More closely related species are more ecologically similar in an experimental test Jean H. Burns1,2 and Sharon Y. Strauss Center for Population Biology, University of California, Davis, CA 95616 Edited by Johanna Schmitt, Brown University, Providence, RI, and approved February 16, 2011 (received for review September 1, 2010) The relationship between phylogenetic distance and ecological similarity is key to understanding mechanisms of community as- sembly, a central goal of ecology. The field of community phylo- genetics uses phylogenetic information to infer mechanisms of community assembly we explore, the underlying relationship be- tween phylogenetic similarity and the niche. We combined a field experiment using 32 native plant species with a molecular phylog- eny and found that closely related plant species shared similar germination and early survival niches. Species also competed more with close relatives than with distant relatives in field soils how- ever, in potting soil this pattern reversed, and close relatives might even have more mutalistic relationships than distant relatives in these soils. Our results suggest that niche conservatism (habitat filtering) and species interactions (competition or facilitation) structure community composition, that phylogenetic relationships influence the strength of species��� interactions, and that conserved aspects of plant niches include soil attributes. Darwin���s naturalization hypothesis | phylogenetic signal Agoverninggoal primary of ecology is to understand the processes species coexistence and how species are assem- bled into communities. As Donoghue (1) notes, ���As we proceed to predict responses to global change, I believe it will be neces- sary to acknowledge and more finely characterize the spectrum that exists in the evolutionary lability of ecologically relevant traits��� (1). Models of community assembly make predictions about how species��� differences affect the likelihood of coexistence (2���6). Stable coexistence requires competitors to differ in their niches, and species that are too ecologically similar cannot coexist (limiting similarity) (2, 7, 8). Although highly similar species with nearly equal fitness maydelay competitive exclusionthroughnearly neutral dynamics, species differences are ultimately required for stable coexistence (9, 10). Intersecting with this discussion of ecological similarity and coexistence is the degree to which phylogenetic relatedness be- tween species reflects their ecological similarity and thus, can be used to understand coexistence and community assembly (11). Community phylogenetics use patterns of relatedness among species in existing communities to infer the processes governing assembly (11���18). Typically, communities in the field are sam- pled, and the distribution of phylogenetic distances between coexisting species is compared with that of null communities that are randomly assembled from the regional species pool. Two mechanisms are commonly invoked when existing communities differ from randomly assembled ones. Limiting similarity is inferred as an important organizing process when communities are comprised of species more distantly related than expected by chance or communities are more evenly represented across the phylogenetic tree than expected (11, 12). In contrast, environ- mental filtering is often invoked to explain phylogenetically clustered coexisting species (13, 17, 19) (that is, closely related species that co-occur in similar environments as a result of shared traits). A basic assumption for both of these interpretations of phy- logenetic pattern is that phylogenetic relatedness is correlated with ecological similarity. Several hypotheses to explain com- munity structure explicitly predict a link between ecological similarity and phylogenetic relatedness. Darwin���s (20) naturali- zation hypothesis predicts that introduced species closely related to the native community are less likely to be successful colonists than are more distantly related introduced species as a result of competitive exclusion between close relatives (20). Darwin (20) argued that closely related species compete most intensely, be- cause they have similar morphologies and niches. However, the degree to which close relatives are similar in niche is still debated (21). Some studies find evidence for phylogenetic signal in niche characteristics (22), whereas others find that important aspects of the niche are highly labile with respect to ancestry (23, 24). With few exceptions, these studies are observational (25, 26), and there has been a call for more experimental studies (13). Owing to their sessile nature, plants can be experimentally placed into the niches of close and distant relatives in the field and then assessed for their performance. We ask whether and to what degree two important aspects of the plant niche���the germination niche and the strength of species interactions (i.e., competition and facilitation)���scale with phylogenetic relatedness. Note that, by measuring plant performance directly, we bypass the potential complications of choosing appropriate traits to measure to best characterize niche differences among species (27). Germination has been shown to be a key process in de- termining plant community composition (28, 29), because a crit- ical aspect of plant success is the ability to germinate and survive in a habitat (28, 29). We asked whether germination and early survival niches in the field are phylogenetically conserved using a field transplant experiment with native species growing at the Bodega Bay Marine Reserve. Each of the 32 focal species was planted into the microhabitats of four relatives that varied in their phylogenetic distance from the focal species. Although phy- logenetic distance was calculated as a continuous metric, the planting sites were originally assigned at random from the species list of the reserve based on taxonomic rank (conspecific, conge- ner, confamilial, and distant relatives). By planting species into the unaltered habitats of their relatives in the field, we included both biotic and abiotic components of the realized niche in our estimation of niche similarity. We then correlated focal species performance with the phylogenetic distance separating the focal species and the destination species (Fig. S1 and Table S1). Additionally, to test whether species interact more strongly (through competition or facilitation) with close relatives than with distant relatives (11, 19, 20), we conducted a species in- teraction experiment in an outdoor lath house. We grew a focal species both alone and with interactors that varied in phyloge- Author contributions: J.H.B. and S.Y.S. designed research, performed research, analyzed data, and wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. 1 To whom correspondence should be addressed. E-mail: jbm122@case.edu. 2 Present address: Department of Biology, Case Western Reserve University, Cleveland, OH 44106-7080. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. 1073/pnas.1013003108/-/DCSupplemental. 5302���5307 | PNAS | March 29, 2011 | vol. 108 | no. 13 www.pnas.org/cgi/doi/10.1073/pnas.1013003108

netic distance from the focal species. These interaction experi- ments were carried out in field soils collected under species that varied in their phylogenetic distance from the focal species. If close relatives are ecologically similar, then we predict that they may experience either greater competition when grown with one another or greater facilitation if, for example, they share soil mutualists. If abiotic or biotic soil characteristics are an impor- tant part of the plant niche, we might also expect the strength or pattern of interactions to vary across soil types and with phylo- genetic distance. Results and Discussion We found that phylogenetic relatedness predicted ecological similarity in both germination and early survival rates as well as in the strength of species interactions. The germination niche was strongly conserved across most species in this study, con- sistent with a role of habitat filtering in the assembly of these communities. We found a negative relationship between phylo- genetic distance and germination rate (Fig. 1A, Table 1, and Tables S2���S4) as well as for germination plus survival over the first 3 mo (last census) (Fig. 1B, Table 1, and Tables S2 and S4). Most species performed best at conspecifics��� and congeners��� sites and less well at confamilials��� and distant relatives��� sites (Fig. S2 and Table S4). The negative relationship between germination and phylogenetic distance was robust to different methods of estimating phylogenetic distance (Fig. S2). Phylogenetic distance also scaled with taxonomic ranks as one might expect (conge- ners = 30 �� 0.62 Mya SE confamilials = 81 �� 0.75 Mya SE distant = 264 �� 1.36 Mya SE) and was nonoverlapping among ranks (Fig. S2). Functional groups behaved similarly, with spe- cies performing less well at distant relatives��� sites, even if those distant relatives were Fabaceae, which could be expected to fa- cilitate distant relatives because of the presence of soil mutualists such as rhizobia and mycorrhizae (Table S4). These germination and early survival patterns could be driven by multiple possible mechanisms, including shared adaptations to soil nutrient profiles, soil moisture or texture, soil biota, or herbivores, to name just a few niche axes. Although the goal of this study was to determine patterns, not mechanisms, we have some information about potential drivers of conservatism of the germination niche. First, differences in herbivory among sites could have influenced patterns with respect to early survival among sites (30), especially if herbivory is not independent of phylogenetic distance (30). We found that the amount of above- ground herbivory was low, did not differ significantly among sites, and tended to be greater at close relatives��� than distant relatives��� sites (site type effect: ��2 = 5.24, P 0.15 conspecific: 0.004 �� 0.002 congener: 0.005 �� 0.003 confamilial: 0.003 �� 0.002 dis- tant: 0% damage because of herbivory). The negative relationship between damage from herbivores and phylogenetic relatedness is consistent with other reports in the literature (30), and if it were a major driver of our patterns of niche similarity, it should result in increased survivorship with increasing phylogenetic distance, a result diametrically opposed to the pattern we found. Second, it is possible that lower germination at phylogeneti- cally distant relatives��� sites could be the result of a greater like- lihood that those sites belong to a different habitat type (e.g., coastal prairie, dune, or seep) (Fig. S1). However, most planting sites were in coastal prairie habitat and spanned the range of phylogenetic distance treatments, such that patterns in germi- nation were not driven by gross differences in habitat type across destination sites (Table S3). Third, we explored if there was any spatial signal in the distribution of relatives at Bodega Bay Ma- rine Reserve. Geographic distance between sites of species was positively related to phylogenetic distance between these same species (slope = 0.26 P 0.001), a result suggesting significant spatial autocorrelation in shared niche attributes such as biotic or abiotic soil characteristics (31). However, phylogenetic dis- tance was a much better predictor of germination and early survival than geographic distance (Table S2). More experiments and data collections are needed to determine which mechanisms are the greatest contributors to this pattern of phylogenetic conservation of the germination niche. We also found evidence for phylogenetic conservation of the strength of species interactions in field soils, consistent with an environment-dependent role for competition and facilitation in driving community assembly patterns at Bodega Bay Marine Reserve (Fig. 2, Figs. S3 and S4, Table 2, and Table S5). We found that most species performed better when grown with dis- tant than with close relatives in field soils (Fig. 2, Table 2, and Fig. S4). Mortality in some soils prevented our running a full model with all interactions with soil type (Table 2). To explore interactions between soil type and the effect of phylogenetic distance, we conducted sign tests. We found that the slope re- lating phylogenetic distance to relative interaction intensity (RII) was positive for 10 of 12 species in conspecific soil, 9 of 12 species in congeneric soil, and 11 of 12 species in confamilial soil (sign tests significant for conspecific and confamilial soils were 0.01 P 0.04), but there was no consistent relationship be- A Proportion total germination (sqrt) Phylogenetic distance (MY) 0.15 0.10 0.05 0.00 0 50 250 100 200 150 Germination and survival last census (sqrt) 0 50 250 100 200 150 B 0.09 0.06 0.03 0.00 Fig. 1. (A) The germination niche was phylogenetically conserved. There was a negative relationship between total germination and phylogenetic distance in the mixed model with species and the interaction between species and phylogenetic distance as random effects (Table 1). (B) Germination and early survival were also phylogenetically conserved for the majority of species (last census) (Table 1). Significant slopes in black (Table S4) conditional prediction lines are from the mixed model. Burns and Strauss PNAS | March 29, 2011 | vol. 108 | no. 13 | 5303 ECOLOGY