Phylogenetic plant community structure along elevation is lineage specific Charlotte Ndiribe1,2,Lo€ıc Pellissier1, Silvia Antonelli3, Anne Dubuis1, Julien Pottier1, Pascal Vittoz1, Antoine Guisan1,4,† & Nicolas Salamin1,2,† 1Department of Ecology and Evolution, University of Lausanne, Biophore, 1015 Lausanne, Switzerland 2Swiss Institute of Bioinformatics, Genopode, 1015 Lausanne, Switzerland 3Division of Biology, Imperial College London, Silwood Park Campus, Ascot, SL5 7PY, U.K. 4Institute of Earth Surface Dynamics, University of Lausanne, Geopolis, 1015 Lausanne, Switzerland Keywords Abstract Community structure, elevation gradient, mountain plants, phylogenetic clustering, The trend of closely related taxa to retain similar environmental preferences phylogenetic overdispersion. mediated by inherited traits suggests that several patterns observed at the com- munity scale originate from longer evolutionary processes. While the effects of Correspondence phylogenetic relatedness have been previously studied within a single genus or Nicolas Salamin, Department of Ecology and family, lineage-specific effects on the ecological processes governing community Evolution, University of Lausanne, Biophore assembly have rarely been studied for entire communities or flora. Here, we Building, 1015 Lausanne, Switzerland. measured how community phylogenetic structure varies across a wide elevation Tel: +41 21 692 41 54; E-mail: [email protected] gradient for plant lineages represented by 35 families, using a co-occurrence index and net relatedness index (NRI). We propose a framework that analyses Funding Information each lineage separately and reveals the trend of ecological assembly at tree This work was funded by a fellowship grant nodes. We found prevailing phylogenetic clustering for more ancient nodes and from the Faculty of Biology and Medicine overdispersion in more recent tree nodes. Closely related species may thus rap- and with additional support from the idly evolve new environmental tolerances to radiate into distinct communities, Herbette Foundation, University of Lausanne, while older lineages likely retain inherent environmental tolerances to occupy Switzerland – Swiss National Science Foundation to NS (CRS113-125240) and AG communities in similar environments, either through efficient dispersal mecha- (Grant No. 31003A-125145, project nisms or the exclusion of older lineages with more divergent environmental tol- BIOASSEMBLE) – European Commission erances. Our study illustrates the importance of disentangling the patterns of (Project FP6-ECOCHANGE) to AG. community assembly among lineages to better interpret the ecological role of traits. It also sheds light on studies reporting absence of phylogenetic signal, Received: 3 April 2013; Revised: 15 and opens new perspectives on the analysis of niche and trait conservatism September 2013; Accepted: 19 September across lineages. 2013 Ecology and Evolution 2013; 3(15): 4925– 4939 doi: 10.1002/ece3.868 †These authors shared last authorship. Introduction physiological traits that mediate species tolerance to envi- ronmental conditions and interspecific competition (Mac- Two main ecological processes are widely recognized to Arthur and Levins 1967; Weiher et al. 2011). The latter govern the assembly of communities from a regional processes has long been thought to be influenced by the species pool. First, neutral processes, which encompass pattern of shared ancestry existing between species (Cav- demographic stochasticity coupled with dispersal limita- ender-Bares et al. 2009; Vamosi et al. 2009) and will be tions and community drift, create random patterns of particularly strong if the evolution of niche traits are con- species coexistence (Hubbell 2001; Chave 2004). Second, served along phylogenetic lineages (Webb et al. 2002; niche-based processes emerge from the functional or Mayfield and Levine 2010). Phylogenetic relatedness has ª 2013 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 4925 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Lineage-Specific Phylogenetic Community Structure C. Ndiribe et al. therefore been proposed as a useful additional tool to bet- between traits within the same taxa (Parra et al. 2010). ter understand the drivers of community assembly (Webb They have prompted proposals to adopt a lineage-based et al. 2002; Losos 2008). perspective to investigating the way communities are Indeed, the recent, large interest in investigating phylo- structured (e.g., Hardy and Senterre 2007; Losos 2008; genetic niche conservatism (Wiens and Graham 2005; Vamosi et al. 2009; Parra et al. 2010), because it can bet- Wiens et al. 2010) in a wide range of organisms such as ter distinguish delicate patterns of differential species’ plants (Webb 2000; Silvertown et al. 2001), birds evolution and variations within and among communities. (Graham et al. 2009), and lizards (Losos et al. 2003) has The forces governing community assembly and how paralleled the use of phylogenetic relatedness to detect this may relate to the phylogeny do not solely vary across patterns of community assembly (Webb et al. 2002; lineages, but also change along environmental gradients. Cavender-Bares et al. 2009). In this context, patterns of This implies that neutral assembly, competition, and envi- phylogenetic clustering are expected when environmental ronmental filtering may prevail under distinct environ- filters drive species assemblages to comprise closely mental conditions (Graham et al. 2009). For instance, related species, and are plausible only under the assump- patterns similar to phylogenetic niche conservatism were tions of phylogenetically conserved traits (Webb 2000; identified in microbial communities along an elevation Vamosi et al. 2009). On the other hand, patterns of phy- gradient, while plant species were found to be less con- logenetic overdispersion are generally inferred when niche served at higher elevations than lower elevation (Bryant differentiation or ecological fitting mediates community et al. 2008). Graham et al. (2009) showed more clustered assembly (Janzen 1985; Cavender-Bares et al. 2004; Bryant bird communities at high elevation, possibly indicating a et al. 2008). Overdispersion can result either from compe- greater prevalence of environmental filtering in harsh abi- tition or facilitation, if species traits are conserved along otic conditions. Despite adopting a lineage-specific the phylogeny, or environmental filtering and if conver- approach to assessing community assembly (Parra et al. gence dominates the evolution of ecologically important 2010, 2011; Duarte et al. 2012), no study so far has, to traits (Cavender-Bares et al. 2009; Swenson and Enquist our knowledge, revealed the trends of plant phylogenetic 2009; Mayfield and Levine 2010). Investigating the phylo- community structure within a lineage-specific approach genetic structure of communities, in terms of clustering across a wide elevation gradient of the Alps. and overdispersion, can therefore provide insights into Furthermore, most studies of phylogenetic community how intrinsic and extrinsic factors influence the structure assembly have been conducted in tropical regions (e.g., of ecological communities by favouring some lineages Webb 2000; Hardy and Senterre 2007), the neotropics over the other (Vamosi et al. 2009). (e.g., Kembel and Hubbell 2006; Swenson and Enquist While in some lineages, ecological traits may be phylo- 2009), and temperate lowlands (e.g., Silvertown et al. genetically conserved, in others, they may show high evo- 2001, 2006; Cavender-Bares et al. 2004), while ecosystems lutionary lability (Cavender-Bares et al. 2004), which has along larger elevation gradients have not been considered been an important process in several examples of radia- so far. Not only do mountainous areas classically depict tion allowing the occupancy of divergent niches. This is archipelagos (Korner€ 2003), with varying functional struc- particularly visible in lineages that radiate into contrasted tures along the climatic cline (Theurillat et al. 2003; Pel- environmental conditions such as observed, for example lissier et al. 2010a), but the interplay of topographically in the Caribbean Anolis lizards (Losos et al. 2003). At the complex alpine areas with past climate change has con- other extreme, considering a wide taxonomic range tributed to a rich phylogenetic history through multiple within the angiosperms may lead to the absence of com- events of sympatric and allopatric speciation. munity phylogenetic patterns (Silvertown et al. 2006), In this study, we assess lineage-specific phylogenetic because lineages of very different ages whose evolution community patterns within angiosperms along a broad might have been governed by very different processes are elevation gradient in a temperate mountain range. We analyzed jointly. In contrast, examining phylogenetic pat- used a comprehensive community-level sampling of an terns within a specific taxonomic group is likely to reveal entire regional flora, containing all of the most abundant more distinct assembly patterns (Swenson et al. 2006; species as well as species-level phylogenetic information. Hardy and Senterre 2007; Losos 2008), as shown for the This provided the necessary context to assess the pro- Floridian oaks (Cavender-Bares et al. 2004). These studies cesses leading to community assembly