greenhouse. We propose that the likely intense competition for belowground resources among closely related plants may have influenced the timing of full development and flowering of plants, resulting in a hierarchical flowering pattern among the coexisting species. Altering flowering time is an evolutionary strategy adopted by plants to maximize the chances of reproduction under stressful conditions (Kazan \u0026amp; Lyons 2016; Gaudinier \u0026amp; Blackman 2020). Thus, our results suggest that selective pressure for high plasticity in flowering phenology is particularly crucial in gypsum annual plant communities in semiarid systems.\u003c/p\u003e \u003cp\u003eIn conclusion, our findings corroborate the hypotheses that phenotypic plasticity in flowering time, rather than phylogenetic constraints, is a crucial property for species coexistence within our ecological system. When coexisting species undergo niche segregation mediated by non-phenological traits, their flowering periods can overlap, enabling them to flower at the time of optimal environmental conditions. This observation aligns with the significant overlap in flowering times reported in other Mediterranean dry grasslands (Fantinato et al., \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Conversely, when coexisting related species compete for resources, temporal segregation of flowering times may emerge as an adaptive strategy to mitigate stressful conditions. Moreover, the significant plasticity in flowering time observed in our target community indicates that it may adapt more successfully to future climate change, which will be particularly severe in the Iberian gypsum drylands, compared to systems with lower levels of phenotypic plasticity (Cleland et al., 2012), provided that environmental conditions remain within certain thresholds that permit this response.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAuthor contributions:\u0026nbsp;\u003c/strong\u003eALL conceived the idea; ALL, RC and PF collected seeds for the experimental set-up; ALL and RC designed methodology; RC collected the data; AMN and RC analysed the data; ALL \u0026nbsp;and RC led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData availability\u003c/strong\u003e \u003cstrong\u003estatement\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eDryad. https://doi.org/10.5061/dryad.98sf7m0tq\u003c/p\u003e\n\u003cp\u003eData could be also provided by Arantzazu L. Luzuriaga (corresponding author): [email protected]\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthical statement\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAuthors assure that legislation on seed collection has been accomplished.\u003c/p\u003e\n\u003cp\u003ePermission obtained from responsible authority to collect seeds.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgments\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe thank Carlos D\u0026iacute;az and Jos\u0026eacute; Margalet for experiment assistance. Roberto L\u0026oacute;pez Rubio for his help with the experimental setup. We thank the Spanish Meteorological Agency (AEMET) for providing climatic data and Yesos Ib\u0026eacute;ricos-Algiss for providing gypsum soil. Financial support was provided by the PHYLOFUNKEY project (PID2023-149999NB-I00 - Spanish Government) and NITOFLOW project (CNS2023-144743, Consolidacion investigadora, Ministerio de Ciencia, Innovaci\u0026oacute;n y Universidades \u0026ndash; Spanish Government).\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAckerly, D. D. Community assembly, niche conservatism, and adaptive evolution in changing environments. \u003cem\u003eInt. J. Plant Sci.\u003c/em\u003e \u003cb\u003e164\u003c/b\u003e, 165\u0026ndash;184 (2003).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAizen, M. A. \u0026amp; V\u0026aacute;zquez, D. P. 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H. \u003cem\u003eA Beginner's Guide to R\u003c/em\u003e (Springer, 2009).\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"scientific-reports","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"scirep","sideBox":"Learn more about [Scientific Reports](http://www.nature.com/srep/)","snPcode":"","submissionUrl":"","title":"Scientific Reports","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Scientific Reports","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Common garden, drought, flowering phenology, gypsum, niche complementarity, phenotipic plasticity, phylogenetic diversity, species assembly, species coexistence","lastPublishedDoi":"10.21203/rs.3.rs-5980745/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-5980745/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eFlowering timing is a critical event in the lifetime of angiosperms, being particularly sensitive to environmental conditions, although the range of flowering response should be ultimately constrained by evolutionary history. We hypothesized that a) if phylogenetic constraints prevail over phenotypic plasticity in the expression of flowering phenology, flowering peaks would be more segregated in diverse assemblages than in assemblages composed of close relatives; b) conversely, if flowering time is mainly a plastic trait, drought would induce significant flowering overlap, irrespective of the phylogenetic diversity in the assemblage. We designed assemblages with annual plants of semiarid systems of Spain, considering two contrasted levels of phylogenetic diversity (PD) and two water availability treatments in a common garden experiment, where we analysed the flowering segregation among species. High PD assemblages resulted in greater flowering overlap, while assemblages composed of close relatives segregated more their flowering peaks. Water stress triggered flowering synchronization both in neighborhoods with high and low phylogenetic diversity. Our findings corroborate that in the very diverse Iberian gypsophilous annual plant communities, it is phenotypic plasticity in response to water availability, rather than phylogenetic constraints what modulates species segregation of flowering phenology, potentially affecting species coexistence.\u003c/p\u003e","manuscriptTitle":"Plasticity versus phylogenetic restrictions in flowering time of coexisting species in experimental annual plant assemblages","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-02-12 06:04:50","doi":"10.21203/rs.3.rs-5980745/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2025-04-09T13:22:38+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-04-08T12:56:52+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"231319658740737689263502624158401330155","date":"2025-03-29T10:42:43+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-02-28T12:45:34+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"303766059864695846100382170405656437110","date":"2025-02-16T07:50:12+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2025-02-16T05:11:00+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2025-02-11T05:00:17+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2025-02-11T03:29:56+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2025-02-10T09:00:45+00:00","index":"","fulltext":""},{"type":"submitted","content":"Scientific Reports","date":"2025-02-07T11:33:07+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"scientific-reports","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"scirep","sideBox":"Learn more about [Scientific Reports](http://www.nature.com/srep/)","snPcode":"","submissionUrl":"","title":"Scientific Reports","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Scientific Reports","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"4b8a64a3-d518-4ada-9245-d49b4f2e2e84","owner":[],"postedDate":"February 12th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[{"id":44152823,"name":"Earth and environmental sciences/Ecology/Community ecology"},{"id":44152824,"name":"Earth and environmental sciences/Ecology/Biodiversity"},{"id":44152825,"name":"Earth and environmental sciences/Ecology/Climate change ecology/Phenology"}],"tags":[],"updatedAt":"2025-07-28T16:06:13+00:00","versionOfRecord":{"articleIdentity":"rs-5980745","link":"https://doi.org/10.1038/s41598-025-12414-8","journal":{"identity":"scientific-reports","isVorOnly":false,"title":"Scientific Reports"},"publishedOn":"2025-07-24 15:57:50","publishedOnDateReadable":"July 24th, 2025"},"versionCreatedAt":"2025-02-12 06:04:50","video":"","vorDoi":"10.1038/s41598-025-12414-8","vorDoiUrl":"https://doi.org/10.1038/s41598-025-12414-8","workflowStages":[]},"version":"v1","identity":"rs-5980745","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5980745","identity":"rs-5980745","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}