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The Evolution of Seed Dispersal Is Associated with Environmental Heterogeneity in Pinus T ⁎ Diego Salazar-Tortosaa, , Bianca Saladinb, Niklaus E

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The Evolution of Seed Dispersal Is Associated with Environmental Heterogeneity in Pinus T ⁎ Diego Salazar-Tortosaa, , Bianca Saladinb, Niklaus E Perspectives in Plant Ecology, Evolution and Systematics 41 (2019) 125464 Contents lists available at ScienceDirect Perspectives in Plant Ecology, Evolution and Systematics journal homepage: www.elsevier.com/locate/ppees The evolution of seed dispersal is associated with environmental heterogeneity in Pinus T ⁎ Diego Salazar-Tortosaa, , Bianca Saladinb, Niklaus E. Zimmermannb, Jorge Castroa, ⁎ Rafael Rubio de Casasa,c,d, a Departamento de Ecología, Facultad de Ciencias, Universidad de Granada, Granada, Spain b Swiss Federal Research Institute WSL, Birmensdorf, Switzerland c Estación Experimental de Zonas Áridas, EEZA-CSIC, Almería, Spain d CEFE UMR 5175, CNRS, Universite de Montpellier, Universite Paul-Valery, Montpellier Cedex 05, France ARTICLE INFO ABSTRACT Keywords: Seed dispersal is a major life history stage for plants. Because of its influence on reproductive success, dispersal is Arid environments expected to be under strong selection. Different ecological circumstances might favour dispersal towards few Anemochory suitable sites or alternatively, the random distribution of propagules among suitable and unsuitable sites. Evolutionary rates However, the evolutionary dynamics favouring specific dispersal syndromes remain a matter of speculation in Seed many cases. Here, we explore the linkage between dispersal and environmental conditions at an evolutionary Trait evolution scale. We use a comparative phylogenetic approach to investigate the evolution of dispersal morphology in the Zoochory genus Pinus and its connection with climatic variability, aridity and fire. Our results show that dispersal appears to have evolved towards two alternative strategies: seeds with vs. without wings, closely matching the dis- tribution of wind- and vertebrate- mediated dispersal within the genus. Moreover, we find a close evolutionary association between dispersal morphology and environmental conditions such that each morphology pre- dominates under particular abiotic conditions. Seeds with bigger wings are selected for primarily in environ- ments with high temperature variability and/or prone to fire, whereas wingless or remnant-winged seeds are evolutionarily linked primarily to environments that are arid or exhibit a high variability in rainfall. These findings suggest a role of seed dispersal in the adaptation to certain environmental conditions, along with the influence of such conditions on the evolution of plant functional traits. 1. Introduction diversification (Bohrer et al., 2005). The role of dispersal as a connector of different demes is expected to Plant dispersal is the movement and establishment of offspring be particularly important if environmental heterogeneity is high (normally seeds) away from the parental patch (Herrera and Herrera, (Comins et al., 1980). When conditions vary across space and time, 2002). It has profound ecological and evolutionary consequences, as it dispersal facilitates survival by spreading risk over a higher number of determines the distribution and demography of populations (e.g. the patches. This becomes particularly adaptive when conditions at the risk of local extinctions) (Gadgil, 1971; Ronce, 2007; Willis et al., maternal patch are likely to become unsuitable over time (i.e., when the 2014). For instance, gene-flow is reduced when dispersal is limited, environment is negatively autocorrelated; Duputié and Massol, 2013). which can lead to the isolation of populations and ultimately promote As a result, selection favours dispersal mechanisms that maximize the speciation (Givnish, 2010). If populations are insufficiently connected probability of reaching a suitable patch and minimize the mortality of to maintain gene flow, demographic dynamics can foster genetic drift propagules (Ronce, 2007). among the different patches, ultimately resulting in lineage In plants, individuals move generally as seeds (Kartzinel et al., Abbreviations: PET, potential evapotranspiration; P, precipitation; W/S, ratio between wing (W) and seed (S) length; PICs, phylogenetically independent contrasts; BM, brownian motion models; OU, Ornstein–Uhlenbeck models; QuaSSE, quantitative state speciation and extinction; BAMM, Bayesian analysis of macroevolu- tionary mixture ⁎ Corresponding authors at: Departamento de Ecología, Facultad de Ciencias, Universidad de Granada, Av. Fuentenueva SN, 18071, Granada, Spain. E-mail addresses: [email protected] (D. Salazar-Tortosa), [email protected] (B. Saladin), [email protected] (N.E. Zimmermann), [email protected] (J. Castro), [email protected] (R. Rubio de Casas). https://doi.org/10.1016/j.ppees.2019.125464 Received 17 May 2018; Received in revised form 10 July 2019; Accepted 15 July 2019 Available online 17 September 2019 1433-8319/ © 2019 Elsevier GmbH. All rights reserved. D. Salazar-Tortosa, et al. Perspectives in Plant Ecology, Evolution and Systematics 41 (2019) 125464 2013; Levin et al., 2003; Wang and Smith, 2002). Seed dispersal is a key Johnson, 1993); ii) The seeds of around 24 species are dispersed by process for plant population dynamics. However, it is often conditioned vertebrates. These vectors collect seeds from cones or the ground, and by the participation of exogenous agents for transportation of the seeds then bury them in specific spots (caches). Dispersal distance differs (Schupp et al., 2010). These agents, or vectors, can be quite diverse among animals, being specially long in the case of birds (approx. 20 are ranging from abiotic factors (e.g., wind) to the participation of animals dispersed by corvids along with other vectors like rodents; Lanner, (e.g., by ingesting or caching the seeds). Some plant groups include 2000, 1996; Thayer and Vander Wall, 2005; Tomback and Linhart, clades that differ in the vectors of dispersal (e.g., wind and animal 1990); iii) Some additional species have mixed dispersal syndromes. dispersal; Vander Wall, 2001). This seems to indicate that evolution of Around 14 have been described to be dispersed by both vertebrates and dispersal traits can be closely coupled to the diversification of certain wind (see for example Vander Wall (2008, 2003)). lineages. The effectiveness of gene flow and the degree of connectivity To study the evolution of dispersal in Pinus and its association with can potentially vary across dispersal syndromes, as different vectors specific environmental conditions, we have investigated 1) whether might lead to differences in population structures and even to different selection has repeatedly favoured the emergence of two alternative rates of speciation and extinction (Goodman, 1987; Lengyel et al., 2009; (wind vs. vertebrate) strategies for dispersal, with mixed dispersal as an Levin, 2000; Qiao et al., 2016). However, in spite of its potential evo- evolutionarily transition form. Alternatively, dispersal evolution might lutionary relevance, the association between dispersal syndromes and have followed a different pattern, such as convergence towards a single plant diversification remains equivocal (Willis et al., 2014). mixed syndrome (in which case anemochory and zoochory would be The seed shadow (i.e., the dispersal kernel) is strongly influenced by just extreme cases) or the differentiation of three dispersal modes; 2) the physical characteristics of the vector that disperses the seeds. Some whether changes in dispersal syndrome can be associated with differ- vectors deposit seeds with higher probability than expected by chance ences in speciation or extinction rates across lineages, i.e., if wind or in sites where germination and early development are favoured. This animal dispersal can be linked to different diversification rates in Pinus; type of dispersal is often associated to animal vectors, and can be and 3) whether a link between environmental conditions and dispersal specially beneficial for recruitment when it also results in low density evolution can be established, such that the different dispersal syn- patterns and therefore low competition among seedlings (Howe and dromes are associated with various components of environmental het- Smallwood, 1982; Spiegel and Nathan, 2010; Wenny, 2001). Con- erogeneity, with a particular focus on the potential associations with versely, other vectors distribute seeds with stochastic probability climatic variability, aridity and fire. among suitable and unsuitable sites. For instance, when seeds are dis- persed by wind (i.e., anemochorous) the seed shadow is mostly a 2. Material and methods function of the distance to the maternal tree. This type of dispersal can be regarded as random relative to the spatial distribution of sites fa- 2.1. Functional traits, climatic and fire data vourable for recruitment (Spiegel and Nathan, 2010; although see Seiwa et al. (2008)). Under conditions of high environmental hetero- Our study system consists of 113 extant species of the genus Pinus. geneity, suitable patches would be sparse and disconnected, which Phylogenetic relationships were inferred by a Bayesian analysis using could increase the advantage of specific dispersal to suitable sites by BEAST (v1.8.0; Drummond and Rambaut, 2007) from eight plastid gene scatter-hoarders (Pesendorfer et al., 2016; Purves et al., 2007; Spiegel regions (matK, rbcL, trnV, ycf2, accD, rpl20, rpoB and rpoC1). The gene and Nathan, 2010). It has been posited that environmental factors af- tree obtained was ultrametric and was dated in BEAST using the node fecting the temporal variability in recruitment and growth, such as dating method where the fossil ages were transformed into calibration aridity and
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