Functional Ecology Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold1; James F Cahill, Jr2; Marten Winter3; Igor V Bartish4 and Andreas Prinzing5,6 1 Department of Botany, Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia. E-mail: pille.gerhold@ut.ee; 2 Department of Biological Sciences, University of Alberta, Edmonton, Alberta, T6G 2E9, Canada. E-mail: jc.cahill@ualberta.ca; 3 German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany. E-mail: marten.winter@idiv.de; 4 Department of Genetic Ecology, Institute of Botany, Academy of Sciences, CZ-25243 Pruhonice 1, Czech Republic. E-mail: Igor.Bartish@ibot.cas.cz; 5 University Rennes 1 / Centre National de la Recherche Scientifique, Research Unit “Ecosystèmes Biodiversité, Evolution” (« UMR 6553 »), Campus Beaulieu, Bâtiment 14 A, 35042 Rennes, France. E-mail: Andreas.Prinzing@univ-rennes1.fr; 6 Alterra, Wageningen UR (University & Research Centre), PO Box 47, NL-6700 AA Wageningen, The Netherlands. Corresponding author: Pille Gerhold, Department of Botany, Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia. E-mail: pille.gerhold@ut.ee. Running headline: Phylogenies and community assembly Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology SUPPORTING INFORMATION Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology Figure S1 Number of publications (black dots) on the topic (("phylogenetic diversity" or "phylogenetic* *dispers*") and (compet* or filter*)) in the Core Collection of Thomson Corporation ISI Web of Knowledge on November, 11, 2014. The total number of publications is 184, the sum of the times cited is 4604, the average citations per item are 25.02, and h-index is 39. Many if not most of these publications consider phylogenetic dispersion of communities as a proxy for community assembly. The number of publications on “Ecology” (grey rhombs) is shown for comparison. 30 8000 20 6000 10 Publications on Ecology Publications on PD as proxy for community assembly 10000 40 4000 0 1996 2002 2008 2014 Year Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology Appendix S1 Possible detriments to other approaches in community ecology Independent of the concern over the validity of the assumptions outlined in this paper we see a risk of collateral damage associated with reliance on process inference from phylogenetic patterns. Collateral damage may be caused when interesting insights are missed and useful approaches and understanding are lost, due to an exaggerated focus on the application of phylogenetic dispersion as a proxy for community assembly. 1. Losing track of functional traits In some cases, phylogenetic information alone might be more powerful for identifying functional trait structure of communities than – available - information on functional traits alone. This might be the case for subtle, often poorly understood interactions between hosts and enemies depending on poorly studied biochemical functional traits (Cadotte et al. 2009) or when traits are only coarsely related to a physiological process of interest (Swenson 2013). Nevertheless, independent information on both traits and phylogenies will always permit richer inferences than interpreting phylogenies only, despite the limitations of inferring assembly from trait similarity (assumptions 2 and 3 above).Studies relying exclusively on phylogenies hence imply a threat of losing track of functional traits and the degree to which their local variation reflects variation in phylogenetic positions of species or other factors. This creates the risk of overlooking the traits actually available for many taxa in many regions (e.g. Kühn, Durka & Klotz 2004), going far beyond classifications into functional-traitgroups. It is also important to recall that phylogenies may be more informative about traits that do not have an ecological function than about traits that do. In plants, for instance, phylogenies tend to strongly reflect the anatomical structure of fruits (such as nuts vs. berries), which in itself is only little Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology related to the function such as fleshiness (e.g. nuts may or may not be fleshy; Frohne & Jensen 1988; Manchester & O'Leary 2010). Overall, phylogenies may remain a valuable proxy for unknown traits, notably those influencing the relationship with natural enemies and mutualists. But considering phylogenies in general better than traits in ecological studies appears in many cases exaggerated (Winter, Devictor & Schweiger 2013 for another example). Inversely, combining information on phylogenies and traits can help us identify, for instance, which aspect of a trait dispersion pattern might reflect the phylogenetic imprint from the habitat species pools and which reflects uniquely local ecological processes such as competitive exclusion. 2. Paucity of hypotheses asked Many of the present studies from community phylogenetics ask one or both of the following questions: What is the relative importance of habitat filtering vs. competition (including other negative density-dependent interactions)? And: What is the relative importance of niche and neutrality? While these are interesting questions central to the field of community ecology, the lack of other questions is noticeable. Technical advancement cannot replace conceptual advancement, and the latter comes to a large degree due to novel hypotheses. Many studies claim to aim at “coming to a deeper understanding” (see Pavoine et al. 2011; Cadotte et al. 2010, among many others). However, the precise nature of this deeper understanding is often less clear, mechanistic hypotheses remain vague. For example, it has been suggested that that phylogenetic proximity increases the probability of negative density-dependent interactions, i.e. where the increased density of one species decreases the density of another (e.g. Webb et al. 2002). However, this is a very big and abstract group of mechanisms, including among others interference competition for instance via allelopathy, resource competition via shading, apparent competition via shared predators where one Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology prey species increases the population of a predator species that then reduces the populations of another prey species, apparent competition via shared pathogens, or apparent competition via shared mutualists where numbers of mutualists are limited. Pooling all these interactions into a single category may often be too rough to come to deep insights into these interactions. Studies that do so remain valuable, but admittance of their descriptive and explorative nature would likely help to communicate the need for more mechanistic hypotheses and tests. 3. Losing track of natural history The approach of using phylogenetic dispersion as a proxy for community assembly is based on sophisticated techniques of constructing phylogenies, inferring parameters from these phylogenies and developing appropriate null-models to assess the significance of these parameters. Inevitably, this takes a lot of time, and often requires specific molecular-lab and programming competences. Time and brain space being limited, investment into the molecular-lab and programming may be detrimental to other competences and activities by any individual researcher, notably understanding the natural history of the study organisms. For centuries the study of community assembly has gained a lot from an intimate knowledge of the natural history of the study organisms, both in field observations and in controlled experiments (e.g. Hairston 1989; Wiens 1992). This intimate knowledge of study organisms in the field should be improved and more intensively integrated into community assembly studies. This could even be in the interest of the molecular lab and programming work. It is a major loss if such work ultimately leads to general conclusions that may seem already well-established in natural history (such as the successive establishment of new lineages through forest succession, known at least since Thoreau 1860). Moreover, knowing the natural history of the study organisms also helps to identify the pertinent environmental covariables to be accounted for such (e.g. Yguel et al. 2011) – to better identify existing relationships and avoid pseudo-correlations. Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology Supplementary references: Cadotte, M.W., Cavender-Bares, J., Tilman, D. & Oakley, T.H. (2009) Using Phylogenetic, Functional and Trait Diversity to Understand Patterns of Plant Community Productivity. Plos One,4, 9. Cadotte, M.W., Jonathan Davies, T., Regetz, J., Kembel, S.W., Cleland, E. & Oakley, T.H. (2010) Phylogenetic diversity metrics for ecological communities: integrating species richness, abundance and evolutionary history. Ecology Letters,13, 96-105. Frohne, U. & Jensen, U. (1988) Systematik des Pflanzenreichs, 5th edn. Wissenschaftliche Verlagsgesellschaft, Stuttgart, Germany. Hairston, N.G. (1989) Ecological Experiments. Purpose, Design and Execution. Cambridge University Press, Cambridge. Kühn, I., Durka, W. & Klotz, S. (2004) BiolFlor - a new plant-trait database as a tool for plant invasion ecology. Diversity and Distributions,10, 363-365. Manchester, S.R. & O'Leary, E.L. (2010) Phylogenetic Distribution and Identification of Fin-winged Fruits. Botanical Review,76, 1-82. Pavoine, S., Vela, E., Gachet, S., de Belair, G. & Bonsall, M.B. (2011) Linking patterns in phylogeny, traits, abiotic variables and space: a novel approach to linking environmental filtering and plant community assembly. Journal of Ecology,99, 165-175. Swenson, N.G. (2013) The assembly of tropical tree communities – the advances and shortcomings of phylogenetic and functional trait analyses. Ecography,36, 264–276. Webb, C.O., Ackerly, D.D., McPeek, M.A. & Donoghue, M.J. (2002) Phylogenies and community ecology. Annual Review of Ecology and Systematics,33, 475-505. Wiens, J.A. (1992) The Ecology of Bird Communities. Cambridge University Press. Winter, M., Devictor, V. & Schweiger, O. (2013) Phylogenetic diversity and nature conservation: where are we? Trends in ecology & evolution (Personal edition),28, 199-204. Yguel, B., Bailey, R., Tosh, N.D., Vialatte, A., Vasseur, C., Vitrac, X., Jean, F. & Prinzing, A. (2011) Phytophagy on phylogenetically isolated trees: why hosts should escape their relatives. Ecology Letters,14, 1117-1124. Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology Table S1 Hypotheses on how ecological assembly processes may result in macroevolutionary patterns, i.e. phylogenetic-patterns-as-result approach instead of using phylogenetic-patterns-asproxy approach. These assembly processes are not inferred but verified by tests. If confirmed these processes may result in macroevolutionary patterns. For instance, should harsh environments indeed filter closely related species, this will favor the sympatry of related species within the same region and their ecological convergence into the same niche, notably in lineages occupying such harsh habitats. Assembly processes include those believed by the phylogenetic-patterns-as-proxyapproach, but also the seven caveats we identify. “Niche conservatism” is used sensu Wiens et al. (2010), equivalent to “phylogenetic signal” sensu Losos (2008). Note also that some of the resulting macroevolutionary patterns feedback on trait conservatism. They do so either positively by convergence among closely related species, or negatively by divergence among closely related species or by convergence among distantly related species. References indicate studies that have treated the suggestion in a given field. Note that these studies rarely cover the entire range of lineages of a major taxon, or the entire range of environments available in a region. None of these studies covers two or more fields from left to right, form ecological process, via description of the macroevolutionary pattern, to the lineages/habitats where one might expect the process. Ecological assembly process Possible test of process (rather than inference from proxies) Hypotheses suggested by phylogenetic-patterns-asresult approach Macroevolutionary Lineages, habitats or traits in pattern resulting from which this ecological process assembly process is expected to operate and influence macroevolution Ecological processes believed to be true by phylogenetic-patterns-as-proxy approach Physiologically harsh abiotic environments filter closely related species Does increasing harshness decrease phylogenetic dispersion? (Li et al. 2014) Sympatry and convergence of niches among closely related species (Hermant et al. 2012) Lineages occupying harsh environments Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology Closely related species mutually outcompete each other Does increasing competition increase phylogenetic dispersion? (Bennett et al. 2013) Allopatry or niche divergence of closely related species (Davies et al. 1998), ultimately slows down diversification within region (Cornell 2013) Lineages occupying habitat types with many competitors Ecological processes suggested as caveats of the phylogenetic-patterns-as-proxy approach (Fig. 1) Communities may select for related dissimilar species, despite regional niche conservatism Do, among a set of closely related species, only dissimilar ones survive? (Prinzing et al. 2008) Sympatry and trait divergence among closely related species (Okuzaki, Takami & Sota 2010; Kozak, Mendyk & Wiens 2009) Lineages of only moderate trait conservatism. Lineages in habitats of high competition pressure Multiple traits, occurring in multiple lineages, may serve the same function Does, within the same habitat, fitness depend on different traits in different lineages? Sympatry and trait divergence among distantly related species Lineages in habitats of high spatio-temporal heterogeneity, permitting different ecological strategies (e.g. annual and perennial plants in deserts) Trait similarity may facilitate coexistence Does increasing trait similarity to neighbours increase fitness gain, e.g. due to increased assistance of mutualists? (Sargent et al. 2011) Sympatry and trait convergence among closely related species (Elias et al. 2009) Lineages interacting with mutualists that can be attracted by similar, related neighbours (e.g. pollinators) Competition may be symmetric and without losers or winners Are competition coefficients among closely related species more symmetric than among distantly related species? Trait convergence of sympatric related species (Cahill et al. 2010; Laiolo 2012) Traits that are important in symmetric competition, such as root traits in plants Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology Frequent/recent disturbances may prevent competitive exclusion of species Does disturbance increase the persistence of related species in communities and reduce checkerboardness between communities? Sympatry does not depend on relatedness (Phillips et al. 2013) Lineages living in frequently disturbed habitats Habitat filtering and competition are independent, increase in parallel or mutually imply each other Are competition coefficients unrelated to levels of abiotic harshness? Are they positively related? (Bowker, Soliveres & Maestre 2010) Joint evolution of traits related to competition and to tolerance to harsh abiotic environment Lineages in habitats in which (i) competitors control abiotic filters (e.g. shading), (ii) abiotic resource limitation increases the importance of biotic competition Phylogenetic dispersion of local communities may reflect that of the corresponding lineage-pool, not local processes Does mean local phylogenetic dispersion of habitat types reflect that of the lineagepools? Does this depend on habitat type? (Lessard et al. 2012) Sympatry of closely related species within particular habitat types but not within others (Prinzing et al. 2008; Kluge & Kessler 2011) Lineages in habitats characterized by environmental factors that are geologically ancient and never entirely disappeared, such as inundation or grazing Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology Supplementary references: Bennett, J.A., Lamb, E.G., Hall, J.C., Cardinal-McTeague, W.M. & Cahill, J.F. (2013) Increased competition does not lead to increased phylogenetic overdispersion in a native grassland. Ecology Letters,16, 1168-1176. Bowker, M.A., Soliveres, S. & Maestre, F.T. (2010) Competition increases with abiotic stress and regulates the diversity of biological soil crusts. Journal of Ecology,98, 551-560. 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(2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters,11, 995-1003. Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing Functional Ecology Okuzaki, Y., Takami, Y. & Sota, T. (2010) Resource partitioning or reproductive isolation: the ecological role of body size differences among closely related species in sympatry. Journal of Animal Ecology,79, 383-392. Phillips, R.D., Xu, T.B., Hutchinson, M.F., Dixon, K.W. & Peakall, R. (2013) Convergent specialization - the sharing of pollinators by sympatric genera of sexually deceptive orchids. Journal of Ecology,101, 826-835. Prinzing, A., Reiffers, R., Braakhekke, W.G., Hennekens, S.M., Tackenberg, O., Ozinga, W.A., Schaminee, J.H.J. & van Groenendael, J.M. (2008) Less lineages - more trait variation: phylogenetically clustered plant communities are functionally more diverse. Ecology Letters,11, 809-819. Sargent, R.D., Kembel, S.W., Emery, N.C., Forrestel, E.J. & Ackerly, D.D. (2011) Effect of Local Community Phylogenetic Structure on Pollen Limitation in an Obligately InsectPollinated Plant. American Journal of Botany,98, 283-289. Wiens, J.J., Ackerly, D.D., Allen, A.P., Anacker, B.L., Buckley, L.B., Cornell, H.V., Damschen, E.I., Davies, T.J., Grytnes, J.A., Harrison, S.P., Hawkins, B.A., Holt, R.D., McCain, C.M. & Stephens, P.R. (2010) Niche conservatism as an emerging principle in ecology and conservation biology. Ecology Letters,13, 1310-1324. Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better) Pille Gerhold; James F Cahill, Jr; Marten Winter; Igor V Bartish and Andreas Prinzing