Evolutionary diversity in tropical tree communities peaks at intermediate precipitation

Abstract

Global patterns of species and evolutionary diversity in plants are primarily determined by a temperature gradient, but precipitation gradients may be more important within the tropics, where plant species richness is positively associated with the amount of rainfall. The impact of precipitation on the distribution of evolutionary diversity, however, is largely unexplored. Here we detail how evolutionary diversity varies along precipitation gradients by bringing together a comprehensive database on the composition of angiosperm tree communities across lowland tropical South America (2,025 inventories from wet to arid biomes), and a new, large-scale phylogenetic hypothesis for the genera that occur in these ecosystems. We find a marked reduction in the evolutionary diversity of communities at low precipitation. However, unlike species richness, evolutionary diversity does not continually increase with rainfall. Rather, our results show that the greatest evolutionary diversity is found in intermediate precipitation regimes, and that there is a decline in evolutionary diversity above 1,490 mm of mean annual rainfall. If conservation is to prioritise evolutionary diversity, areas of intermediate precipitation that are found in the South American ‘arc of deforestation’, but which have been neglected in the design of protected area networks in the tropics, merit increased conservation attention.

Full text

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Evolutionary diversity in tropical
tree communities peaks at
intermediate precipitation
Danilo M. Neves1,20*, Kyle G. Dexter2,3,20, Timothy R. Baker4, Fernanda Coelho de Souza4,5,
Ary T. Oliveira-Filho1, Luciano P. Queiroz6, Haroldo C. Lima7, Marcelo F. Simon8,
Gwilym P. Lewis9, Ricardo A. Segovia2,10, Luzmila Arroyo11, Carlos Reynel12,
José L. Marcelo-Peña12, Isau Huamantupa-Chuquimaco7,13, Daniel Villarroel11,
G. Alexander Parada11, Aniceto Daza12, Reynaldo Linares-Palomino12,14,
Leandro V. Ferreira15, Rafael P. Salomão15,16, Geovane S. Siqueira17,
Marcelo T. Nascimento18, Claudio N. Fraga7 & R. Toby Pennington3,19
Global patterns of species and evolutionary diversity in plants are primarily determined by a
temperature gradient, but precipitation gradients may be more important within the tropics, where
plant species richness is positively associated with the amount of rainfall. The impact of precipitation
on the distribution of evolutionary diversity, however, is largely unexplored. Here we detail how
evolutionary diversity varies along precipitation gradients by bringing together a comprehensive
database on the composition of angiosperm tree communities across lowland tropical South America
(2,025 inventories from wet to arid biomes), and a new, large-scale phylogenetic hypothesis for the
genera that occur in these ecosystems. We nd a marked reduction in the evolutionary diversity of
communities at low precipitation. However, unlike species richness, evolutionary diversity does not
continually increase with rainfall. Rather, our results show that the greatest evolutionary diversity
is found in intermediate precipitation regimes, and that there is a decline in evolutionary diversity
above 1,490 mm of mean annual rainfall. If conservation is to prioritise evolutionary diversity, areas of
intermediate precipitation that are found in the South American ‘arc of deforestation’, but which have
been neglected in the design of protected area networks in the tropics, merit increased conservation
attention.
Given predictions of increased temperature and precipitation extremes1, it is imperative to understand the mech-
anisms driving the distribution of biodiversity along climatic gradients. Recent macroecological studies2,3 have
shown that the inability of most plant lineages to survive regular frost may underlie the latitudinal diversity gra-
dient for owering plants (angiosperms), which are most species-rich and evolutionarily diverse in the tropics3–9.
1Department of Botany, Federal University of Minas Gerais, Belo Horizonte, 31270-901, Brazil. 2School of GeoSciences,
University of Edinburgh, Edinburgh, EH9 3JN, UK. 3Royal Botanic Garden Edinburgh, Edinburgh, EH3 5LR, UK. 4School
of Geography, University of Leeds, Leeds, LS2 9JT, UK. 5Departamento de Engenharia Florestal, Universidade de
Brasília, Brasília, 70910-900, Brazil. 6Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana,
Feira de Santana, 44036-900, Brazil. 7Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, 22460-
030, Brazil. 8EMBRAPA Recursos Genéticos e Biotecnologia, Brasília, 70770-200, Brazil. 9Comparative Plant and
Fungal Biology Department, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK. 10Instituto de Ecología
y Biodiversidad (IEB), Universidad de Chile, Santiago, Chile. 11Museo de Historia Natural Noel Kempff Mercado,
Universidad Autónoma Gabriel René Moreno, Santa Cruz de la Sierra, 2489, Bolivia. 12Facultad de Ciencias Forestales,
Universidad Nacional Agraria La Molina, Lima, 15024, Peru. 13Universidad Nacional de San Antonio Abad del Cusco,
Cusco, 08000, Peru. 14Smithsonian Conservation Biology Institute, Lima, 15001, Peru. 15Coordenação de Botânica,
Museu Paraense Emilio Goeldi, Belém, 66077-530, Brazil. 16Universidade Federal Rural da Amazônia, Belém, 66077-
530, Brazil. 17Reserva Natural Vale, Linhares, 29909-030, Brazil. 18Laboratório de Ciências Ambientais, Centro de
Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, 28013-620, Brazil.
19Department of Geography, University of Exeter, Exeter, EX4 4RJ, UK. 20These authors contributed equally: Danilo M.
Neves and Kyle G. Dexter. *email: dneves@icb.ufmg.br
OPEN
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While there is compelling evidence for the importance of frost in shaping patterns of species and evolutionary
diversity of plants2,3, drought is another major axis of environmental stress that merits attention. Patterns of vari-
ation in angiosperm species richness across tropical drought gradients are clear: species richness is highest under
the wettest conditions4–8. However, unlike frost, there are no studies that examine the role of drought in driving
patterns of evolutionary diversity at large spatial scales.
Our understanding of the inuence of evolutionary history on major gradients in the global distribution of
biodiversity is framed by two hypotheses. e importance of climatic history for the latitudinal diversity gradient
has given rise to the ‘Out of the Tropics’ Hypothesis10 (OTH), which builds upon the assumption that many major
clades of animals and plants originated and initially diversied when the Earth’s climate was primarily warm and
wet10–13. e Tropical Conservatism Hypothesis11,12,14,15 (TCH) is complementary to the OTH, and proposes that
lineages associated with climatic extremes (e.g., strong seasonal frost and drought) are descendants of clades
from warmer and wetter regions and derived from a small subset of lineages that developed the necessary inno-
vations to thrive in harsh conditions. us, if greater time for diversication in the wet tropics and ancestral
preferences for such conditions were the primary forces shaping diversity patterns across large-scale gradients of
both temperature2,3 and precipitation, we would expect wet tropical environments to hold the greatest amount of
evolutionary diversity.
Alternatively, phylogenetic conservatism for harsh environments may play a distinct role in shaping evolution-
ary diversity patterns across climatic gradients. Phylogenetic conservatism for dry biomes has been demonstrated
for multiple plant clades, and these can be tens of millions of years old15. If these clades spill out of dry extremes
into areas with intermediate precipitation to coexist with members of the majority of angiosperm clades that
prefer high rainfall environments, we may expect areas with intermediate precipitation to have higher amounts
of evolutionary diversity because they can contain specialised lineages from both extremes. We refer to this alter-
native hypothesis as the ‘Environmental Crossroads Hypothesis’ (ECH). Previous research on patterns of species
richness across climatic gradients have both supported16–18 and failed to support the ECH4–8, but we do not know
of studies that have tested it from an evolutionary perspective.
Testing the validity of these hypotheses in an evolutionary context requires large-scale data on the distribution
and phylogenetic relationships of multiple lineages along gradients of environmental stress. In contrast to prior
studies of evolutionary diversity in the tropics19,20, this study is based on continental-scale sampling that suciently
covers tropical climatic gradients. We use a database of 2,025 tree communities from moist forests to savannas and
dry woodlands, covering the full breadth of environmental space of lowland tropical South America (http://neotrop-
tree.info). We then combine it with a new time-scaled molecular phylogeny for 852 angiosperm genera (Figs.1 and
S1), which represent 93% of the genera occurrences and 99% of species occurrences in the database.
Figure 1. Time-calibrated molecular phylogeny of 852 angiosperm genera found in lowland tree communities
of tropical South America. Phylogenetic reconstruction based on sequences of rbcL and matK plastid regions
from plants collected during eldwork or available in GenBank. Tree topology and divergence times of taxa
were estimated using a Bayesian Markov Chain Monte Carlo approach. Branch lengths were time-scaled using
a relaxed molecular clock with fossil-based age constraints implemented on nodes (Appendix1). Colours
represent mean annual precipitation (MAP), with warmer colours indicating drier conditions. e minimum
and maximum MAP are given. Scale (length) is in myrs and is equivalent to branch lengths in the phylogeny
(80 myrs). Dotted lines indicate 1,200 mm and 1,800 mm of MAP. Black circles indicate the nodes comprising
lineages from the major angiosperm clades: Magnoliids, Monocots, Superrosids, Superasterids. Black squares
indicate nodes comprising some of the dry-adapted lineages that are absent or have a much lower frequency of
occurrence in wet environments, at least as trees (e.g., Cactaceae, Zygophyllaceae, Asteraceae; see Discussion).
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Quantifying evolutionary diversity is of interest from both biodiversity conservation and ecosystem function
perspectives. e importance of conserving areas of high evolutionary diversity has been widely recognised21,22,
and recent studies show that ecosystem function should also be higher in areas of greater evolutionary diver-
sity23–28 (e.g., higher plant community productivity25–28). While many metrics have been developed to quantify
evolutionary diversity in ecological communities29, we employ Faith’s Phylogenetic Diversity21 (the sum of all
branch lengths in a given community; PD), as it aligns most closely with the richness dimension of evolutionary
diversity29. However, raw PD is strongly correlated with taxonomic richness20,22, thus being strongly aected by
sample eort. Our dataset includes a large number of sites across the breadth of environmental gradients, but the
sampling eort varies, which will inuence the number of taxa found, and raw PD values. We therefore focus our
analyses on the standardised eect size of PD, a metric we refer to as lineage diversity – a measure of the excess
or decit of PD given the number of genera found in a sample. Specically, we use lineage diversity estimates to
address the predictions stemming from the OTH, TCH and ECH, and to provide conservation insights that go
beyond approaches relying upon species richness alone.
Results
We found strong and clear phylogenetic signal for the precipitation conditions in which genera occur (λ = 0.5;
P < 0.001). Closely related genera are more likely to occur under a similar precipitation regime(measured as
mean annual precipitation; henceforth MAP). In addition, the clades that are comprised largely of genera in dry
regions (MAP<1200 mm, red and orange in Fig.1) tend to be young compared to clades comprised largely of
genera in wetter regions (MAP>1800 mm, green and blue in Fig.1). ese results are expected and in agree-
ment with the OTC, TCH and ECH. Contrary to predictions from the OTH or TCH, whereby highest lineage
diversity would be found in wetter regions, we nd that communities in areas with intermediate MAP have the
highest lineage diversity (Fig.2). A piecewise regression model, whereby a break-point is identied between two
non-overlapping linear regressions, provided a better t to the lineage diversity and MAP relationship (r2 = 0.48;
P < 0.001) than a linear regression (r2 = 0.16; P < 0.001) or a quadratic polynomial, ‘hump-shaped’ model
(r2 = 0.42; P < 0.001) (TableS1 and Fig.S2 in Supplementary Materials).
e break-point that represents the peak in lineage diversity was identied at 1,490 mm of MAP, with lin-
eage diversity declining as MAP increases or decreases from this value (Fig.2a). Below the threshold (in drier
conditions), MAP explained 49% of the observed deviance in a generalized least squares framework (GLS) that
accounts for spatial autocorrelation (Fig.2a). Above the threshold, MAP explained 11% of the deviance (Fig.2a).
Assessing the distribution of communities that are not covered by the existing network of protected areas
in South America, we nd that the top 5% communities (80 unprotected sites) with highest lineage diversity
are largely found across the intermediate MAP region (Fig.3, Appendix2). In addition, these sites are found in
municipalities that have lost 66,685 Km2 of their natural cover over the last 30 years (more than twice the size of
Belgium; Appendix2).
Figure 2. Relationship between mean annual precipitation (MAP) and lineage diversity(standardised eect
size of phylogenetic diversity, a measure of the evolutionary diversity of communities) across 2,025 lowland tree
communities of tropical South America. (a) Eect of MAP on lineage diversity (LD). Break point (1,490 mm)
was determined by piecewise regression. r2 = coecient of determination from generalized least squares (GLS)
models that account for spatial autocorrelation. GLS was calculated for before (y = 0.002326x − 2.634307) and
aer (y = −0.0006x + 0.711) the break point. (b) Geographical variation of lineage diversity and MAP. Colours
of the symbols illustrate lineage diversity and are identical to colours in (a) (warmer colours indicate higher
values). Circles indicate communities below and triangles above the precipitation break point (1,490 mm).
Grey areas around the curves in (a) are 99% condence intervals. ese represent, for a given value of MAP, the
interval estimate for the mean of LD, thus reecting the uncertainty around this mean. Dashed lines represent
national borders and contours represent mean annual precipitation in (b).
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When considering alternative measures of climatic water availability, such as climatic water decit, precipitation sea-
sonality and water decit duration, we also found a peak in lineage diversity at intermediate values (Fig.S3). In contrast,
we found no relationship between temperature-related variables and lineage diversity (Fig.S4). ese results are robust
to (i) including unsampled genera in the phylogeny30 (Fig.S5), (ii) controlling for potential richness-dependence of our
lineage diversity metric31 (Fig.S6), (iii) dierent temporal calibration methods (Fig.S7), and are consistent (iv) across
a set of phylogenies from the posterior distribution (Fig.S8) and (v) when using a species-level phylogeny (Fig.S9).
Discussion
e mismatch that we uncovered between higher species richness in wetter environments4–7 and higher lineage
diversity in areas under intermediate MAP (Fig.2a,b) indicates that the distribution of evolutionary diversity
in neotropical tree communities might not be as simplistic as previously thought, based on studies with lim-
ited coverage of environmental gradients19,20,32. Our results support the ECH by showing that communities at
the threshold between wet and dry environments (1,200 mm ≤ MAP < 1,800 mm; Fig.2b) contain both wet and
dry-adapted lineages and therefore high evolutionary diversity. e dramatically reduced lineage diversity across
communities at the dry extreme (MAP < 1,200 mm; i.e., semi-arid woodlands; blue circles in Fig.2b) may reect
the limited ability of wet-adapted lineages to survive in dry climates, with lineages there representing a phyloge-
netically nested subset of the continental pool that can tolerate low MAP.
Towards the wet extreme (MAP ≥ 1,800 mm), the unexpectedly reduced lineage diversity suggests that interme-
diate MAP may also be a threshold for the dry-adapted subset of lineages. ese results are in agreement with phy-
logenetic studies showing that plant lineages in seasonally dry environments (e.g., caatinga woodlands; blue circles in
northeastern Brazil in Fig.2b) are oen conned to these environments over evolutionary timescales15. Such evidence
for phylogenetic conservatism in dry environments, combined with our results showing highest lineage diversity in
intermediate MAP, bring support to the ECH, whereby highest evolutionary diversity along any environmental gra-
dient, if sampled extensively as in this study, will be found in intermediate conditions because communities located
at one environmental extreme (e.g. hyper-wet) are likely to be missing lineages adapted and conned to the other
extreme (e.g., highly seasonally dry; Fig.1). Meanwhile, the high species richness in wet areas, despite having lower
lineage diversity, may be due to recent species diversication in wet areas. e wet tropics of South America have been
a cradle ofrecent lineage diversication, at least for some clades33–35 (although see Fine et al.36 for a counterexample).
Nonetheless, well-resolved species-level phylogenies are needed to assess the ubiquity of high recent diversication
rates in the wet tropics and the role that variable diversication rates may play in the observed patterns.
Our results are of relevance for conservation strategies in South America that take into account evolutionary
diversity37. One approach to conserving maximum tropical plant lineage diversity would be to protect dierent
communities at either end of the precipitation gradient, and our study therefore highlights the unique and oen
over-looked lineages found in dry communities (Fig.1 and Appendix2) that are currently under-protected38.
Our results also highlight an additional approach, which would be to protect the evolutionarily diverse commu-
nities found at intermediate precipitation. e intermediate MAP region includes ecosystems within the ‘arc of
deforestation’ where habitat alteration has been rapid and pervasive39, and where climate change eects may be
severe40. Nonetheless, these evolutionarily diverse communities are largely unprotected by the existing network
of protected areas in South America (Fig.3; see Appendix2 for detailed information on these communities).
Per unit area, protection of tree communities in the arc of deforestationand in Central Brazil may conserve
the widest range of evolutionary lineages of South American trees. Because the amount of evolutionary diver-
sityin communities is associated with resilience to climate change41, ensuring that these communities are con-
served, in conjunction with wetter and drier habitats, is important to ensure that the full evolutionary diversity of
neotropical forests is preserved in the face of land-use and climate change.
Figure 3. Conservation assessment of lineage diversity across lowland tree communities in tropical South
America. Distribution of the top 5% unprotected tree communities with highest lineage diversity (80 sites; red
circles). Unprotected status was determined by overlaying the distribution of our sites on to the coverage of
protected areas across South America.
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Methods
Datasets. We extracted climatic data and inventories of 2,025 tree communities from NeoTropTree (NTT;
http://neotroptree.info; Appendix2). Taxonomic nomenclature was made consistent by querying species names
against Tropicos (http://tropicos.org) and Flora do Brasil (http://oradobrasil.jbrj.gov.br). e NTT database
includes environmental variables for all its sites, derived from multiple sources (see Supplementary Methods for
details). We constructed a molecular phylogeny for 1,100 lowland tropical tree genera from South America by
sequencing the rbcL and matK plastid regions from plants collected during eldwork or from GenBank (http://
www.ncbi.nlm.nih.gov/) (Appendix 3). We aligned the genetic data using MAFFT (http://align.bmr.kyushu-u.
ac.jp/ma), and performed Bayesian phylogenetic inference using BEAST v.1.8.2in the CIPRES Science Gateway
(https://www.phylo.org; see Supplementary Methods for further details). Branch lengths were time-scaled using
a relaxed molecular clock with fossil-based age constraints implemented on 86 nodes (Appendix1). In order to
assess the robustness of results to temporal calibration approach (Fig.S7), we also generated a maximum like-
lihood phylogeny using RAxML v842, and time-scaled it using penalized likelihood and the same fossil calibra-
tions43, via the TreePL soware44 (available at https://github.com/blackrim/treePL). ese phylogenies were then
pruned to the 852 genera in the community matrix for downstream analyses.
Data analyses. We determined the precipitation niche of each genus by calculating the mean MAP for sites
at which it occurred. We then color-coded these values at terminal branches in order to visualise their phyloge-
netic distribution. We estimated phylogenetic signal for mean MAP by using Pagel’s lambda45, which varies from
0 to 1. A value of 1 indicates a strong relationship between phylogenetic position of genera and their mean MAP,
while a value of 0 indicates that there is no relationship between mean MAP and the phylogeny. We assessed the
signicance of lambda using a likelihood ratio test. We conducted the trait mapping and phylogenetic signal
analyses using the phyloch46 and phytools47 packages in the R Statistical Environment48.
We calculated lineage diversity as the total phylogenetic branch length (PD) in communities21 standardized
for genus-level richness (i.e., standardized eect size of PD; sesPD49), a metric we refer to as lineage diversity.
is metric measures how PD deviates from a null expectation, generated by randomly shuing the tips of
the phylogeny and recalculating PD in communities49. We tested whether the lineage diversity (LD) results are
robust to including missing taxa by randomly inserting into the phylogeny the 68 genera that are present in the
genus-by-site matrix but lacking appropriate molecular data. is consisted of determining the most derived
consensus clade for each missing taxon (MDCC; i.e., family, subfamily, tribe or subtribe30,50,51), and then insert-
ing them in random positions within their MDCCs. We repeated this procedure 100 times for each of 100 trees
sampled from across the posterior distribution (see Fig.S5 and ‘Phylogenetic tree’ in Supplementary Methods).
We tested whether the decreasing LD in wet communities (mean annual precipitation ≥1,800 mm) is a
richness-dependent artefact31 by calculating LD using a set of 100 genus-by-site matrices randomly rarefacted to
86 genera (1/4 of maximum generic richness31 in wet communities) and phylogenetic trees pruned to the genus
pool in each matrix. Because communities found in drier conditions (mean annual precipitation <1,800 mm)
show a pattern of decreasing lineage diversity towards drier, species-poor environments and richness-dependent
artefacts would operate in the opposite direction31, we tested for a potential richness-dependence using wet com-
munities only. ese analyses generated 100 LD values for each of the 519 wet communities, which were used to
calculate mean values per community (Fig.S6).
We tested whether our results are robust to phylogenetic uncertainty by calculating LD across a set of 100 phylog-
enies from the posterior distribution (see Fig.S8 and ‘Phylogenetic Tree’ in Supplementary Methods). Finally, we cal-
culated LD using a simulated species-level phylogeny (see Fig.S9 and ‘Phylogenetic tree’ in Supplementary Methods).
We assessed the goodness-of-fit between lineage diversity and climatic variables (see ‘Database’ in
Supplementary Methods) through adjusted coecients of determination, AIC values and signicance tests for
linear, quadratic and piecewise regressions52 (TableS1). We assessed variation in the adjusted coecients of deter-
mination for these regressions using the full genus-by-site matrix (920 genera) and a set of 10,000 phylogenetic
trees that include the 68 missing genera (see imputation methods above and Fig.S2).
Because spatial autocorrelation can inate type I error in traditional statistical tests and aect parameter estimates,
we accounted for it by performing generalized least squares analyses with four dierent spatial structures: exponential,
Gaussian, linear and spherical. Model selection was based on the minimization of AIC values; i.e., ∆AIC relative to the
null model without spatial autocorrelation. An exponential spatial structure accounted best for spatial autocorrelation
relative to other spatial structures in both models; i.e., for before (∆AIC = −456.4) and aer (∆AIC = −208.9) the
break-point in lineage diversity (Fig.2a). We conducted the spatial analyses using the nlme package53 in R48.
Conservation assessment. We assessed the protection status (protected or unprotected) of our 2,025
tree communities by overlaying their distribution on to the coverage of protected areas across South America
(Appendix2). We used conservation units from the World Database of Protected Areas (IUCN & UNEP -
WCMC, www.protectedplanet.net; downloaded on July 2019). We also computed the loss of natural cover over
the last 30 years for the municipalities where our tree communities are found (c.90% of our sites; Appendix2)
using information from the MapBiomas Project (http://mapbiomas.org).
Data availability
Time-calibrated molecular phylogenies are deposited at the Dryad Digital Repository (https://doi.org/10.5061/
dryad.gf1vhhmk0).A full description with details of data accessibility for Neo-TropTree can be found athttp://
www.neotroptree.info/.
Received: 13 July 2019; Accepted: 13 November 2019;
Published: xx xx xxxx
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Acknowledgements
We thank Alexandra Clark and Michelle Hart (Royal Botanic Garden Edinburgh) for their help with sequencing
of the matK/rbcL loci. We thank the following people for their help with collection and preparation of plant
specimens: Adilson Pintor, Pablo Prieto (field expeditionin Rio de Janeiro state); Aécio Santos (Goiásand
Tocantinsstates); Camilo Barbosa, Catarina Carvalho, Lisandra Teixeira, Nara Mota, Pedro Viana (Pará); Caio
Vivas, José Lima (Bahia); Eric Hattori, Fernanda Freitas, Flávia Pezzini, Pedro Taucce (Minas Gerais); Marcella
Baroni (Mato Grosso do Sul); Flávia Costa (Manaus). Funding:National Environmental Research Council/
UK (NE/I028122/1) to D.M.N., K.G.D., T.R.B and R.T.B.; Conselho Nacional de Desenvolvimento Cientíco
e Tecnológico/Brazilto L.P.Q. (SISBIOTA 563084/2010-3) and M.T.N. (Scholarships 236805/2012-6 PDE
CsF and305617/2018-4); National Science Foundation/USA (DEB-1556651) to DMN; Mohamed bin Zayed
Species Conservation Fund (Grant 12053537) to DMN; Leverhulme Trust International Academic Fellowship
to K.G.D.;Coordenação de Aperfeiçoamento de Pessoal de Nível Superior/Brazil (Program “Visiting Senior
Professor in the Amazon”) to R.P.S. We also thank two anonymous reviewers for their insightful comments.
Author contributions
D.M.N. wrote the original manuscript with substantial input from K.G.D., R.T.P. and T.R.B.; D.M.N. carried
out analyses with substantial input from K.G.D.; F.C.S., K.G.D., D.M.N. and R.A.S. generated the phylogenetic
trees; A.O.F. assembled the tree community dataset; D.M.N. led eldwork planning, collection, identication,
preparation and curation of plant specimens, with help from K.G.D., R.T.P., T.R.B, L.P.Q., H.C.L., M.F.S., G.P.L.,
L.A., C.R., J.L.M.-P., I.H.-C., D.V., G.A.P., A.D., R.L.-P., L.V.F., R.P.S., G.S.S., M.T.N. and C.N.F. All authors
commented on the manuscript and approved the last version.
Competing interests
e authors declare no competing interests.
Additional information
Supplementary information is available for this paper at https://doi.org/10.1038/s41598-019-55621-w.
Correspondence and requests for materials should be addressed to D.M.N.
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