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
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6000
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Publications on Ecology
Publications on PD as proxy for
community assembly
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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.
Cahill, J.F., McNickle, G.G., Haag, J.J., Lamb, E.G., Nyanumba, S.M. & Clair, C.C.S. (2010) Plants
Integrate Information About Nutrients and Neighbors. Science,328, 1657-1657.
Cornell, H.V. (2013) Is regional species diversity bounded or unbounded? Biological Reviews,88,
140-165.
Davies, S.J., Palmiotto, P.A., Ashton, P.S., Lee, H.S. & Lafrankie, J.V. (1998) Comparative ecology
of 11 sympatric species of Macaranga in Borneo: tree distribution in relation to
horizontal and vertical resource heterogeneity. Journal of Ecology,86, 662-673.
Elias, M., Gompert, Z., Willmott, K. & Jiggins, C. (2009) Phylogenetic community ecology needs
to take positive interactions into account. Communicative & Integrative Biology,2, 113116.
Hermant, M., Hennion, F., Bartish, I.V., Yguel, B. & Prinzing, A. (2012) Disparate relatives: Life
histories vary more in genera occupying intermediate environments. Perspectives in
Plant Ecology Evolution and Systematics,14, 283-301.
Kluge, J. & Kessler, M. (2011) Phylogenetic diversity, trait diversity and niches: species assembly
of ferns along a tropical elevational gradient. Journal of Biogeography,38, 394-405.
Kozak, K.H., Mendyk, R.W. & Wiens, J.J. (2009) Can Parallel Diversification Occur in Sympatry?
Repeated Patterns of Body-Size Evolution in Coexisting Clades of North American
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processes amid species pool influences. Trends in Ecology & Evolution,27, 600-607.
Laiolo, P. (2012) Interspecific interactions drive cultural co-evolution and acoustic convergence
in syntopic species. Journal of Animal Ecology,81, 594-604.
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plants along elevational gradient in the Hengduan Mountains Region, southwest China.
Journal of Systematics and Evolution,52, 280-288.
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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
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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