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Freezing and water availability structure the evolutionary diversity of trees across the Americas

Authors:
  • Instituto de Ecologia y Biodiversidad, Chile

Abstract

The historical course of evolutionary diversification shapes the current distribution of biodiversity, but the main forces constraining diversification are still a subject of debate. We unveil the evolutionary structure of tree species assemblages across the Americas to assess whether an inability to move or an inability to evolve is the predominant constraint in plant diversification and biogeography. We find a fundamental divide in tree lineage composition between tropical and extratropical environments, defined by the absence versus presence of freezing temperatures. Within the Neotropics, we uncover a further evolutionary split between moist and dry forests. Our results demonstrate that American tree lineages tend to retain their ancestral environmental relationships and that phylogenetic niche conservatism is the primary force structuring the distribution of tree biodiversity. Our study establishes the pervasive importance of niche conservatism to community assembly even at intercontinental scales.
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EVOLUTIONARY BIOLOGY
Freezing and water availability structure the
evolutionary diversity of trees across the Americas
Ricardo A. Segovia1,2*, R. Toby Pennington3,4, Tim R. Baker5, Fernanda Coelho de Souza5,6,
Danilo M. Neves7, Charles C. Davis8, Juan J. Armesto2,9,10, Ary T. Olivera-Filho7, Kyle G. Dexter1,3
The historical course of evolutionary diversification shapes the current distribution of biodiversity, but the main
forces constraining diversification are still a subject of debate. We unveil the evolutionary structure of tree species
assemblages across the Americas to assess whether an inability to move or an inability to evolve is the predominant
constraint in plant diversification and biogeography. We find a fundamental divide in tree lineage composition
between tropical and extratropical environments, defined by the absence versus presence of freezing temperatures.
Within the Neotropics, we uncover a further evolutionary split between moist and dry forests. Our results demon-
strate that American tree lineages tend to retain their ancestral environmental relationships and that phylogenetic
niche conservatism is the primary force structuring the distribution of tree biodiversity. Our study establishes the
pervasive importance of niche conservatism to community assembly even at intercontinental scales.
INTRODUCTION
A central challenge in biogeography and macroevolution is to un-
derstand the primary forces that drove the diversification of life and
the assemblage of ecological communities. Was diversification con-
fined within continents and characterized by adaptation of lineages to
different major environments (i.e., biome switching), or did lineages
tend to disperse across great distances but retain their ancestral envi-
ronmental niche (i.e., phylogenetic niche conservatism)? Classically,
the attempts to define biogeographic regions based on shared plant
and animal distributions lend support to the first hypothesis, that large-
scale patterns may be explained by regionally confined evolutionary
diversification, rather than long-distance dispersal (13). However,
recent studies of the distribution of plant lineages at global scales have
documented high levels of intercontinental dispersal [e.g., (48)] and
revealed that lineages tend to retain their ancestral biomes when
dispersing (9,10). These recent findings suggest that environmental
associations of lineages may be the primary force organizing the course
of diversification, but a key knowledge gap is in studies comparing
the degree of evolutionary similarity among species assemblages at
large geographic scales. Taking advantage of recent advances in the
availability of broadscale biodiversity and genomic data and appro-
priate analytical methods (11), we unveil the evolutionary structure
of tree assemblage diversity at an intercontinental scale.
With high mountain chains running north to south across latitudes
and a mosaic of contrasting environments, the Americas represent
a natural laboratory to investigate the evolutionary forces behind
community assembly and the modern distribution of biodiversity.
Here, we examine the phylogenetic composition of angiosperm tree
assemblages across the Americas as a means to determine whether
dispersal limitation or phylogenetic niche conservatism had a greater
impact on the present-day evolutionary composition of tree assem-
blages. If lineages tend to retain their environmental niche as they
diversify across space, then we would expect major evolutionary groups
to be restricted to specific environmental regimes. This leads to the
prediction that lineage composition of assemblages from extratropical
regions in both hemispheres should be more similar to each other
than to assemblages that occur in intervening tropical regions. In ad-
dition, we would predict that assemblages from dry tropical environ-
ments should show greater similarity in tree lineage composition to
each other than to assemblages from moist environments with which
they may be spatially contiguous (12). Alternatively, if diversification
is spatially restricted and biome switching is common, then the major
evolutionary grouping of assemblages should be segregated geo-
graphically. Thus, we would predict assemblages from South America
(which was physically isolated through the Cenozoic) to constitute one
group and assemblages from North and Central America to constitute
another.
To test the relative importance of phylogenetic niche conservatism
versus dispersal limitation, we analyzed data from ~10,000 tree
assemblages with a new, temporally calibrated genus-level phylogeny
that includes 1358 genera (~90% of tree genera sampled per assem-
blage). We assessed similarity in lineage composition among assem-
blages using clustering analyses and ordinations based on shared
phylogenetic branch length. Next, we identified the indicator lineages
for each major group in the clustering analysis and explored the geo-
graphic and environmental correlates of the distribution of the main
evolutionary clusters. We further assessed the degree to which climatic
variables versus geographic position could classify sites into different
evolutionary groups. If climatic variables provide a better means of
distinguishing groups than geographic variables, then this would sup-
port the idea that phylogenetic conservatism is more important than
dispersal limitation in determining the distribution of evolutionary
lineages, while the converse would hold if geographic variables per-
form better. Last, we estimated the unique evolutionary diversity (i.e.,
sum of phylogenetic branches of lineages restricted to individual groups)
versus shared evolutionary diversity (i.e., sum of shared phylogenetic
branches) across evolutionary groups (for details, see Materials and
Methods section).
1School of GeoSciences, University of Edinburgh, Edinburgh, UK. 2Instituto de
Ecología y Biodiversidad, Santiago, Chile. 3Tropical Diversity Section, Royal Botanic
Garden Edinburgh, Edinburgh, UK. 4Department of Geography, University of Exeter,
Exeter, UK. 5School of Geography, University of Leeds, Leeds, UK. 6Departamento
de Engenharia Florestal, Universidade de Brasília (UNB), Campus Universitário Darcy
Ribeiro, Asa Norte, Brasília 70910-900, Brazil. 7Department of Botany, Federal
University of Minas Gerais, Belo Horizonte, Brazil. 8Department of Organismic and
Evolutionary Biology, Harvard University, Cambridge, MA, USA. 9Departamento de
Ecología, Universidad Católica de Chile, Santiago, Chile. 10Facultad de Ciencias Naturales y
Oceanográficas, Universidad de Concepción, Concepción, Chile.
*Corresponding author. Email: segoviacortes@gmail.com
Copyright © 2020
The Authors, some
rights reserved;
exclusive licensee
American Association
for the Advancement
of Science. No claim to
original U.S. Government
Works. Distributed
under a Creative
Commons Attribution
License 4.0 (CC BY).
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RESULTS
We show that the evolutionary lineage composition of American
tree assemblages is structured primarily by phylogenetic niche conser-
vatism. The two principal groups (K=2) have a tropics-extratropics
structure (Fig.1). The extratropical group is not geographically re-
stricted, but includes temperate tree assemblages from North America
and southern South America, connected by a high-elevation corridor
in low latitudes (Fig.1,AandB). The tropics-extratropics structure
of tree evolutionary diversity shows a strong correspondence (97%
match, fig. S1) with the absence versus occurrence of freezing tem-
peratures within a typical year (see Fig.1,CandD). We observe that
most evolutionary diversity, measured as summed phylogenetic branch
length, occurs within the tropics, but that there is unique evolutionary
diversity restricted to the extratropics (~10% of the total; Fig.2B
and fig. S3A). Ordination and indicator clade analyses revealed that
the tropics-extratropics segregation is associated with the distribution
of specific clades, such as the Fagales, which includes the oaks (Quercus),
beeches (Fagus), coihues (Nothofagus), and their relatives (Fig.3 and
tables S1 and S2).
On the basis of two different analyses (Elbow and Silhouette
methods; see Materials and Methods for discussion of selecting op-
timal K), clusters of K=3 and K=4 groups are also supported as
additional informative splits (fig. S2), and each of their major groups
capture substantial unique evolutionary diversity (Fig.2B, fig. S3,
and table S2). In K=3, the main extratropical cluster grouped as-
semblages from North America and extreme southern South America,
while the remaining assemblages from temperate southern South
America and the Andean tropics grouped with assemblages from the
arid or semiarid tropics and subtropics (fig. S4). The third group was
formed by the moist tropics (fig. S4). For K=4, the extratropics were
split into a largely temperate North American group and a second
group that joins subtropical sites in South and Central America with
southern temperate forests and high elevation sites in the Andes (Fig.
2A). In the tropics, there is one group uniting assemblages found in
ever-moist and warm conditions, and a second group of assemblages
that extend into drier and subtropical areas (Fig.2C and fig. S5A),
including most tropical dry forest assemblages (Fig.2A and Table S3).
We refer to the four groups of assemblages in K=4 as the northern
extratropical, southern extratropical, tropical moist, and tropical dry
groups.
Focusing on the K= 4 analyses, we found that climatic variables
perform markedly better than geographic variables in classifying in-
dividual assemblages into evolutionary groups, supporting the preem-
inence of phylogenetic niche conservatism as opposed to dispersal
limitation in structuring the distribution of biodiversity in tree as-
semblages. A simple climatic model with mean annual precipitation
(MAP), mean annual temperature (MAT), maximum climatological
water deficit (CWD), and temperature seasonality (TS) succeeded in
classifying 86.4% of assemblages, on average, into the correct evolu-
tionary group. A simple geographic model, that South American as-
semblages should fall into a separate group from North and Central
American assemblages, and with latitude and longitude as input
−120 −100 −80 −60 −40
−40−20 02040
Tropical assemblages
Extratropical assemblages
K= 2
A
−40 −20 02
04
0
0
1000 2000 3000 4000
Latitude
Elevation (masl)
B
−0.6 −0.4 −0.2 0.0 0.2
−0.4 −0.2 0.0 0.2 0.4
Evolutionary ordination axis 1
Evolutionary ordination axis 2
C
−0.6 −0.4 −0.2 0.0 0.2
−0.4 −0.2 0.0 0.2 0.4
Evolutionary ordination axis 1
Evolutionary ordination axis 2
Freezing
Nonfreezing
D
Fig. 1. The geographic, evolutionary, and environmental relationships of the two principal evolutionary groups (from K = 2 clustering analysis). (A) Geographic
distribution of angiosperm tree assemblages and their affiliation with either the tropical (n = 7145) or extratropical (n = 2792) evolutionary group. (B) Distribution of as-
semblages over elevation and latitude, showing that the extratropical group is largely restricted to high elevations at low latitudes. (C and D) Distribution of assemblages
over the first two axes of an ordination based on evolutionary composition with assemblages in (C) colored according to group affiliation and in (D) as to whether or not
they experience freezing temperatures in a regular year [from (50)]. masl, meters above sea level.
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−120 −100 −80 −60 −40
−40 −20 02040
Tropical moist
Tropical dry
Southern extratropical
Northern extratropical
K= 4
A
−20 −10 01
02
0
−2000 −1000 0
Minimum temperature of coldest month (°C)
Maximum climatological
water deficit (CWD)
C
B
Northern
extratropical
Southern
extratropical
Tropical dry
Tropical moist
12,586 Ma
4914 Ma
3992 Ma
5835 Ma
5715 Ma
1284 Ma
11,954 Ma
1942 Ma
Fig. 2. The geographic, evolutionary, and environmental relationships among four evolutionary groups (from K = 4 clustering analysis). (A) Geographic distribu-
tion of angiosperm tree assemblages and their affiliation with one of the four evolutionary groups. (B) Euler diagram representing the amount of evolutionary history,
quantified as phylogenetic diversity (PD) (in millions of years), restricted to each cluster versus that shared between clusters. (C) Distribution of assemblages over ex-
tremes of temperature (minimum temperature of coldest month) and water availability [maximum climatological water deficit (CWD)]. Lines represent the 95th quantile
of the density of points for each group.
Evolutionary ordination axis 1 (9.6%)
Evolutionary ordination axis 2 (6.7%)
Moist lowland tropics (evergreen
and semideciduous forest)
Tropical savanna
Tropical dry forests
Northern temperate
Tropical high elevation (>2000 masl)
Chaco
Southern South America
−0.4 −0.2 0.0 0.2 0.4
−0.50.0
Fig. 3. Phylogenetic ordination of tree assemblages based on their evolutionary lineage composition. Colors in the main plot represent the groups from K = 4
clustering analyses and the different symbols represent major vegetation formations. The subset plot shows the clades most strongly associated with the first two axes
of the evolutionary ordination.
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variables, classified 76.0% of assemblages correctly on average. Add-
ing latitude and longitude may even overemphasize the importance
of geography given that latitude and longitude are correlated with cli-
matic variation. In the climatic classification for K= 4 groups, tem-
perature variables surpass precipitation variables as the most im-
portant classificatory variables [mean decrease in Gini index when
excluded (13); for TS, 2728; MAT, 1565; MAP, 1064; and CWD, 936].
When focusing only on the tropics, these climatic variables correctly
classify sites 83.6% of the time, with the most important variable being
CWD (mean decrease in a Gini index of 792), followed by MAT
(722), TS (643), and MAP (642). When focusing only on the extra-
tropics, these climatic variables correctly classify sites 98.4% of the
time. TS was by far the most important variable (mean decrease in a
Gini index of 719), which is in line with previous research showing
that Southern Hemisphere temperate areas are less seasonal than
Northern Hemisphere temperate areas (14,15). TS was followed in
importance by CWD (157), MAP (92), and MAT (75). Analyses
with generalized linear models suggest that MAP is the most im-
portant climatic variable to distinguish assemblages in the tropical
moist from tropical dry groups and that TS is the most important to
distinguish the two extratropical groups (fig. S6).
DISCUSSION
Our results demonstrate that the tropics-extratropics evolutionary
structure of tree diversity is principally associated with the environmen-
tal threshold of the presence versus absence of freezing temperatures
(Fig.1,AandB, and fig. S1). This pattern is consistent with evidence
documenting that only angiosperm lineages that were able to evolve
traits to avoid freezing-induced embolism radiated into high latitudes
(16). In addition, we determined that a unique, sizeable portion of
the total evolutionary diversity of angiosperm trees is restricted to
extratropical assemblages, as the fossil record corroborates (17,18).
Collectively, this evidence suggests that the phylogenetic conserva-
tism of lineages from the extratropics has a major relevance for the
diversification of angiosperm trees in the Americas. Kerkhoff etal.
(19) estimated that in the extratropical region (defined by them as
areas north of 23°N and south of 23°S), angiosperm lineages produced
extratropical descendants at least 90% of the time. Considering that
some areas subjected to regular freezing at high elevations in equatorial
latitudes may be better classified as extratropical, as demonstrated
here by our results (Fig.1), extratropical phylogenetic conservatism
could even be greater than found by Kerkhoff etal. (19).
We suggest that extratropical conservatism has a major impor-
tance in the biogeography of the Americas. The relatively recent
uplift of the Andes would have created novel environments, with reg-
ular freezing temperatures, at low latitudes. Freezing temperatures
would have filtered dispersal into this new habitat, allowing extra-
tropical lineages to move from both north and south to equatorial
latitudes (20,21), but constraining the immigration of lineages from
lowland, frost-free environments. Fossil pollen demonstrates the ar-
rival in the northern Andes of tree genera from temperate forests in
the Northern Hemisphere, including Juglans (Juglandaceae), Alnus
(Betulaceae), and Quercus (Fagaceae), at about 2.2million years (Ma),
1.0 Ma, and 300,000 years, respectively, and the arrival of southern
genera, including Weinmannia (Cunoniaceae) and Drymis (Wintera-
ceae), during the late Pliocene and Pleistocene (1.5–3.2 Ma) (20,22).
Likewise, phylogenetic evidence shows recent diversification in the
Andes of lineages that seem to have originated in the extratropics,
including Lupinus (Fabaceae) (23), Adoxaceae/Valerianceae (24,25),
and Gunnera (Gunneraceae) (26).
Our results also point to a moist versus dry evolutionary divide
within the Neotropics. Tropical moist group assemblages hold the
greatest amount of evolutionary diversity, both overall and unique
to them, despite occupying the most restricted extent of climatic space
of any of the K=4 groups (Fig.2,BandC). Tropical dry group
assemblages, in contrast, extend across a broader climatic space, but
hold less evolutionary diversity overall (Fig.2,BandC). This asym-
metry in the accumulation of diversity may reflect phylogenetic con-
servatism for a putatively moist and hot ancestral angiosperm niche
(27), or could result from a favorable environment in tropical moist
regions that can be occupied by any angiosperm lineage, even those
that also occur in cooler or drier conditions (28,29). Regardless, the
similarity in the lineage composition of the extensive but discontin-
uously distributed tropical dry forests (12) indicates their separate
evolutionary history. Tropical dry forests have been described as dis-
persal limited (e.g., 12), but this refers to the ability of constituent
taxa to persist locally over evolutionary time scales, thereby inhibiting
immigration. However, even a low rate of dispersal and immigration
among American tropical dry forest regions suffices to maintain flo-
ristic cohesion. Such evolutionary isolation of the dry forest flora has
previously been suggested by studies in Leguminosae (12,30), and is
shown here to be evident at the evolutionary scale of all angiosperm
tree species.
Our results also help to clarify the contentious evolutionary sta-
tus of savanna and Chaco regions in the Neotropics. We find that
the southern savannas (the Cerrado region of Brazil) are more evolu-
tionary related to tropical moist forests than dry forests (Fig.2A, and
fig. S4), as previously suggested for specific clades (30,31). However,
northern tropical savannas (i.e., Llanos of Venezuela and Colombia
and those in Central America) are split in their evolutionary linkages
between the tropical moist and tropical dry groups (Fig.3 and table
S3). This may reflect the distinct ecology of many northern savannas
[e.g., the Llanos are hydrological savannas (32)] and suggest a diver-
gent evolutionary history for northern and southern savannas. Our
results may also help to resolve the debates around the evolutionary
affinities of the Chaco [e.g., (33,34)], by showing that this geograph-
ically defined region houses a mix of extratropical and tropical
lineages (Fig.2).
More broadly, our analyses consistently point to evolutionary links
between assemblages in seasonally dry and seasonally cold areas
(Fig. 2 and fig. S4). For example, when we consider K=3 evolutionary
groups, a single “dry and cool” group coalesces, including southern
South American extratropics, seasonally tropical dry forests, and
Mexican pine-oak forests, with the other two groups being the trop-
ical moist forest group and a largely northern, extratropical group
(fig. S4). Along the same lines, the southern extratropical group from
the K=4 clustering also includes subtropical forests in arid and semi-
arid regions of Chile, Mexico, and elsewhere (Fig.2), while the tropical
dry group includes tree assemblages occurring in cool areas at high
elevation, largely in the southern Atlantic Forest of Brazil (Fig.2).
When we consider K=5 evolutionary groups, these cool sites, which
are also moister than the rest of the tropical dry group, split off to
form a fifth group that also takes in sites at higher elevation in the
Andes, the Guianan Highlands, Central America, and the Caribbean
(fig. S5).
We show that the evolutionary composition of tree assemblages
in the Americas is determined primarily by the presence versus
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absence of freezing temperatures, dividing tropical from extratropical
regions. Within the tropics, we find further evolutionary subdivision
among assemblages experiencing moist versus seasonally dry con-
ditions. These findings demonstrate that phylogenetic niche conserva-
tism is the primary force organizing the diversification, community
assembly, and, therefore, the biogeography of angiosperm trees. Tree
species that can inhabit areas experiencing freezing temperatures
and/or environments subjected to seasonal water stress belong to a
restricted set of phylogenetic lineages, which gives a unique evolu-
tionary identity to extratropical forests and tropical dry forests in the
Americas. While our study is restricted to New World trees, we suggest
that plant biodiversity globally may be evolutionarily structured fol-
lowing a tropics-extratropics pattern, while diversity within the tropics
may be structured primarily around a moist-dry pattern. These find-
ings advocate strongly for integrating the concepts of extratropical con-
servatism and tropical-dry conservatism into our understanding of
global macroevolutionary trends and biogeographic patterns.
MATERIALS AND METHODS
Tree assemblage dataset
Our tree assemblage dataset was derived by combining the NeoTropTree
(NTT) database (35) with selected plots from the Forest Inventory
and Analysis (FIA) Program of the U.S. Forest Service (36), accessed
on 17 July 2018 via the BIEN package (37). Sites in the NTT database
are defined by a single vegetation type within a circular area of 5-km
radius and contain records of tree and tree-like species, i.e., free-
standing plants with stems that can reach over 3m in height [see
www.neotroptree.info and (38) for details]. Each FIA plot samples
trees that are ≥12.7-cm diameter at breast height in four subplots
(each being 168.3m2) that are 36.6m apart. We aggregated plots from
the FIA dataset within 10-km-diameter areas, to parallel the spatial
structure of the NTT database. We excluded any sites that had less
than five angiosperm genera, as preliminary analyses suggested that
these sites lacked sufficient information to be confidently placed in
evolutionary ordinations and clustering described below. Therefore,
the FIA dataset was reduced considerably, and some regions with a
low diversity of angiosperms have no samples in our study. This pro-
cedure produced a total dataset of 9937 tree assemblages distributed
across major environmental and geographic gradients in the Americas.
Genus-level phylogenetic tree
We obtained sequences of the rbcL and matK plastid gene for 1358
angiosperm tree genera, from GenBank (www.ncbi.nlm.nih.gov/
genbank/), building on previous large-scale phylogenetic efforts for
angiosperm trees in the Neotropics (39,40). Sequences were aligned
using the MAFFT software (41). “Ragged ends” of sequences that
were missing data for most genera were manually deleted from the
alignment.
We estimated a maximum likelihood phylogeny for the genera
in the RAxML v8.0.0 software (42) on the CIPRES web server (www.
phylo.org). We constrained order-level relationships in the tree, fol-
lowing the phylogeny in Gastauer etal. (43), which is based on the
topology proposed by the Angiosperm Phylogeny Group IV. We
concatenated the two chloroplast markers following a general time
reversible+gamma model of sequence evolution. We included se-
quences of Nymphaea alba (Nymphaeaceae) as an outgroup. We used
a maximum likelihood bootstrap analysis to assess support for rela-
tionships in the phylogeny. Most deeper relationships in the phylogeny
had high support values (>70 bootstrap support), which is expected
given that ordinal relationships were fixed. More recent nodes in the
phylogeny had lower support with the relationships of genera within
families having mean bootstrap support values of ~60. However, we
confirmed that relationships of families within orders and genera within
families generally matched those in more detailed phylogenetic analyses
(with more variable genetic markers), specifically those studies listed
in table S4. The low support values are likely attributable to the rela-
tively low variability of the matK and rbcL markers within angiosperm
families.
We temporally calibrated the maximum likelihood phylogeny
using the software treePL (44). We implemented age constraints for
320 internal nodes [family level or higher, from (45)] and for 123 gen-
era stem nodes (based on ages from a literature survey; table S4). The
rate smoothing parameter (lambda) was set to 10 based on a cross-
validation procedure. The final dated phylogeny can be found in the
Supplementary Materials.
Phylogenetic distance analysis and clustering
We used the one complement of the Phylosor index (i.e., 1 − Phylo-
Sorensen) to build a matrix of phylogenetic dissimilarities between
plots based on genera presence-absence data. The Phylosor index
sums the total branch length of shared clades between sites (46) rel-
ative to the sum of branch lengths of both sites
Complement of Phylo − Sorensenij = 1 − BLij / 0.5 * (BLi + BLj)
where BLij is the sum of shared phylogenetic branch length between
sites i and j, and BLi and BLj are the sum of branch length of phylog-
enies comprising solely genera within sites i and j, respectively.
Thus, if all branches are shared between two plots, then the dissim-
ilarity measure takes on a value of 0. If no branches are shared
between plots (i.e., the plots comprise two reciprocally monophyletic
clades), then the dissimilarity measure will take on a value of 1.
This metric was estimated using the phylosor.query() function in the
PhyloMeasures (47) package for R. Analyses with the one complement
of the Unifrac phylogenetic similarity measure gave highly similar
results and are not presented here.
We used K-means clustering to explore the main groups, in terms
of (dis)similarity in the tree assemblage dataset, according to the
Phylosor dissimilarity measures. Preliminary analyses using hierarchical
clustering approaches did not produce coherent groupings. The K-
means clustering algorithm requires the number of groups/clusters
(K) to be specified in advance. To estimate the best value for K, the
optimal number of clusters to parsimoniously explain the variance
in the dataset, we used the Elbow method and an approach based on
the average Silhouette width (fig. S2). The Elbow method assesses
how the total within-cluster sum of squares (TSS) changes as a function
of the number of clusters. Each additional cluster lowers the TSS,
and the elbow of the curve is formed when adding another cluster
fails to lower the TSS substantially compared to previous increases
in cluster number. On the other hand, the Silhouette width analysis
determines how well each assemblage fits within its assigned evolu-
tionary group/cluster, with higher values indicating that the site is
closer compositionally to the “median” composition (i.e., centroid)
of its assigned group relative to its proximity to the “median” com-
position of the other groups. The higher the average silhouette width
across all assemblages, the better the clustering. The Elbow analyses
suggest anything from K=3 to K=5 to be the best clustering, and
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the Silhouette width analysis point to K=2 to be the best clustering.
On the basis of these results, we selected K=2 (Fig.1), K= 3 (fig.
S4), K=4 (Fig.2), and K=5 (fig. S5) for further analysis and inter-
pretation. No geographic or environmental data were used to in-
form the clustering analyses (48). The K-means clustering was carried
out with the kmeans() function in base R (R Core Development
Team, 2016).
In addition, we performed an evolutionary ordination of tree as-
semblages based on their phylogenetic lineage composition, following
protocols developed by Pavoine (49). We specifically used an evolu-
tionary principal components analysis, implemented with the evopca()
function in the “adiv” package (49), with a Hellinger transformation
of the genus by site matrix, as this is a powerful approach to detect
phylogenetic patterns along gradients, while also allowing positioning
of sites and clades in an ordination space (11). The first two axes ex-
plained 9.6 and 6.7% of the variation in the data, with subsequent
axes each explaining <5.5%.
Correspondence between clustering results
and environmental variables
We tested the correlation between our K= 2 clustering result and
eight different delimitations of the tropics, as per Feeley and Stroud
(50). These delimitations were as follows: (C1) all areas between 23.4°S
and 23.4°N; (C2) all areas with a net positive energy balance; (C3)
all areas where MAT does not co-vary with latitude; (C4) all areas
where temperatures do not go below freezing in a typical year; (C5) all
areas where the mean monthly temperature is never less than 18°C;
(C6) all areas where the mean annual “biotemperature”≥24°C; (C7)
all areas where the annual range of temperature is less than the average
daily temperature range; and (C8) all areas where precipitation sea-
sonality exceeds TS. We calculated the correspondence between our
binary clustering (i.e., tropical versus extratropical) and each of these
delimitations as the proportion of sites where the delimitations matched.
To assess whether the K= 4 clustering is mainly influenced by
climate or by geography, we determined the proportion of assem-
blages that can be correctly categorized into their evolutionary group
by environmental variables versus spatial variables, using a random
forest classification tree approach (13). The explanatory variables
for the environmental model were MAT, MAP, and TS from the
Worldclim dataset (51) and maximum CWD from Chave etal. (52).
For the geographic model, we used a basic division between South
America versus North and Central America together, as this reflects
the historic geographic isolation of South America. We also included
latitude and longitude as explanatory variables in this basic geographic
model. We excluded sites in the Caribbean from both models as it
was not certain how to group them in the geographic model. Even
including them would not have changed the results substantially as
they only comprise 2.4% of sites in our total assemblage database.
These analyses were implemented with the randomForest() function in
the “randomForest” package (13).
To explore the best climatic variable to explain the divisions be-
tween groups within the tropics and the extratropics, we used a mixed
model with a binomial response (tropical dry versus tropical moist
for the tropics and extratropical north versus extratropical south for
the extratropics). To account for spatial autocorrelation, we grouped
assemblages in 1° × 1° grid cells and incorporated the many-level grid
cell factor as a random effect. We implemented the mixed model with
the function glmer() from the lme4 package (53). To determine the best
climatic variable, we compared the models based on the Akaike in-
formation criterion (AIC). As candidate variables, we focused on
the same variables as in the random forest analysis, MAT, MAP, TS,
and CWD.
Shared versus unique PD
As the Phylosor estimation of evolutionary (dis)similarity cannot
distinguish variation associated to differences in total PD, or phy-
logenetic richness, versus variation associated to phylogenetic turn-
over per se, we measured the shared and unique PD associated with
each group for the K=2, K=3, and K=4 clustering analyses. First,
we estimated the association of genera with each group by an indi-
cator species analysis following de Caceres etal. (54). Specifically,
we used the multipatt() function in the R Package indicspecies (55)
to allow genera to be associated with more than one group (when
K>2). The output of the multipatt function includes the stat index,
which is a function of the specificity (the probability that a surveyed
site belongs to the target site group given the fact that the genus has
been found) and fidelity (the probability of finding the genus in sites
belonging to the given site group). We constructed pruned phylog-
enies excluding those genera with specificity greater than 0.6 for a
group, or combination of groups, to estimate the total PD found in
each group or combination of groups without their specific indicators.
Then, we subtracted these totals from the entire total for the com-
plete, unpruned phylogeny to determine the amount of phylogenetic
diversity restricted to each group or combination of groups. Last, we
estimated the PD shared across all groups as that which was not
restricted to any particular group or any combination of groups.
We fit these different PD totals as areas in a Euler diagram with the
euler() function in the “eulerr” package (56) for the K=2 and K=3
clustering and with the Venn() fuction in the “venn” package (57)
for the K=4 clustering.
Indicator lineages for clusters
To further characterize the composition of the evolutionary groups,
we conducted an indicator analysis to determine the evolutionary
clades most strongly associated with each group. We created a site ×
node matrix, which consists of a presence/absence matrix for each
internal node in the phylogeny and ran an indicator analysis for the
nodes. We selected the highest-level, independent (i.e., non-nested)
nodes with the highest stat values to present in tables S1 and S2. The
indicator node analysis was carried out with function multipatt() in
the R Package indicspecies (55).
SUPPLEMENTARY MATERIALS
Supplementary material for this article is available at http://advances.sciencemag.org/cgi/
content/full/6/19/eaaz5373/DC1
View/request a protocol for this paper from Bio-protocol.
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Acknowledgments: We thank E. Manson, D. Coenen, and C. Pertusi for help in the mining of
genetic sequences from GenBank. Funding: CONICYT PIA APOYO CCTE AFB170008 and a
Leverhulme Trust Research Fellowship RF-2015-653. R.A.S. was supported by a Newton
International Fellowship from The Royal Society and by Conicyt PFCHA/Postdoctorado Becas
Chile/2017 No. 3140189; K.G.D. and T.R.B. were both supported by Leverhulme International
Academic Fellowships. R.T.P., T.R.B., K.G.D., and D.M.N. were supported by NERC Grant NE/
I028122/1. Author contributions: R.A.S. and K.G.D. designed the study and carried out the
analyses. R.A.S., K.G.D., F.C.d.S., and D.M.N. built the phylogeny. A.T.O.-F. compiled the NTT
dataset. R.A.S., K.G.D., and R.T.P. wrote the manuscript with input from all the coauthors.
Competing interests: The authors declare that they have no competing interests. Data and
materials availability: All data needed to evaluate the conclusions in the paper are present in
the paper and/or the Supplementary Materials. Additional data related to this paper may be
requested from the authors.
Submitted 17 September 2019
Accepted 19 February 2020
Published 6 May 2020
10.1126/sciadv.aaz5373
Citation: R. A. Segovia, R. T. Pennington, T. R. Baker, F. Coelho de Souza, D. M. Neves, C. C. Davis,
J. J. Armesto, A. T. Olivera-Filho, K. G. Dexter, Freezing and water availability structure the
evolutionary diversity of trees across the Americas. Sci. Adv. 6, eaaz5373 (2020).
on May 6, 2020http://advances.sciencemag.org/Downloaded from
Americas
Freezing and water availability structure the evolutionary diversity of trees across the
J. Armesto, Ary T. Olivera-Filho and Kyle G. Dexter
Ricardo A. Segovia, R. Toby Pennington, Tim R. Baker, Fernanda Coelho de Souza, Danilo M. Neves, Charles C. Davis, Juan
DOI: 10.1126/sciadv.aaz5373
(19), eaaz5373.6Sci Adv
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... Ever since natural historians first observed that groups of organisms are geographically restricted -palms to the tropics, pines to north temperate climates, extant lemurs to Madagascar, hummingbirds to the Americas (1)understanding the factors that shape turnover of evolutionary lineages has been a central question in biogeography and macroevolution (2)(3)(4). While the importance of geography and ecology as the main axes determining the distribution of lineages, i.e. phylogenetic turnover or beta diversity, was already established >200 years ago (1), their relative contributions are still debated (4)(5)(6)(7)(8). ...
... While the importance of geography and ecology as the main axes determining the distribution of lineages, i.e. phylogenetic turnover or beta diversity, was already established >200 years ago (1), their relative contributions are still debated (4)(5)(6)(7)(8). The key processes determining turnover, phylogenetic niche conservatism (PNC) and geographic dispersal limitation (DL) (3,6), have both spatial and temporal dimensions, reflecting the spatial distribution of lineages and the evolutionary time scales over which barriers to dispersal, whether environmental (i.e., PNC) or spatial (i.e., DL), are overcome (6,9). To understand the contemporary spatial structure of diversity, turnover across space and time need to be considered together (4,6,9,10), but this is rarely achieved in empirical studies. ...
... For most terrestrial organisms, oceans and areas experiencing frost pose major barriers to dispersal and adaptation, resulting in high phylogenetic turnover amongst continents (11,12) and across the tropical-temperate divide, manifest in tropical niche conservatism (3,13). However, more general insights remain elusive. ...
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Early natural historians - Compte de Buffon, von Humboldt and De Candolle - established ecology and geography as two principal axes determining the distribution of groups of organisms, laying the foundations for biogeography over the subsequent 200 years, yet the relative importance of these two axes remains unresolved. Leveraging phylogenomic and global species distribution data for Mimosoid legumes, an iconic pantropical clade with 3,400 species, we show that the water availability gradient from deserts to rainforests dictates turnover of lineages within continents across the tropics. We demonstrate that 95% of speciation occurs within a precipitation niche, showing profound phylogenetic niche conservatism, and that lineage turnover boundaries coincide with isohyets of precipitation. We reveal similar patterns on different continents, implying that evolution and dispersal follow universal processes.
... In contrast to taxonomic diversity patterns along elevational gradients (McCain & Grytnes, 2010), comparatively less is known about phylogenetic diversity patterns, which may provide more mechanistic insights into how diversity shifts across elevations (e.g. Culmsee & Leuschner, 2013;Qian et al., 2014;Segovia et al., 2020). Indeed, phylogenetic diversity is strongly correlated with high-dimensional trait diversity (Tucker et al., 2018), suggesting that it can provide insights to the diversity of resource-use strategies within assemblages, particularly in regions of the world where trait data are not widely available (Cornwell et al., 2019). ...
... This result supports the notion of environmental filtering being the main driver of community assembly at lower elevations, where water availability is more limiting (Cavender-Bares et al., 2004;Mazel et al., 2016;Webb et al., 2002). As a result, at the landscape scale, phylogenetic clustering and therefore the TNC hypothesis is likely the predominant mechanism influencing diversity in tropical dry forests (Griffiths et al., 2020;Segovia et al., 2020). ...
... The high variation in elevation and temperature that takes place along small distances in mountainous regions (McKnight et al., 2007;Melo et al., 2009) may create barriers that expedite diversification events (Weir, 2006) and consequently increase the turnover component of phylogenetic beta diversity (Peixoto et al., 2017). This likely suggests that ecological processes such as niche convergence play an important role in shaping community assembly along this gradient, allowing old, distantly related species with convergent adaptations to tolerate cooler temperatures (Qian & Ricklefs, 2016;Segovia et al., 2020). ...
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... N orthern Hemisphere forests and shrublands are now dominated by species comprising temperate and subtropical lineages, marking one of the major floristic transitions in the vegetation history of the Cenozoic 1-3 . Paleobotanical reconstructions suggest that a cooling global climate afforded ecological opportunities to plant groups that were physiologically predisposed to disperse into and radiate within broadening seasonal biomes across what would become the Americas and Eurasia [4][5][6][7][8] . Central to this pattern of floristic replacement with significant ecological consequence are the roughly 900 species currently recognized within Fagaceae (oak, beech, chestnut, stone oak). ...
... The oak family plays a major ecological role in terms of sheer abundance of standing biomass 6,[9][10][11][12][13][14][15][16][17] and a variety of mutualistic associations involving ectomycorrhizal fungi [18][19][20] , gall-forming insects [21][22][23] , and seed-dispersing vertebrates [24][25][26][27][28][29] . Interactions between Fagaceae and their co-distributed biota suggests degrees of host specificity and the potential for co-evolution, reciprocal diversification, and expansion of range size. ...
... We hypothesize the shift to windpollination alone did not increase the diversification rate of oak species immediately, but instead served as a predisposed neutral change that later facilitated rapid radiation of this genus during the expansion of seasonal climates (Fig. 1). This hypothesis is partially supported by the findings that oaks have their highest species richness in cool-temperate areas in middle latitudes and montane areas at lower latitudes of the Americas, where they form ecologically dominant forests 6,50 . ...
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Northern Hemisphere forests changed drastically in the early Eocene with the diversification of the oak family (Fagaceae). Cooling climates over the next 20 million years fostered the spread of temperate biomes that became increasingly dominated by oaks and their chestnut relatives. Here we use phylogenomic analyses of nuclear and plastid genomes to investigate the timing and pattern of major macroevolutionary events and ancient genome-wide signatures of hybridization across Fagaceae. Innovation related to seed dispersal is implicated in triggering waves of continental radiations beginning with the rapid diversification of major lineages and resulting in unparalleled transformation of forest dynamics within 15 million years following the K-Pg extinction. We detect introgression at multiple time scales, including ancient events predating the origination of genus-level diversity. As oak lineages moved into newly available temperate habitats in the early Miocene, secondary contact between previously isolated species occurred. This resulted in adaptive introgression, which may have further amplified the diversification of white oaks across Eurasia.
... Phylogenetic niche conservatism refers to a pattern whereby lineages retain ancestral ecological traits (Harvey & Pagel, 1991). At a large scale, high levels of conservatism have been reported for plants (e.g., in the southern hemisphere, Crisp et al., 2009; for the succulent biome, Ringelberg et al., 2020; and across the Americas, Segovia et al., 2020), demonstrating the prevalence of biome stasis at speciation and designating niche conservatism as a key factor structuring the distribution of plant diversity. Even within the moist tropical forest biome, independent phylogenetic reconstructions of the niche of tree lineages were strongly correlated between continents, indicating a worldwide deep phylogenetic signal for the climatic niche (Hardy et al., 2012). ...
... On the African continent and elsewhere, despite the prevalence of niche conservatism in plants (Crisp et al., 2009;Linder et al., 2012;Segovia et al., 2020), many clades have transcended major ecological barriers, such as the forest-savanna boundary (see White, 1978 for Diospyros;Gorel et al., 2019 for Erythrophleum and references therein), but the direction, timing, functional trait association and distribution of such shifts over plant phylogeny have not been characterised at the scale of a whole flora. Here, we determined the climatic niche lability of the African tropical woody flora. ...
... We developed a genus-level phylogeny following Segovia et al. (2020) and Sanchez-Martinez et al. (2020) in which the species were attached to their respective genus as polytomies ( Figure S10). We did not consider large-scale phylogenies resolved to the species level because they are still largely based on plastid markers and their topologies are not reliable for many genera due to recurrent chloroplast captures (see references in SI). ...
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Climatic niche evolution during the diversification of tropical plants has received little attention in Africa. To address this, we characterised the climatic niche of >4000 tropical African woody species, distinguishing two broad bioclimatic groups (forest vs. savanna) and six subgroups. We quantified niche conservatism versus lability at the genus level and for higher clades, using a molecular phylogeny of >800 genera. Although niche stasis at speciation is prevalent, numerous clades individually cover vast climatic spaces suggesting a general ease in transcending ecological limits, especially across bioclimatic subgroups. The forest biome was the main source of diversity, providing many lineages to savanna, but reverse shifts also occurred. We identified clades that diversified in savanna after shifts from forest. The forest‐savanna transition was not consistently associated with a growth form change, though we found evolutionarily labile clades whose presence in forest or savanna is associated respectively with climbing or shrubby species diversification. We provided new knowledge on the climatic niche evolution during the diversification of African tropical plants. We characterized the climatic niche of >4000 tropical African woody species, distinguishing two broad bioclimatic groups (forest vs. savanna) and six subgroups. Although niche stasis at speciation is prevalent, numerous clades individually cover vast climatic spaces suggesting a general ease in transcending ecological limits. The forest biome was the main source of diversity, providing many lineages to savanna, but reverse shifts also occurred.
... In addition, environmental filtering imposed by Pleistocene climate variations (ca. 2.6 Ma to 11,000 years) and present climatic and edaphic conditions constrain the establishment of new species, contributing to distinctive species assemblages within the continents (6,10,11). Climatic seasonality has been suggested to be the most important environmental condition defining the main boundaries of Neotropical bioregions (6), the floristic distinctions between neighboring evergreen, deciduous and semideciduous forests (12,13), and the dominant functional traits of moist forests (14). Biogeographical patterns in floristic variation have been documented for old-growth forests (15)(16)(17)(18), but not for the subset of species that colonize successional forests in human-modified landscapes across the Neotropics. ...
... The main factors associated with the 14 floristic groups of species composition were location and climatic and edaphic conditions, similar to patterns found for old-growth forests (6,11,36). Factors related to anthropogenic impact (previous land-use type, landscape forest cover, and human footprint) were not significantly associated with floristic groups. Together, our results indicate that biogeographic history and ecological filtering, rather than anthropogenic impact, drive variation in species composition of early successional forests at the continental scale in the Neotropics. ...
... In addition, environmental filtering imposed by Pleistocene climate variations (ca. 2.6 Ma to 11,000 years) and present climatic and edaphic conditions constrain the establishment of new species, contributing to distinctive species assemblages within the continents (6,10,11). Climatic seasonality has been suggested to be the most important environmental condition defining the main boundaries of Neotropical bioregions (6), the floristic distinctions between neighboring evergreen, deciduous and semideciduous forests (12,13), and the dominant functional traits of moist forests (14). Biogeographical patterns in floristic variation have been documented for old-growth forests (15)(16)(17)(18), but not for the subset of species that colonize successional forests in human-modified landscapes across the Neotropics. ...
... The main factors associated with the 14 floristic groups of species composition were location and climatic and edaphic conditions, similar to patterns found for old-growth forests (6,11,36). Factors related to anthropogenic impact (previous land-use type, landscape forest cover, and human footprint) were not significantly associated with floristic groups. Together, our results indicate that biogeographic history and ecological filtering, rather than anthropogenic impact, drive variation in species composition of early successional forests at the continental scale in the Neotropics. ...
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Forests that regrow naturally on abandoned fields are important for restoring biodiversity and ecosystem services, but can they also preserve the distinct regional tree floras? Using the floristic composition of 1215 early successional forests (≤20 years) in 75 human-modified landscapes across the Neotropic realm, we identified 14 distinct floristic groups, with a between-group dissimilarity of 0.97. Floristic groups were associated with location, bioregions, soil pH, temperature seasonality, and water availability. Hence, there is large continental-scale variation in the species composition of early successional forests, which is mainly associated with biogeographic and environmental factors but not with human disturbance indicators. This floristic distinctiveness is partially driven by regionally restricted species belonging to widespread genera. Early secondary forests contribute therefore to restoring and conserving the distinctiveness of bioregions across the Neotropical realm, and forest restoration initiatives should use local species to assure that these distinct floras are maintained.
... The ability to withstand cold temperatures and large fluctuations in temperatures are thus expected to be important drivers of plant species distributions along such gradients. Since the thermal tolerances of plants are highly conserved and adaptations to freezing temperatures require specific physiological adaptations [4,5], the evolutionary and phylogenetic histories of species become important in driving species distribution patterns across such environmental gradients [6][7][8]. ...
... This pattern of phylogenetic overdispersion along the tropical montane gradient may stem from a combination of processes. First, freezing temperatures appear to have posed an obstacle to tropical species on an evolutionary time scale [4,5]. The potential physiological pathways for overcoming frost are limited, particularly for woody evergreen species [4]. ...
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Frost and freezing temperatures have posed an obstacle to tropical woody evergreen plants over evolutionary time scales. Thus, along tropical elevation gradients, frost may influence woody plant community structure by filtering out lowland tropical clades and allowing extra-tropical lineages to establish at higher elevations. Here we assess the extent to which frost and freezing temperatures influence the taxonomic and phylogenetic structure of naturally patchy evergreen forests (locally known as shola ) along a mid-upper montane elevation gradient in the Western Ghats, India. Specifically, we examine the role of large-scale macroclimate and factors affecting local microclimates, including shola patch size and distance from shola edge, in driving shola metacommunity structure. We find that the shola metacommunity shows phylogenetic overdispersion with elevation, with greater representation of extra-tropical lineages above 2000 m, and marked turnover in taxonomic composition of shola woody communities near the frost-affected forest edge above 2000 m, from those below 2000 m. Both minimum winter temperature and patch size were equally important in determining metacommunity structure, with plots inside very large sholas dominated by older tropical lineages, with many endemics. Phylogenetic overdispersion in the upper montane shola metacommunity thus resulted from tropical lineages persisting in the interiors of large closed frost-free sholas, where their regeneration niche has been preserved over time.
... Moreover, when possible, species inclusion in the dataset was verified by evaluating herbaria vouchers. Both African (23,44,78) and South American (79)(80)(81) datasets have been explored and validated in previous research aiming to investigate macroecological, biogeographic, and evolutionary research questions within continents. Further details on how both datasets were assembled can be found in the references (23,44,(78)(79)(80)(81) and in the SI Appendix, SI Materials and Methods. ...
... Both African (23,44,78) and South American (79)(80)(81) datasets have been explored and validated in previous research aiming to investigate macroecological, biogeographic, and evolutionary research questions within continents. Further details on how both datasets were assembled can be found in the references (23,44,(78)(79)(80)(81) and in the SI Appendix, SI Materials and Methods. Here, we only included checklists of frost-free areas [fourth criterion of (82)] and below 1,750 m of elevation. ...
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Significance Our full-scale comparison of Africa and South America’s lowland tropical tree floras shows that both Africa and South America’s moist and dry tree floras are organized similarly: plant families that are rich in tree species on one continent are also rich in tree species on the other continent, and these patterns hold across moist and dry environments. Moreover, we confirm that there is an important difference in tree species richness between the two continents, which is linked to a few families that are exceptionally diverse in South American moist forests, although dry formations also contribute to this difference. Plant families only present on one of the two continents do not contribute substantially to differences in tree species richness.
... Many savanna lineages, on the other hand, may already possess the eco-physiological adaptations needed to cope with a seasonally dry climate, which may explain the greater amount of immigration into the Caatinga of lineages that previously inhabited the Cerrado + Pampas region. Such an active role for climatic similarity is also reflected in mechanisms regulating community-level diversity patterns and greater floristic similarity between SDTF and savannas (Dexter et al., 2015;Fernandes et al., 2020;Segovia et al., 2020). ...
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The Brazilian Caatinga is considered the richest nucleus of the Seasonally Dry Tropical Forests (SDTF) in the Neotropics, also exhibiting high levels of endemism, but the timing of origin and the evolutionary causes of its plant diversification are still poorly understood. In this study, we integrate comprehensive sampled dated molecular phylogenies of multiple flowering plant groups and estimations of ancestral areas to elucidate the forces driving diversification and historical assembly in the Caatinga flowering plants. Our results show a pervasive floristic exchange between Caatinga and other neotropical regions, particularly those adjacent. While some Caatinga lineages arose in the Eocene/Oligocene, most dry-adapted endemic plant lineages found in region emerged from the middle to late Miocene until the Pleistocene, indicating that only during this period the Caatinga started to coalesce into a SDTF like we see today. Our findings are temporally congruent with global and regional aridification events and extensive denudation of thick layers of sediments in Northeast (NE) Brazil. We hypothesize that global aridification processes have played important role in the ancient plant assembly and long-term Caatinga SDTF biome stability, whereas climate-induced vegetation shifts, as well as the newly opened habitats have largely contributed as drivers of in situ diversification in the region. Patterns of phylogenetic relatedness of Caatinga endemic clades revealed that much modern species diversity has originated in situ and likely evolved via recent (Pliocene/Pleistocene) ecological specialization triggered by increased environmental heterogeneity and the exhumation of edaphically disparate substrates. The continuous assembly of dry-adapted flora of the Caatinga has been complex, adding to growing evidence that the origins and historical assembly of the distinct SDTF patches are idiosyncratic across the Neotropics, driven not just by continental-scale processes but also by unique features of regional-scale geological history.
... However, the spatial distribution of plants across contrasting precipitation regimes provides a valuable proxy of drought tolerance in observational studies (Esquivel-Muelbert et al. 2019). Although acaulescent and non-acaulescent palm growth forms did not form different climatic groups concerning overall precipitation conditions, acaulescent palms occupied drier environments (mean annual precipitation; Fig. 3), considered the most important climatic variable to distinguish moist from seasonally dry Neotropical plant assemblages (Segovia et al. 2020). We found a geographic division of palm growth form, with non-acaulescent palms mostly distributed in Amazonia and acaulescent across the seasonally dry habitats of South America (Fig. 4). ...
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Rainforests have been a source of lineages to open and seasonally dry habitats throughout Angiosperm evolution, especially in the Neotropics. However, the underlying mechanisms that allow such shifts remain poorly understood at large spatial scales. Here, we test whether acaulescence (an underground stem or a very short stem concealed in the ground) has affected the colonization and speciation in Neotropical seasonally dry habitats by cocosoid palms (Cocoseae). Acaulescent species maintain their growth underground, which increases their chances of survival from prolonged seasonal dry season and frequent fires. We use an integrative approach based on trait‐dependent diversification models, phylogenetic comparative methods and ecological niche models. We found that shifts towards acaulescent growth form were accompanied by evolutionary transitions to seasonally dry habitats. Acaulescent lineages had higher speciation rates than non‐acaulescent ones. However, the interaction between acaulescence and seasonally dry habitats had no significant effect on Cocoseae speciation rates. Acaulescent palms are primarily distributed in Neotropical seasonally dry habitats and non‐acaulescent palms are concentrated in Amazonian rainforests. Our results suggest that an underground stem, with high carbohydrate and water storage capacity, is a preadaptation by which rainforest lineages were able to colonize and diversify in new fire‐prone, increasingly seasonal and drier adaptive zones. The projected global expansion of dry seasonal habitats requires an understanding of how drought‐avoidance functional traits evolve and how they are linked to seasonally dry habitats. Our results are, thus, a step forward in determining plant response mechanisms to drier and seasonal conditions.
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The extent to which phylogenetic biome conservatism vs biome shifting determines global patterns of biodiversity remains poorly understood. To address this question, we investigated the biogeography and trajectories of biome and growth form evolution across the Caesalpinia Group (Leguminosae), a clade of 225 species of trees, shrubs and lianas distributed across the Rainforest, Succulent, Temperate and Savanna Biomes. We focused especially on the little-known Succulent Biome, an assemblage of succulent-rich, grass-poor, seasonally dry tropical vegetation distributed disjunctly across the Neotropics, Africa, Arabia and Madagascar. We reconstructed a time-calibrated phylogeny, assembled species occurrence data and assigned species to areas, biomes and growth forms. These data are used to estimate the frequency of transcontinental disjunctions, biome shifts and evolutionary transitions between growth forms and test for phylogenetic biome conservatism and correlated evolution of growth forms and biome shifts. We uncovered a pattern of strong phylogenetic Succulent Biome conservatism. We showed that transcontinental disjunctions confined within the Succulent Biome are frequent and that biome shifts to the Savanna, Rainforest and Temperate Biomes are infrequent and closely associated with shifts in plant growth forms. Our results suggest that the Succulent Biome comprises an ecologically constrained evolutionary arena spanning large geographical disjunctions across the tropics. © 2018 The Authors.New Phytologist
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The tropics have long been a focal point of interest in ecology and evolutionary biology - but where actually are the tropics? Classically, the tropics have been defined as all areas lying between 23.4° North and South as these zones receive direct overhead solar radiation at some point during the year. However, a suite of different environmental and climatic characteristics have also been employed to classify regions as tropical or not. The aims of this paper are to 1) briefly review some of the different criteria commonly used to define the tropics, 2) map the extent and distribution of tropical land areas according to these different criteria, and 3) asses the concordance between these criteria and a sample of recent "tropical" studies. More specifically, we review eight criteria that are frequently used (implicitly or explicitly) to define the tropics. We then map the location and extent of land areas that are "definitely tropical" (i.e., the core tropics) and areas that are "tropical by most definitions". Finally, we examine how the different classifications apply to tropical research through an analysis of the study locations of > 200 recent tropical biology articles. Depending on the definition, the extent of the terrestrial tropics ranges from 23 million to 66 million km² - a nearly threefold difference. Likewise, the classification of many areas as being tropical vs. non-tropical depends on the specific criterion employed. Of the tropical studies reviewed here, only 44% were based on data collected from the core tropics, and 12% of tropical studies were based on data collected from sites outside of the geographic tropics but with tropical climates. Many different criteria are used to classify areas as tropical vs. non-tropical, leading to inconsistencies when estimating the extent of tropical areas and variation in the classification of ecosystems and species as being tropical vs. non-tropical.
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Several studies have demonstrated the contribution of northern immigrants to the flora of the tropical Andes-the world's richest and most diverse biodiversity hotspot. However, much less is known about the biogeographic history and diversification of Andean groups with southern origins, although it has been suggested that northern and southern groups have contributed roughly equally to the high Andean (i.e., páramo) flora. Here we infer the evolutionary history of the southern hemisphere plant genus Gunnera, a lineage with a rich fossil history and an important ecological role as an early colonising species characteristic of wet, montane environments. Our results show striking contrasts in species diversification, where some species may have persisted for some 90 million years, and whereas others date to less than 2 Ma since origination. The outstanding longevity of the group is likely linked to a high degree of niche conservatism across its highly disjunct range, whereby Gunnera tracks damp and boggy soils in cool habitats. Colonisation of the northern Andes is related to Quaternary climate change, with subsequent rapid diversification appearing to be driven by their ability to take advantage of environmental opportunities. This study demonstrates the composite origin of a mega-diverse biota.
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1) The Cerrado Domain of central Brazil houses the largest extent of savanna in the Neotropics, but despite its simple characterisation as a giant savanna, it contains considerable vegetation heterogeneity that is poorly understood. 2) We aimed to determine how vegetation types in the Cerrado diverge in their tree species composition and what role ecological factors play in driving compositional patterns. 3) We used a dataset of 1,165 tree species inventories spread across the Cerrado Domain, which come from six vegetation types that have a substantial arboreal component: woody savannas, dystrophic cerradão, mesotrophic cerradão, seasonally dry tropical forests, semideciduous forests and evergreen forests. We found three extremes in terms of tree species composition, with clear underlying ecological drivers, which leads us to propose a ternary model, the ‘Cerrado Vegetation Triangle’, to characterize woody vegetation in the Cerrado. At one extreme, we found that semideciduous and evergreen forests are indistinguishable floristically and are found in areas with high water availability. At another extreme lie seasonally dry tropical forests which are found on more fertile soils. At the third extreme, we found that all types of savanna, and dystrophic cerradão, are highly similar in tree species composition and are commonly found in areas of poor soils and high flammability. Mesotrophic cerradão is transitional in tree species composition between savannas and seasonally dry tropical forest. 4) The lack of variation in tree species composition attributed to climatic variables indicates that within homogeneous macroclimatic zones, many types of forest and savanna co-exist due to complex mosaics of local substrate heterogeneity and fire history. 5) Synthesis. Our findings highlight the complexity of forest-savanna transitions in the Cerrado Domain, with relevance for understanding the future of Cerrado vegetation under environmental change. If nitrogen deposition is extensive, some savannas may be more likely to transition to mesotrophic cerradão or even seasonally dry tropical forest whereas if water availability increases these same savannas may transition to semideciduous or evergreen forest. Our ‘Cerrado Vegetation Triangle’ model offers a simple conceptual tool to frame discussions of conservation and management.
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Knowledge about the biogeographic affinities of the world’s tropical forests helps to better understand regional differences in forest structure, diversity, composition, and dynamics. Such understanding will enable anticipation of region-specific responses to global environmental change. Modern phylogenies, in combination with broad coverage of species inventory data, now allow for global biogeographic analyses that take species evolutionary distance into account. Here we present a classification of the world’s tropical forests based on their phylogenetic similarity. We identify five principal floristic regions and their floristic relationships: (i) Indo-Pacific, (ii) Subtropical, (iii) African, (iv) American, and (v) Dry forests. Our results do not support the traditional neo- versus paleotropical forest division but instead separate the combined American and African forests from their Indo-Pacific counterparts. We also find indications for the existence of a global dry forest region, with representatives in America, Africa, Madagascar, and India. Additionally, a northern-hemisphere Subtropical forest region was identified with representatives in Asia and America, providing support for a link between Asian and American northern-hemisphere forests.
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Within the tropics, the species richness of tree communities is strongly and positively associated with precipitation. Previous research has suggested that this macroecological pattern is driven by the negative effect of water‐stress on the physiological processes of most tree species. This implies that the range limits of taxa are defined by their ability to occur under dry conditions, and thus in terms of species distributions predicts a nested pattern of taxa distribution from wet to dry areas. However, this ‘dry‐tolerance’ hypothesis has yet to be adequately tested at large spatial and taxonomic scales. Here, using a dataset of 531 inventory plots of closed canopy forest distributed across the western Neotropics we investigated how precipitation, evaluated both as mean annual precipitation and as the maximum climatological water deficit, influences the distribution of tropical tree species, genera and families. We find that the distributions of tree taxa are indeed nested along precipitation gradients in the western Neotropics. Taxa tolerant to seasonal drought are disproportionally widespread across the precipitation gradient, with most reaching even the wettest climates sampled; however, most taxa analysed are restricted to wet areas. Our results suggest that the ‘dry tolerance' hypothesis has broad applicability in the world's most species‐rich forests. In addition, the large number of species restricted to wetter conditions strongly indicates that an increased frequency of drought could severely threaten biodiversity in this region. Overall, this study establishes a baseline for exploring how tropical forest tree composition may change in response to current and future environmental changes in this region.
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Aim The latitudinal diversity gradient (LDG) is a primary emergent property of the biosphere, yet the cause(s) of this pattern are still debated. Key to many hypotheses is the origins and maintenance of tropical hyperdiversity, and the role of climate in driving low latitude speciation. Here, we analyse patterns of tropical and extratropical floral diversification and migration during the early Palaeogene “greenhouse” interval, to shed further light on the relationship between climatic change, latitude and floral diversity. Location The early Palaeogene, from ~63 to 42 million years ago, of the US Gulf Coastal Plain (GCP) and Colombia. Taxon Terrestrial plants, using pollen and spores as a proxy. Methods We analyse species diversity trends using coverage and sample size‐based interpolation and extrapolation, Chao1 estimated richness, and evenness metrics. Capture–mark–recapture (CMR) modelling is used to estimate origination and extinction probabilities. Origination patterns on the GCP are separated into in situ speciation versus immigration. Results While Colombian (tropical) palynofloral richness and origination rates increased in conjunction with warming, GCP richness remained stable. The single rise in GCP origination rates, coincident with the Palaeocene–Eocene Thermal Maximum, was largely driven by the immigration of Eurasian taxa, rather than in situ origination, which was the case in Colombia. Main conclusions These results show that the relationships among climatic parameters and diversification and dispersal are not straightforward. While temperature may have driven diversification in the tropics, other factors, such as precipitation, insolation or biological interactions, may have constrained diversification in the extratropics. Furthermore, our results suggest that outward dispersal from the tropics was limited in the warm world of the early Palaeogene, with most GCP immigrants being sourced from other extratropical regions. These findings suggest that the tropics and extratropics may have functioned independently at this time.
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Amazonia arguably harbours the highest plant species diversity of all wet tropical regions on earth. There is increasing evidence that this enormous diversity is the product of a rather long and complex process and not of a single cause. Here, we investigated divergence times and diversification dynamics in the Neotropical Quiinoideae (Malpighiales: Ochnaceae s.l.) to explore different evolutionary hypotheses for the accumulation of high species diversity. Additionally, we reappraised the phylogenetic relationships and species circumscriptions using sequences of six plastid and nuclear DNA regions and the most comprehensive taxon sampling of the subfamily to date. Molecular dating indicated that Quiinoideae originated during the late Cretaceous, whereas crown group taxa started to diverge at the Eocene-Oligocene boundary. The lack of rate shifts in this subfamily supports the “museum” model of diversification. The rather constant species accumulation also suggests that the Pleistocene glacial cycles did not play an important role for the diversification of Quiinoideae. While ancestral area reconstruction was inconclusive, the post-Miocene divergence times of the west Amazonian species provided some evidence that these areas might not have been available for colonization until the demise of the Lake Pebas and Acre wetlands. New infrageneric groups were inferred, and some species were found to be non-monophyletic, requiring taxonomic reassessment and demonstrating the need for including multiple individuals per species in species-level phylogenies.