vol. 165, no. 3 the american naturalist march 2005
E-Article
Explosive Radiation of Malpighiales Supports a Mid-Cretaceous
Origin of Modern Tropical Rain Forests
Charles C. Davis,1,* Campbell O. Webb,2,? Kenneth J. Wurdack,3,? Carlos A. Jaramillo,4,? and
Michael J. Donoghue2,k
1. Department of Ecology and Evolutionary Biology, University of
Michigan Herbarium, Ann Arbor, Michigan 48108-2287;
2. Department of Ecology and Evolutionary Biology, Yale
University, P.O. Box 208106, New Haven, Connecticut 06520;
3. Department of Botany and Laboratories of Analytical Biology,
Smithsonian Institution, P.O. Box 37012, National Museum of
Natural History, MRC-166, Washington DC 20013-7012;
4. Biostratigraphy Team, Instituto Colombiano del Petro?leo, AA
4185, Bucaramanga, Colombia
Submitted May 12, 2004; Accepted October 27, 2004;
Electronically published February 1, 2005
abstract: Fossil data have been interpreted as indicating that Late
Cretaceous tropical forests were open and dry adapted and that mod-
ern closed-canopy rain forest did not originate until after the
Cretaceous-Tertiary (K/T) boundary. However, some mid-Cretaceous
leaf floras have been interpreted as rain forest. Molecular divergence-
time estimates within the clade Malpighiales, which constitute a large
percentage of species in the shaded, shrub, and small tree layer in
tropical rain forests worldwide, provide new tests of these hypotheses.
We estimate that all 28 major lineages (i.e., traditionally recognized
families) within this clade originated in tropical rain forest well before
the Tertiary, mostly during the Albian and Cenomanian (112?94 Ma).
Their rapid rise in the mid-Cretaceous may have resulted from the
origin of adaptations to survive and reproduce under a closed forest
canopy. This pattern may also be paralleled by other similarly diverse
lineages and supports fossil indications that closed-canopy tropical
rain forests existed well before the K/T boundary. This case illustrates
that dated phylogenies can provide an important new source of ev-
idence bearing on the timing of major environmental changes,
which may be especially useful when fossil evidence is limited or
controversial.
* Corresponding author; e-mail: chdavis@umich.edu.
? E-mail: campbell.webb@yale.edu.
? E-mail: kwurdack@lms.si.edu.
? E-mail: carlos.jaramillo@ecopetrol.com.co.
k E-mail: michael.donoghue@yale.edu.
Am. Nat. 2005. Vol. 165, pp. E36?E65. 
 2005 by The University of Chicago.
0003-0147/2005/16503-40446$15.00. All rights reserved.
Keywords: biome evolution, fossils, K/T boundary, Malpighiales, pe-
nalized likelihood, tropical rain forest.
Modern tropical rain forests are one of the most important
and species rich biomes on the planet. They can be defined
as having a stratified closed canopy, as receiving abundant
precipitation, as experiencing equable temperatures, and
as containing woody angiosperm species, at least in the
understory (Richards 1996; Whitmore 1998; Morley 2000).
During the past 20 years the view has become widespread
that the expansion and diversification of this vegetation
type occurred principally during the past 65 million years,
following the mass extinction event at the Cretaceous-
Tertiary (K/T) boundary (?65 Ma [Tiffney 1984; Wing
and Boucher 1998; Morley 2000; Johnson and Ellis 2002;
Ziegler et al. 2003]; Cretaceous and Cenozoic timescales
following Gradstein et al. [1995] and Berggren et al.
[1995]). This hypothesis was initially supported by the
rarity of large stems (Wheeler and Baas 1991; Wing and
Boucher 1998) and large diaspores (Tiffney 1984; Wing
and Boucher 1998) of angiosperms in the Cretaceous and
by the marked increase in diaspore size in the Early Ter-
tiary. Large seeds facilitate the establishment of seedlings
under a rain forest canopy (Grime 1979).
Studies of fossil leaves and wood (Upchurch and Wolfe
1987, 1993; Wolfe and Upchurch 1987) partially corrob-
orated this pattern by indicating that most Late Cretaceous
floras of southern North America, which was tropical or
nearly so, represented open and subhumid (though not
deciduous) forests. This contrasts with fossil floras in the
same areas after the recovery from the K/T extinction
event, which resemble modern tropical rain forests (Wolfe
and Upchurch 1987; Johnson and Ellis 2002). However,
floras from the early Late Cretaceous (Cenomanian; ?100
Ma) of Kansas, Nebraska, and New Jersey have leaf sizes
and morphologies characteristic of wetter climates (Wolfe
and Upchurch 1987). Upchurch and Wolfe (1993) inter-
preted one flora (Fort Harker, KS) as typical megathermal
(120 mean annual temperature [Upchurch and Wolfe
Dating the Origin of Tropical Rain Forests E37
Table 1: Contemporary importance of tree species of Malpighiales and Ericales (APG 2003) in three tropical rain forests
Location
All species Malpighiales Ericales
No. spp. No. ind. No. spp. No. ind. No. spp. No. ind.
All trees ?10 cm diameter at breast height:
Gunung Palung 325 2,807 69 (21.2) 671 (23.9) 32 (9.8) 320 (11.4)
Dzanga-Sangha 258 2,254 59 (22.8) 537 (23.8) 23 (8.9) 413 (18.3)
Yasun?? 1,092 9,184 107 (9.7) 871 (9.4) 100 (9.1) 832 (9.0)
Trees ?10 cm diameter at breast height:a
Gunung Palung 164 655 46 (28.0) 250 (38.1) 17 (10.3) 114 (17.4)
Dzanga-Sangha 105 407 28 (26.6) 135 (33.1) 7 (6.6) 90 (22.1)
Yasun?? 583 2,139 62 (10.6) 270 (12.6) 44 (7.5) 100 (4.6)
Note: Gunung Palung National Park, West Kalimantan (Webb 1997; Webb and Peart 2000); Dzanga- -Palung p Gunung Sanghap Dzanga
Sangha National Park, Central African Republic (D. Harris and J. Hall, unpublished data; Hall 2003); Yasun?? p Yasun??, Ecuador (Pitman et al.
2001). Figures are the sum of trees and species at a number of sample plots at each site. Percentages of species diversity and of the total number
of individuals are shown in parentheses. (Some plant groups at Dzanga-Sangha have not yet been fully separated into morphotype, and the
numbers here represent an underestimate of the number of species.)
a Species that were not observed to have a maximum diameter 125 cm (i.e., understory trees).
1987]) rain forest and as evidence against the view that
such forests did not originate until the Tertiary.
The advent of strongly supported phylogenies of living
plants based primarily on molecular sequence data pro-
vides a new source of evidence on questions of this sort.
Here we argue that insights into the origin of modern
tropical rain forests (as defined above) can be obtained by
estimating the timing of the diversification of major an-
giosperm clades that inhabit these forests and by dem-
onstrating that the habitat of the ancestral species of these
diversifications most likely occurred in warm, wet, closed-
canopy forests. This novel approach to examining biome
evolution may help to break the impasse on the question
of the age of the modern tropical rain forest when direct
fossil evidence is limited.
One large clade of tropical flowering plants that is es-
pecially suited for such an analysis is Malpighiales (APG
2003). Members of Malpighiales were previously assigned
to 13 different angiosperm orders (Cronquist 1981) and
are highly diverse in both morphology and species (Chase
et al. 2002). They include ?16,000 species (?6% of all
angiosperms; numbers of species from Stevens [2003]; to-
tal angiosperm species diversity from Thorne [2002]) be-
longing to many well-known tropical groups and are an
important component of the understory of tropical rain
forests worldwide (table 1). We used Bayesian, likelihood,
and parsimony methods to estimate the phylogeny and
divergence times of Malpighiales from approximately
6,300 base pairs (bp) of DNA sequence data representing
all three plant genomes: plastid atpB and rbcL, nuclear
ribosomal 18S, and mitochondrial nad1B-C. Given the
resulting trees and data on the ecology of all major lineages
of Malpighiales, we used both parsimony and maximum
likelihood to reconstruct the probable habitat occupied by
the first members of this highly diverse clade.
Material and Methods
Gene Sequencing
Our data sets include 124 species representing all tradi-
tionally recognized families of Malpighiales (APG 2003);
outgroup species from the closely related clades Celastrales,
Oxalidales, and Huaceae (APG 2003; Soltis et al. 2003);
and members of the core eudicot clades Saxifragales (Davis
and Chase 2004) and Caryophyllales (Soltis et al. 2003).
Seventy-seven, 32, 20, and 11 sequences were newly ob-
tained for this study for atpB, rbcL, 18S, and nad1B-C,
respectively; the remaining were obtained from GenBank.
Amplification and sequencing protocols for atpB, rbcL,
18S, and nad1B-C followed Chase et al. (2002), Hoot et
al. (1995), Soltis and Soltis (1997), and Davis and Wurdack
(2004), respectively. Nucleotide sequences were aligned by
eye; the ends of sequences, as well as ambiguous internal
regions, were trimmed from each data set to maintain
complementary data between taxa. The aligned plastid,
nuclear, and mitochondrial data sets included 2,825, 1,653,
and 1,887 bp, respectively. Supplementary information,
including data matrices and trees analyzed in this study,
is available from TreeBASE (http://www.treebase.org) or
the appendixes to this article.
Phylogenetic Analysis
Parsimony bootstrap percentages (Felsenstein 1985) for
each clade were estimated in PAUP? version 4.0b10 (Swof-
ford 2003) from 10,000 heuristic search replicates, tree
bisection-reconnection branch swapping, MulTrees on,
and simple taxon addition (saving 10 trees per replicate).
Parsimony bootstrap consensus trees generated from the
three data sets revealed no strongly supported (?90%
bootstrap) incongruent clades between the independent
E38 The American Naturalist
analyses of the plastid, nuclear, and mitochondrial data
sets and were subsequently analyzed simultaneously with
parsimony and Bayesian methods (Whitten et al. 2000;
Reeves et al. 2001). Parsimony searches were performed
as above, but with 100 random taxon addition replicates
saving all optimal trees at each step.
To choose the optimal model of sequence evolution, we
performed a series of hierarchical likelihood ratio tests (Fel-
senstein 1981; Huelsenbeck and Rannala 1997) using Mo-
deltest version 3.06 (Posada and Crandall 1998). Bayesian
analyses were implemented in MrBayes version 3.0b4 (Huel-
senbeck and Ronquist 2001) under the modelGTR
 I
 G
with default priors for the rate matrix, branch lengths,
gamma shape parameter, and the proportion of invariant
sites. A Dirichlet distribution was used for the base fre-
quency parameters, and an uninformative prior was used
for the tree topology. Ten chains were initiated with a ran-
dom starting tree and run for one million generations sam-
pled every 1,000 generations. Following a burn-in period
of 200,000 generations, trees were sampled from the pos-
terior distribution to calculate clade posterior probabilities.
Habitat Reconstruction
To infer the ancestral habitat of Malpighiales, we optimized
the habitat of major lineages of extant Malpighiales onto
the Bayesian tree with the highest likelihood score and
onto the 162 most parsimonious trees using parsimony
and maximum likelihood as implemented in Mesquite ver-
sion 1.0 (Maddison and Maddison 2003). The habitat of
major lineages of extant Malpighiales was scored as a two-
state character: either inhabiting warm, wet, closed-canopy
forest (i.e., rain forest) or not. Habitat was either ascer-
tained directly from floristic and monographic treatments
or inferred with the aid of distributional information on
rain forests in the Americas (Prance 1989a; Richards 1996),
Africa (White 1983; Richards 1996), Asia (Richards 1996;
Morley 2000), and Australia (Richards 1996). Malpighiales
not found in tropical rain forests typically occur in sa-
vannahs or open woodland habitats in tropical latitudes.
A relatively small number of clades (e.g., some Euphor-
biaceae, Salicaceae, and Violaceae), however, occur in tem-
perate zones. We scored tropical open forest and temper-
ate-zone inhabitants as a single state, ?nonwarm/wet/
closed,? because our primary concern was whether
Malpighiales occupied warm, wet, closed-canopy forest an-
cestrally. Habitat occupancy is a valid character for an-
cestral state reconstruction because it is directly related to
intrinsic (genetically based) physiological characteristics of
taxa that inhabit this biome (Webb et al. 2002). For habitat
scoring see appendix B.
We performed two reconstructions to ascertain the an-
cestral habitat of Malpighiales: one in which habitat was
scored for each family (sensu APG [2003]) and the other
in which it was scored for all genera sampled in the phy-
logenetic analysis. The family-level scoring helped to avoid
sampling bias by ensuring that habitats occupied by un-
sampled genera were also included. Taxa inhabiting both
rain forest and open tropical/temperate habitats were
coded as polymorphic. Assumptions about character
weighting were evaluated under parsimony using step ma-
trices (Maddison 1994) to explore how great a cost must
be imposed on the transition from rain forest for the an-
cestral condition to be unambiguously open tropical/tem-
perate (Ree and Donoghue 1998). For the likelihood re-
constructions, the single fixed tree topology with the
highest likelihood score from Bayesian searches was input
with branch lengths and analyzed under the general Mk1
model (Lewis 2001) with the rate parameter estimated
from the data. Polymorphic taxa were analyzed as either
1 or 0, and each of these reconstructions was performed
twice under the alternative state (i.e., four analyses in
total).
Divergence Time Estimates
We chose the Bayesian tree from above to test for rate
constancy among lineages. Branch lengths and an asso-
ciated likelihood score were calculated on this tree in
PAUP? under the optimal sequence model and associated
parameters with, and without, a molecular clock enforced.
The test statistic 2( ) was compared to a x2 ln L1 ln L0
distribution (with degrees of freedom;n 2 n p
of taxa) to assess significance. A global molecularnumber
clock was rejected ( ) for the combined data set.P ! .05
The nonclock tree was rooted with Dillenia and Peri-
discus, which are members of the core eudicot clades Car-
yophyllales (Soltis et al. 2003) and Saxifragales (Davis and
Chase 2004), respectively (see app. C for full tree). Di-
vergence times were estimated on this tree using penalized
likelihood (PL; Sanderson 2002) as implemented in r8s
version 1.7 (Sanderson 2003). Penalized likelihood has
been shown to outperform both clock and nonclock non-
parametric rate smoothing methods when data depart
from a molecular clock (Sanderson 2002). This method
relies on a data-driven, cross-validation procedure that
sequentially removes taxa from the tree, estimates param-
eters without the removed branch, and calculates the x2
error associated with the difference between the predicted
and actual values. The optimal smoothing value for the
global data set was 31.62.
To estimate standard errors associated with divergence
times, we used the parametric bootstrapping strategy out-
lined by Davis et al. (2002): 100 data sets were simulated
on the r8 smoothed topology using the computer software
Seq-Gen version 1.2.7 (Rambaut and Grassly 1997); re-
Dating the Origin of Tropical Rain Forests E39
Table 2: Fossil age constraints
Extant taxon Fossil taxon
Fossil
type
Oldest reliable age
(Ma) Location
Acalypha1 Acalypha type Pollen Early Paleocene (61.0) China (Kiangsu)
Austrobuxus-Dissilaria clade2 Malvacipollis diversus Pollen Late Paleocene (55.5) Australia
Balanops3 Balanops caledonica Pollen Late Oligocene (23.8) Scotland (Hebrides)
Caryocar4 Retisyncolporites
angularis
Pollen Early Eocene (55.5) Venezuela
Casearia5 Casearia type Pollen (Late) Middle Eocene (37.0) Panama
Chrysobalanus6 Chrysobalanus type Pollen (Early) Middle Eocene
(49.0)
Colorado
Clusiaceae7 Palaeoclusia chevalieri Flower Late Turonian (89.0) New Jersey
Ctenolophon8, 9 Ctenolophonidites
costatus
Pollen Maastrichtian (66.0) Nigeria
Cunoniaceae10 Platydiscus peltatus Flower Early Campanian (83.5) Sweden (Kristianstad
Basin)
Drypetes11 Drypetes type Pollen Late Eocene (33.7) France (Aisne)
Hippomaneae (Homalanthus)12, 13 Crepetocarpon perkinsii Fruit Middle Eocene (40.0) Tennessee
Phyllanthus14 Phyllanthus type Pollen Late Eocene (33.7) Atlantic Ocean
Rhizophoraceae sensu lato
(incl. Erythroxylaceae)15, 16 Zonocostites ramonae Pollen (Early) Late Eocene (36.9) Colombia
Salix-Populus clade17 Pseudosalix handleyi Twigs,
leaves,
flowers
Middle Eocene (48.0) Utah
Stigmaphylloids (Malpighiaceae
crown group)18?20 Perisyncolporites pokornyi Pollen Middle Eocene (49.0) Colombia
Note: Each fossil taxon provides a reliable minimum age estimate for taxa sampled in this study. In the case of palynofossils, we selected only pollen types
that were easily assignable to taxa included in our phylogenetic analyses. Palynofossils assigned to extant taxa are based on taxonomic assessments by Muller
(1981) and updated accordingly for taxonomy and stratigraphy following the numerical references in appendix A (which includes a tree showing fossil
constraints). For Cretaceous and Cenozoic timescales see Gradstein et al. (1995) and Berggren et al. (1995).
sulting simulated data sets were imported into PAUP?, and
branch lengths were estimated on the smoothed topology
for each of these data sets with the sequence model and
parameters estimated from the original data; and resulting
branch length estimates from the simulated data sets were
used to calculate the variance in divergence time estimates
(i.e., 95% confidence interval).
We used four macrofossils and 11 palynofossils from
the Cretaceous and Tertiary as reliable minimum age con-
straints for several internal clades (table 2). Two maximum
age constraints were independently enforced for the basal
node of the tree. We first constrained the basal node to
be no older than 125 m.yr. This corresponds to the earliest
known occurrence of tricolpate pollen, a synapomorphy
that marks the eudicot clade, of which Malpighiales are a
member (Magallo?n et al. 1999; Sanderson and Doyle 2001;
APG 2003). The pollen fossil record has been intensively
studied throughout the initial rise of angiosperms, and
tricolpate pollen increases steadily in abundance and di-
versity from its first isolated reports in the late Barremian,
becoming ubiquitous in the Albian. Hence, it has been
considered unlikely that the eudicot clade originated much
earlier than the late Barremian (Magallo?n et al. 1999; San-
derson and Doyle 2001). This may be an overestimate for
the age of our basal node, which does not correspond to
the entire eudicot clade but rather to core eudicots exclu-
sive of Gunnerales (Soltis et al. 2003). We also chose this
date because it corresponds to the oldest molecular age
estimate by Wikstro?m et al. (2001) for our basal node
(their node 12).
We also constrained the basal node to be no older than
109 m.yr., which was the youngest (and therefore the most
conservative) age estimate by Wikstro?m et al. (2001) for
the same node. Our choice of this constraint was influ-
enced in part by the fact that their youngest estimates dated
the entire eudicot clade (their node 6) as 125 m.yr., which
we have taken as a maximum age for eudicots based on
the fossil record of tricolpate pollen (Magallo?n et al. 1999;
Sanderson and Doyle 2001).
Results
Our phylogenetic analyses and clock-independent dating
estimates indicate that all of the 28 major lineages within
Malpighiales, plus the previously unplaced taxon Centro-
placus (APG 2003), originated well before the K/T bound-
E40 The American Naturalist
ary. Given our maximum age constraint of 125 m.yr. (fig.
1), Malpighiales originated in the late Aptian (114 Ma),
and most major clades began to diversify shortly thereafter.
The optimal age estimates for 24 of these 29 clades imply
that they originated within a 20-m.yr. time window (114?
94 Ma), between the Aptian and through the Cenomanian:
five during the late Aptian (114?112 Ma), 16 during the
Albian (111?100 Ma), and three during the Cenomanian
(98?94 Ma). Three more clades appeared during the Con-
iacian (89?85 Ma), and the two most recently derived
originated during the Campanian (76 Ma).
Optimal age estimates in which the maximum age con-
straint for our basal node was 109 m.yr. yielded similar
results: Malpighiales originated in the mid-Albian (102
Ma), 24 of the 29 clades originated within a 13-m.yr. win-
dow (102?89 Ma) from the Albian to the Turonian, one
during the Santonian (84 Ma), and four during the Cam-
panian (78?72 Ma). These ages are more consistent with
the fossil pollen record because most core eudicots have
tricolpate pollen, which does not appear until within the
Albian (e.g., Doyle and Robbins 1977).
All of our age estimates for crown group Malpighiales
are much older than those inferred by Wikstro?m et al.
(2001; their node 22, 81?74 Ma vs. our estimates of 119?
101 Ma). The conclusion that their estimates are too young
holds even without the use of molecular dating methods
because fossil flowers of Clusiaceae, representing a fairly
derived clade within Malpighiales (perhaps related to the
modern genera Clusia and Garcinia), are known from the
Turonian, about 89 Ma (Crepet and Nixon 1998).
Tropical rain forest was inferred to be the ancestral hab-
itat for Malpighiales, and for most of the clades shown in
figure 1. Under parsimony, a cost of between 2.67 and
3.01 for the Bayesian tree, and between 2.64 and 3.01 for
the parsimony trees, had to be imposed on the transition
from rain forest to open tropical/temperate habitats before
the ancestral condition was inferred to be open tropical/
temperate. Maximum likelihood reconstructions yielded
similarly robust results (table 3).
Discussion
As we have noted, fossil evidence indicates that tropical
rain forest appeared after the K/T event in many areas
where Late Cretaceous forests were apparently more open
and dry adapted (Tiffney 1984; Upchurch and Wolfe 1987,
1993; Wolfe and Upchurch 1987; Wing and Boucher 1998;
Morley 2000; Johnson and Ellis 2002; Ziegler et al. 2003).
Further expansion and taxonomic diversification of this
biome took place during the Cenozoic. The Paleocene-
Eocene transition (?50 Ma) was characterized by high
global temperatures (Wolfe 1978; Upchurch and Wolfe
1987; Zachos et al. 2001) and coincided with a significant
increase in low-latitude palynofloral diversity (Jaramillo
2002). A similar, although less pronounced, climatic op-
timum during the mid-Miocene (?15 Ma; Zachos et al.
2001) resulted in the reexpansion and diversification of
rain forests worldwide (Morley 2000). Finally, Quaternary
(1.6?0 Ma) glacial cycles are thought to account for the
diversification of many species-rich rain forest clades
(Prance 1982; Whitmore and Prance 1987; Behrensmeyer
et al. 1992; Richardson et al. 2001). Major geological events
during the Cenozoic also facilitated the intercontinental
migration of tropical plants, for example, the closing of
the Tethys Seaway (Hall 1998), Paleogene land connections
across the North Atlantic (Tiffney 1985a, 1985b; Davis et
al. 2002a), and Neogene uplift of the Andes and the closure
of the Isthmus of Panama (Gentry 1982; Burnham and
Graham 1999).
Although these Cenozoic events surely contributed to
the diversification of many rain forest clades, age estimates
for Malpighiales suggest that its major lineages originated
well before the K/T boundary. The simplest interpretation
of our results is that Malpighiales occupied closed-canopy,
moist, megathermal forests (i.e., rain forests) during their
early evolution in the mid-Cretaceous. The alternative, that
preexisting lineages in Malpighiales entered the rain forest
habitat independently, would require that all the various
morphological and physiological adaptations associated
with living in this environment (Richards 1996; Whitmore
1998) evolved independently in most of the 29 major line-
ages and that all their non?rain forest ancestors went ex-
tinct. It could be that Late Cretaceous Malpighiales lived
in the wettest, most shaded local habitats in open sub-
humid forests, as suggested by the fact that Turonian Clu-
siaceae, used as our oldest minimum age constraint (Cre-
pet and Nixon 1998), are from a flora (South Amboy)
thought to represent the subhumid interval (Wolfe and
Upchurch 1987) and were ?preadapted? to the appearance
of rain forest climates. However, under this scenario we
would expect to find more lines of Malpighiales persisting
today in drier areas.
Limited Cretaceous fossil data (Upchurch and Wolfe
1987, 1993; Wolfe and Upchurch 1987; Morley 2000) sug-
gest that angiosperm-dominated moist megathermal for-
ests had arisen by the Cenomanian in the interval of the
inferred origin of most rain forest clades in Malpighiales.
Cenomanian leaves from the Dakota Formation of Kansas
and Nebraska and the lower Raritan Formation of New
Jersey (Woodbridge Clay) are physiognomically diverse
and show many of the foliar adaptations characteristic of
understory plants of modern tropical rain forests (Richards
1996), including large leaves with entire margins and drip
tips, as well as plants with probable vining habits (Up-
church and Wolfe 1987, 1993; Wolfe and Upchurch 1987;
Morley 2000). A flora from the Dakota Formation near
Figure 1: Penalized likelihood chronogram of Malpighiales. Figure reduced from 124-taxon data set to represent only the 28 recommended families
of Malpighiales sensu APG (2003) plus the previously unplaced taxon Centroplacus. For outgroups and rooting see text. Bootstrap values and Bayesian
posterior clade probabilities (150%/0.50), respectively, indicated near nodes; bullet p support values ?50%/0.50. The monophyly of Malpighiales
was supported by a very high bootstrap value (100%) and posterior probability (1.0). Confidence intervals shown with shaded bars. Divergence
times were calculated on this rate-smoothed topology by calibrating nodes with several minimum age constraints from macrofossil and palynological
data (table 1). A maximum age constraint of 125 m.yr. was enforced for the root node based on the oldest occurrence of tricolpate pollen grains
representing the eudicot clade (see text). The K/T boundary (?65 Ma) is marked with a dashed line. The origin of Malpighiales is estimated at 114
Ma. The scale bar indicates major Cretaceous and Cenozoic intervals: , , , ,A p Aptian Al p Albian Ce p Cenomanian T p Turonian Cp
, , , , , , , ,Coniacian S p Santonian Cap Campanian M p Maastrichtian Pp Paleocene E p Eocene O p Oligocene Mi p Miocene P/Pp
. For complete 124-taxon chronogram, see appendix C.Pliocene/Pleistocene
E42 The American Naturalist
Table 3: Ancestral habitat for major Malpighiales clades illus-
trated in figure 1 as inferred from maximum likelihood
Taxa
Family scoring
(TRF : OT/T)
Generic scoring
(TRF : OT/T)
TRF OT/T TRF OT/T
Achariaceae 1.0 : 0a .11 : .89a .96 : .04a .99 : .01a
Balanopaceae 1.0 : 0a .99 : .01a .92 : .08a .98 : .02a
Bonnetiaceae .88 : .12 .30 : .70 .61 : .39 .50 : .50
Caryocaraceae 1.0 : 0a .96 : .04a .98 : .02a 1.0 : 0a
Centroplacus 1.0 : 0a .93 : .07a .97 : .03a .98 : .02a
Chrysobalanceae 1.0 : 0a .99 : .01a .92 : .08a .99 : .01a
Clusiaceae .91 : .09a .78 : .22 .75 : .25 .75 : .25
Ctenolophonaceae 1.0 : 0a .93 : .07a .97 : .03a .99 : .01a
Elatinaceae 1.0 : 0a .56 : .44 .87 : .13 .78 : .22
Euphorbiaceae 1.0 : 0a .85 : .15 .99 : .01a 1.0 : 0a
Goupiaceae 1.0 : 0a .11 : .89a .96 : .04a .99 : .01a
Humiriaceae 1.0 : 0a .96 : .04a .98 : .02a 1.0 : 0a
Hypericaceae .01 : .99a .11 : .89a .69 : .31 .38 : .62
Irvingiaceae 1.0 : 0a .95 : .05a .93 : .07a .98 : .02a
Ixonanthaceae 1.0 : 0a .96 : .04a .95 : .05a .98 : .02a
Lacistemataceae 1.0 : 0a .11 : .89a .91 : .09a .82 : .18
Linaceae 1.0 : 0 .95 : .05a .93 : .07a .98 : .02a
Lophopyxidaceae 1.0 : 0a .94 : .06a .84 : .16 .91 : .09a
Malpighiaceae 1.0 : 0a .56 : .44 .87 : .13 .78 : .22
Malpighiales (CG) 1.0 : 0a .86 : .14 .99 : .01a 1.0 : 0a
Ochnaceae 1.0 : 0a .78 : .22 .97 : .03a .99 : .01a
Pandaceae 1.0 : 0a .92 : .08a .99 : .01a .99 : .01a
Passifloraceae 1.0 : 0a .12 : .88a .96 : .04a .98 : .02a
Phyllanthaceae 1.0 : 0a .22 : .78 .94 : .06a .96 : .04a
Picrodendraceae 1.0 : 0a .22 : .78 .94 : .06a .96 : .04a
Podostemaceae .01 : .99a .11 : .89a .69 : .31 .38 : .62
Putranjivaceae 1.0 : 0a .94 : .06a .84 : .16 .91 : .09a
Rhizophoraceae 1.0 : 0a .92 : .08a .99 : .01a 1.0 : 0a
Salicaceae 1.0 : 0a .11 : .89a .91 : .09a .82 : .18
Violaceae 1.0 : 0a .11 : .89a .96 : .04a .98 : .02a
Note: Proportional likelihood values of rain forest habitat (TRF) versus
those in open tropical/temperate environments (OT/T) are separated by a
colon. Reconstructions for both familial and generic scorings are shown and
are further subdivided into analyses in which all taxa that had been scored
as polymorphic were coded as either TRF or OT/T. Boldface indicates stem
groups for which there is significant statistical support for OT/T environments.
Stem clade reconstructions are shown unless otherwise indicated as CG (crown
group).
a Reconstruction judged best as determined by a log-likelihood decline of
at least two units between states (i.e., the threshold value).
Fort Harker, Kansas, contains especially large leaves and
was cited (Upchurch and Wolfe 1987, 1993; Wolfe and
Upchurch 1987) as evidence that typical rain forest orig-
inated much earlier than others have argued. This inferred
period of wetter climates is also supported by paleoclimatic
reconstructions for the Cenomanian (Barron and Wash-
ington 1985; Barron et al. 1989; Beerling and Woodward
2001), which indicate that mid latitudes may have been
similar in precipitation and temperature to present-day
low latitudes. Moreover, vegetation simulations for the
mid-Cretaceous suggest that rain forests could have existed
in low-latitude regions of present-day South America, Af-
rica, northern Australia, and India (Beerling and Wood-
ward 2001), and they may have persisted in similar areas
until the latest Cretaceous (Otto-Bliesner and Upchurch
1997; Upchurch et al. 1998; Beerling and Woodward 2001).
Extraordinary fossil evidence from the Castle Rock flora
of Colorado suggests that highly diverse rain forests were
present in North America shortly after the K/T boundary
(Johnson and Ellis 2002). Johnson and Ellis (2002) inter-
preted these forests as a new phenomenon of the Cenozoic,
but our phylogenetic evidence from Malpighiales, ancillary
evidence from Cenomanian floras such as Fort Harker,
and paleoclimate models suggest instead that on a global
scale, rain forests may be much older. Any Cretaceous rain
forests, however, must have been more geographically re-
stricted than those that developed during the Cenozoic.
Although tropical floras are well known at middle latitudes
in the Late Cretaceous, most of them indicate subhumid
conditions. However, this does not rule out the existence
of wet megathermal vegetation at lower latitudes, where
there are numerous fossil pollen floras but megafossil flo-
ras, which allow more direct inferences on physiognomy
of the vegetation, are rare and poorly known (Upchurch
and Wolfe 1987).
The rarity of large angiosperm diaspores during the Cre-
taceous and their increased size after the K/T boundary
have also been cited as evidence that closed-canopy en-
vironments like those of modern rain forests were not
present during the Cretaceous (Tiffney 1984; Wing and
Boucher 1998). This assumed that larger diaspores help
seedlings become established and survive better in heavily
shaded environments such as the understory of tropical
rain forests. Recent studies (Grubb 1996, 1998; Grubb and
Metcalfe 1996), however, suggest that large diaspores,
while an advantage in low-light environments, are not a
requirement for successful germination and establishment
in the rain forest and may relate more to the ability to
germinate on dense leaf litter than to light availability (see
also Feild et al. 2004). Seeds of contemporary Malpighiales
are on average larger than the mean for samples of all
angiosperms (A. Moles, personal communication, Seed In-
formation Database, Kew Gardens). However, the clusia-
ceous fossil flower from the Turonian of New Jersey was
small, with a multiovulate ovary !1 mm in diameter (Cre-
pet and Nixon 1998). It is possible that the paucity of large
Cretaceous diaspores is partly a function of poor sampling
of low-latitude floras. Large fruits and seeds from the Cam-
panian-Maastrichtian of West Africa were the main ex-
ception noted by Wing and Tiffney (1987) to their gen-
eralization that Cretaceous angiosperm diaspores were
small (cf. Chesters 1955). Another possibility is that the
Dating the Origin of Tropical Rain Forests E43
small size of Cretaceous diaspores reflects not so much
open environments as the absence of bird and mammal
dispersers, whose radiation after the K/T event has been
proposed as an alternative explanation for the Early Ter-
tiary increase in diaspore size (Wing and Tiffney 1987).
Malpighiales account for up to 40% of the understory
tree community in tropical rain forests (table 1). We sug-
gest that Malpighiales were among the earliest angiosperm
colonizers of the understory in the Cretaceous (Crane
1987), following representatives of the basal ANITA grade,
which have been depicted as playing a similar role at the
earliest stages of the angiosperm radiation (Feild et al.
2004). ANITA-grade plants, some eumagnoliids, and Mal-
pighiales may have successfully competed with existing
nonangiospermous plants in the understory, and Mal-
pighiales may have filled a niche that was less occupied
by the other new angiosperm groups: the small, subcanopy
tree. Modern Malpighiales are often 2?10 m tall, are able
to grow and reproduce without direct sunlight, and are
more flexible in growth habit than cycad-like seed plants
(Crane 1987; Feild et al. 2004), that is, like ANITA-grade
plants but generally taller. The recently documented
(Schneider et al. 2004) Late Cretaceous radiation of de-
rived ferns (Polypodiaceae sensu lato) may represent a
parallel occupation of forest floor and epiphytic niches.
Most angiosperm wood fossils from the mid-Cretaceous
are relatively small (Crane 1987; Wing and Boucher 1998),
suggesting that the forest canopy at the beginning of the
radiation of Malpighiales was dominated by large conifers
(Crane 1987). The diversity of conifers remained relatively
steady during the late Albian?early Cenomanian, whereas
cycadophytes, pteridophytes, and pteridosperms exhibited
dramatic declines. Crane (1987) suggested that the latter
taxa were replaced by angiosperm shrubs or small trees.
A similar mixture of dicotyledonous trees and conifers is
found today in the heath and montane forests of southeast
Asia, which contain emergent Agathis or Dacrydium spe-
cies, and the giant Araucaria- and Agathis-dominated rain
forests of Queensland, New Guinea, New Caledonia, and
New Zealand (Richards 1996). By the time of the Ceno-
manian Dakota and Raritan floras, however, the shift in
the dominant trees from conifers to angiosperms had
probably occurred (Upchurch and Wolfe 1987, 1993; Wolfe
and Upchurch 1987; Cantrill and Poole 2005).
The pattern exhibited by Malpighiales may be paralleled
by other similarly diverse tropical clades. Ericales (APG
2003), for example, form a well-supported clade (Bremer
et al. 2002) and are morphologically heterogeneous; their
members have been placed in 11 different angiosperm
orders (Cronquist 1981), and they are similarly species rich
(?11,000 species; see Stevens 2003 and Thorne 2002). Er-
icales also form an important component of the under-
story diversity in tropical rain forests (up to ?22%; table
1). Together, Ericales and Malpighiales account for more
than half of the understory stems in some of these forests
(?55% in Asia and Africa). Molecular divergence-time es-
timates for Ericales suggest that they originated in the
Cretaceous during approximately the same time period as
Malpighiales (?106 Ma [Wikstro?m et al. 2001]). Like Mal-
pighiales, Ericales have a fossil record dating back to the
Turonian (Magallo?n et al. 1999), and it appears that many
of their major lineages may extend back to the Cretaceous
(Bremer et al. 2002) and originated rapidly (Anderberg et
al. 2002). The coincident pattern of diversification in these
two major clades may mark the origin of tropical rain
forests as we know them today. In the case of Malpighiales,
we have demonstrated that dated phylogenies can provide
an important new source of evidence on the timing of
major environmental changes, which may be especially
useful in such cases where direct fossil evidence is limited
or controversial.
Acknowledgments
We thank W. Anderson, P. Ashton, R. Burnham, J. Doyle,
B. O?Meara, J. Rest, M. Sanderson, G. Upchurch, S. Wing,
and M. Wojciechowski for helpful discussion; J. Hall, D.
Harris, and N. Pitman for sharing forest plot data; A.
Moles and the Kew Seed Information Database for seed
size data; D. Mindell and P. Tucker for lab space; and M.
Alford, M. Chase, and M. Simmons for DNA samples.
C.C.D. was supported by the National Science Foundation
(NSF) Assembling the Tree of Life grant (EF 04-31242),
by a Rackham faculty grant from the University of Mich-
igan, and by the Michigan Society of Fellows. C.O.W. was
funded by the NSF (DEB-0212873). K.J.W. was supported
by the Smithsonian Institution and the Lewis B. and Do-
rothy Cullman Program for Molecular Systematic Studies
at the New York Botanical Garden. This article is dedicated
to A. H. Gentry.
APPENDIX A
Numbered references for fossil minimum age constraints presented in table 2 and figure A1. Exact placement of fossil
constraints are shown in figure A1 using the same numbered references. Palynofossils assigned to extant taxa sampled
in our data set were based on taxonomic assessments by Muller (1981) and updated accordingly for taxonomy and
stratigraphy using the references below. Maximum age constraints of 125 and 109 Ma assigned to the basal node from
Magallo?n et al. (1999) and Wikstro?m et al. (2001), respectively.
Figure A1: Fossil constraints; minimum age fossil constraints shown on tree using numbered references in appendix A
Dating the Origin of Tropical Rain Forests E45
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E46
APPENDIX B
Table B1: Taxa sequenced, voucher information, and GenBank accession numbers
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Achariaceae OT/T and TRF
(Cronquist 1981)
(SRFG)
Acharia tragodes
Thunb. Cloete s.n. (BOL) AF209520 AJ418795 AY674643 AF206728 OT/T (Cronquist
1981)
Hydnocarpus sp. Chase 1301 (K) (origi-
nally misdet. as
Ixonanthes
icosandra)
AF209607 AF206783 AY674714 AF206941 TRF (Sleumer 1938,
1954)
Kiggelaria sp. Alford 51 (BH) AY788231 AY788180 AY674719 AY674609 TRF (Sleumer 1975)
Pangium edule
Reinw. Chase 1285 (K) AF209644 AJ18801 AY674742 AF206979 TRF (Sleumer 1954)
Balanopaceae TRF (Carlquist 1980;
Cronquist 1981)
Balanops vieillardii
Baill. Chase 1816 (K) AF209534;
AF089760
AF089760 AY674479 AF206860 TRF (Carlquist 1980;
Cronquist 1981)
Bonnetiaceae OT/T (Maguire 1972;
Robson 1981; Gen-
try 1996)
Archytaea multiflora
Benth. Kubitzki & Feuerer
97-26 (HBG)
AY788202 AY380342 AY674648;
AY674649
AY674574 OT/T (Maguire 1972;
Gentry 1996)
Caryocaraceae TRF (Prance 1973;
Prance and Freitas
da Silva 1973;
Cronquist 1981)
Caryocar glabrum
Pers. Mori 22997 (NY) AF206745 Z75671 AY674662 AF206881 TRF (Prance 1973;
Prance and Freitas
da Silva 1973;
Cronquist 1981)
Celastraceaea OT/T and TRF
(SRFG)
Brexia madagascar-
iensis Thouars Schwerdtfeger 25471
(B); Kew 1977-
14901 (K?); Wur-
dack s.n. (US)
AJ235419 L11176 AY674655 U42543 OT/T (Fosberg and
Renvoize 1980)
Celastrus orbiculatus
Thunb. Simmons 1773 (BH) AY788263 AY788194 AY674664 AY788162 OT/T and TRF (Hou
1955, 1962)
Celastrus scandens
L. Simmons 1783 (BH) AY788264 AY788195 AY674665 AY674581 OT/T and TRF (Hou
1955, 1962)
Denhamia celastro-
ides (F. Muell.) L.
W. Jessup Chase 2050 (K) AY788267 AJ402941 AY674680 AY674591 TRF (Jessup 1984)
E47
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Elaeodendron orien-
tale Jacq. Chase 1213 (K) AY788269 AY380347 AY674689 AY674593 OT/T (de la Bathie
1946; Fosberg and
Renvoize 1980)
Euonymus alatus
Siebold Simmons 1772 (BH) AY788270 AY788197 AY674694 AY788164 OT/T and TRF (Blak-
elock 1951; Hou
1962)
Maytenus arbutifolia
(Hochst. ex A.
Rich.) R. Wilczek Collenette 2/93 (K) AY788271 AY380352 AY674732 AY674616 OT/T and TRF (Hou
1962; Demissew
1985)
Maytenus senegalen-
sis (Lam.) Exell Collenette 4/93 (K) AY788272 AY380353 AY788286 AY788165 OT/T and TRF (Hou
1962; Demissew
1985)
Paxistima canbyi A.
Gray Simmons 1775 (BH) AY788273 AY788198 AY674746 AY674623 OT/T (Navaro and
Blackwell 1990)
Plagiopteron suaveo-
lens Griff. Chase 1335 (K) AJ235562 AJ235787 AY674751 AF206993 TRF (Baas et al. 1979)
Siphonodon celastri-
neus Griff. Chase 2097 (K) AF209676 AF206821 AY674771 AF207021 OT/T and TRF (Hou
1964; Jessup 1984)
Stackhousia minima
Hook. f. Molloy s.n. (CHR) AJ235610 AJ235795 AY674773 AF207026 OT/T (Barker 1984;
Carlquist 1987)
Tripterygium regelii
Sprague &
Takeda Simmons 1776 (BH) AY788260 AY788193 AY674781 AY788161 OT/T (Ma et al. 1999)
Cephalotaceaea OT/T (Lowrie 1998)
Cephalotus folicu-
laris Labill. Chase 147 (NCU) AY788265 L01894 AY674666 U42516 OT/T (Lowrie 1998)
Chrysobalanaceae s.s.b TRF (Prance 1970,
1972a, 1973, 1989a;
1989b)
Atuna racemosa
Rafin. Chase 2118 (K) AY788203 AF089758 AY674650 AY674575 TRF (Prance 1989b)
Chrysobalanus icaco
L. FTG 76-311 (voucher
loc.); Wurdack
AF209562 L11178 AY674668 U42519 TRF (Prance 1970,
1972a)
Hirtella bicornis
Mart. & Zucc. Ducke Res. 2-
303Z.489 (K?)
AY788225 AF089756 AY674706 AY674603 TRF (Prance 1972a,
1973)
Licania sp. Ducke Res. 2-302
(K?); FTG 64-734
(FTG?)
AF209617 L11193 AY788279 U42520 TRF (Prance 1972a,
1973, 1989b)
Clusiaceae TRF (Kubitzki 1978;
Cronquist 1981;
Robson 1981)
Clusia gundlachii
Stahl Chase 341 (NCU) AY788209 Z75673 AY788278 AY674584 TRF (Cronquist 1981)
E48
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Ctenolophonaceae TRF (Van Hooren and
Nooteboom 1988a)
Ctenolophon engleri-
anus Mildbr. Dourse 1572 (K); Mc-
Pherson 16911
(MO)
AY788215 AJ402940 AY674676 AY674589 TRF (Van Hooren and
Nooteboom 1988a)
Cunoniaceaea OT/T and TRF
(Hoogland 1979,
1981; Bradford
1998, 2002)
Eucryphia sp. Strybing Arb 86-0250;
Chase 2528 (K)
AF209584 L01918 AY674693 U42533 OT/T (Bentham and
Mueller 1864)
Dichapetalaceae TRF (Prance 1972b,
1973; Breteler 1991)
Dichapetalum spp. Fisson s.n. (K); Chase
624 (K)
AJ235455 AF089764 AY674683 AF206902 TRF (Prance 1972b,
1973; Breteler 1991)
Dilleniaceaea TRF (Hoogland 1951,
1952)
Dillenia philippine-
nesis Rolfe Chase 2102 (K) AY788268 L01903 AY674684 AY788163 TRF (Hoogland 1952)
Elaeocarpaceaea OT/T and TRF (Bri-
zicky 1965; Baker et
al. 1998)
Crinodendron hook-
erianum Gay Chase 909 (K?) AF209570 AF206754 AY674673 AF206893 OT/T and TRF
(Bricker 1991)
Elaeocarpus spp. D. M. Hicks 8455
(K?); Alverson s.n.
(WIS)
AF209581 AF20675 AY788285 AF206906 TRF (Baker et al.
1998; Coode 2001)
Sloanea spp. Alverson 2211 (WIS);
Chase 343 (NCU)
AJ235603 AF022131 AY674772 U42826 TRF (Smith 1944,
1954)
Elatinaceae OT/T (Tucker 1986;
Leach 1989)
Elatine triandra
Schkuhr Brunton et al. 13384
(MICH); Crins &
Stabb 9600 (MICH)
AY788219 AY380349 AY674690 AY674594 OT/T (Tucker 1986)
Erythroxylaceae OT/T and TRF
(Cronquist 1981)
(SRFG)
Erythroxylum spp. FTG63-251E; Chase
134 (NCU?); Wur-
dack D713 (US)
AJ235466 L13183 AY674692 AF206909 OT/T and TRF (de la
Bathie 1952; Payens
1958; Cronquist
1981; Verdcourt
1984; Plowman
1989; Webster
1994b; Plowman
and Berry 1999)
E49
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Euphorbiaceae OT/T and TRF
(Cronquist 1981;
Webster 1994a;
1994b) (SRFG)
Acalypha californica
Benth. Levin 2192 (SD) AY788199 AY380341 AY674642 AY674571 OT/T and TRF (Web-
ster 1994b)
Clutia tomentosa L. Geumshuizan 6505
(MO)
AY788210 AY788168 AY674669 AY674585 OT/T (Webster 1994a,
1994b)
Codiaeum variega-
tum (L.) Blume Wurdack D33 (US) AY788211 AY788169 AY674670 AY674586 TRF (Airy Shaw
1980a; Radcliffe-
Smith 1987; Web-
ster 1994b)
Conceveiba marti-
ana Baill. Bell 93-176 (US) AY788212 AY788170 AY674671 AY674587 TRF (Webster 1994b;
Murillo 2000)
Croton alabamensis
var. alabamensis
E. A. Smith ex
Chapman Wurdack D8 (US) AY788214 AY788171 AY674675 AY674588 OT/T (Webster 1993,
1994b)
Dalechampia spa-
thulata
(Scheidw.) Baill. Wurdack D10 (US) AY788216 AY788172 AY674677 AY788149 OT/T and TRF (Web-
ster and Armbrus-
ter 1991; Webster
1994b)
Endospermum mol-
uccanum (Teijsm.
& Binn.) Kurz Chase 1258 (K) AY788220 AJ402950 AY674691 AY674595 TRF (Airy Shaw 1972;
Webster 1994b)
Euphorbia spp. Chase 102 (NCU);
voucher unknown
for U42535
AJ235472 AY788174 AY674695 U42535 OT/T and TRF (Web-
ster 1994b)
Hevea sp. Gillespie 4272 (US) AY788223 AY788175 AY674703 AY674601 TRF (Schultes 1990;
Webster 1994b)
Homalanthus popul-
neus (Geiseler)
Pax Chase 1266 (K) AY788226 AY380350 AY674707 AY674604 TRF (Airy Shaw 1968;
Webster 1994b)
Hura crepitans L. Wurdack D89 (US) AY788228 AY788177 AY674711 AY674606 OT/T and TRF (Stan-
dley and Steyer-
mark 1949; Webster
1994b)
Lasiocroton baha-
mensis Pax & K.
Hoffm. Wurdack D58 (US) AY788233 AY788181 AY674723 AY788152 OT/T (Adams 1972;
Webster 1994b)
Neoscortechinia kin-
gii (Hook. f.) Pax
& K. Hoffm. Chase 1265 (K) AY788239 AJ402977 AY674738 AY674619 TRF (Webster 1994b)
E50
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Omphalea diandra
L. Chase 570 (K) AY788241 AY788183 AY674740 AY674622 OT/T and TRF (Airy
Shaw 1980a; Web-
ster 1994b)
Pera bicolor Muell.
Arg. Gillespie 4300 (US) AY788244 AY380355 AY674747 AY674624 TRF (Webster 1994b)
Pimelodendron
zoanthogyne J. J.
Sm. Chase 1268 (K) AY788247 AJ418812 AY674750 AY674628 TRF (Airy Shaw
1980a, 1980b; Web-
ster 1994b)
Pogonophora schom-
burgkiana Miers
ex Benth. Larpin 1022 (US) AY788250 AY788185 AY674755 AY788156 TRF (Webster 1994b)
Ricinus communis L. Wurdack D9 (US);
Hills, unvouchered
AY788253 AY788188 AY674763 AY674633 OT/T (Webster 1994b)
Spathiostemon jav-
ensis Blume Chase 1261 (K) AY788227 AY788176 AY674708 AY788151 TRF (Airy Shaw 1972;
Webster 1994b)
Suregada boiviniana
Baill. Rakotomalaza et al.
1292 (MO)
AY788255 AY788189 AY788284 AY788157 TRF (Airy Shaw 1975,
1980a; Webster
1994b)
Tetrorchidium sp. Bell 93-204 (US) AY788257 AY788191 AY674777 AY788159 TRF (Radcliffe-Smith
1987; Webster and
Huft 1988; Webster
1994b)
Trigonostemon ver-
rucosus J. J. Sm. Chase 1274 (K) AY788259 AY788192 AY674780 AY788160 TRF (Airy Shaw 1975,
1980a; Webster
1994b)
Euphroniaceae OT/T (Steyermark
1987)
Euphronia guianen-
sis (R. H.
Schomb.) H.
Hallier Mori 23699 (NY) AY788221 AF089762 AY674696 AY674597 OT/T (Steyermark
1987)
Goupiaceae TRF (Lundell 1985;
Takhtajan 1997)
Goupia glabra Aubl. Prevost 3031 (CAY) AJ235484 AJ235780 AY674699 AF206920 TRF (Lundell 1985;
Takhtajan 1997)
Huaceaea TRF (Perkins 1909;
Baas 1972; Takhta-
jan 1997)
Afrostyrax sp. Cheek 5007 (K) AJ235385 AJ235771 AY674645 AF206840 TRF (Perkins 1909;
Baas 1972; Takhta-
jan 1997)
E51
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Humiriaceae TRF (Cuatrecasas
1961; Cronquist
1981)
Humiria spp. Anderson 13654
(MICH), Wurdack
s.n. (US)
AJ235495 L01926 AY674710 AF206930 TRF (Cuatrecasas
1961; Cronquist
1981)
Vantanea guianensis
Aubl. Pennington 13855 (K) AY788261 Z75679 AY674783 AY674639 TRF (Cuatrecasas
1961; Cronquist
1981)
Hypericaceae OT/T (Hutchinson
1973; Robson 1974,
1977, 1981, 1987,
1990)
Hypericum spp. Chase 837 (K); Wur-
dack D492 (US)
AF209602 AF206779 AY674715 AF206934 OT/T (Hutchinson
1973; Robson 1974,
1977, 1981, 1987,
1990)
Vismia spp. Miller et al. 9313
(MO); Gustafsson
302 (NY)
AY788262 AF518382 AY674784 AF674640 OT/T (Hutchinson
1973; Robson 1974)
Irvingiaceae TRF (Harris 1996)
Irvingia malayana
Oliv. Simpson 2638 (K?) AF209605 AF123278 AY674717 AF206939 TRF (Harris 1996)
Klainedoxa gabonen-
sis Pierre Bradley et al. 1092
(MO)
AY788232 AY663630 AY674720 AY674610 TRF (Harris 1996)
Ixonanthaceaec TRF (Kool 1988)
Ixonanthes chinensis
Champ. Chen 9812087 (K?) AY788230 AY788179 AY674718 TRF (Kool 1988)
Ochthocosmus longi-
pedicellatus Stey-
erm. & Luteyn Berry 6561 (MO) AY674621 TRF (Kool 1988)
Lacistemataceae TRF (Adams 1972;
Sleumer 1980;
Cronquist 1981;
Takhtajan 1997)
Lacistema aggrega-
tum Rusby Pennington et al. 583
(K)
AF206949 AF206787 AY674722 AF206949 TRF (Adams 1972;
Sleumer 1980;
Cronquist 1981;
Takhtajan 1997)
Lepidobotryaceaea TRF (Hammel and
Zamora 1993;
Takhtajan 1997)
Ruptiliocarpon cara-
colito Hammel &
Zamora Pennington & Zamori
631 (K); Hammel
19102 (MO)
AY788275 AJ402997 AY674765 AY788166 TRF (Hammel and
Zamora 1993;
Takhtajan 1997)
E52
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Linaceae OT/T and TRF (Rog-
ers and Mildner
1976; Cronquist
1981; Van Hooren
and Nooteboom
1988b)
Durandea pentagyna
K. Schum. Takeuchi 7103 (MO) AY788218 AY788173 AY674688 AY788150 TRF (Van Hooren and
Nooteboom 1988b)
Linum spp. Chase 111 (NCU;
Chase 478 (K);
Nickrent 2900
(SIU)
L24401 AY380351 AY674726 L24401 OT/T (Rogers 1969;
Rogers and Mildner
1976; Cronquist
1981)
Reinwardtia indica
Dumort. Chase 230 (NCU) AJ235577 L13188 AY674762 AF207005 OT/T (Robertson
1971; Cronquist
1981)
Lophopyxidaceae TRF (Hutchinson
1973; Takhtajan
1997)
Lophopyxis maingayi
Hook. f. Adelbai P-10203 (US) AY788235 AY663643 AY674728 AY674614 TRF (Hutchinson
1973; Takhtajan
1997)
Malesherbiaceae OT/T (Cronquist
1981; Gentry 1996;
Gengler-Novak
2002)
Malesherbia lineari-
folia Poir. Chase 609 (K) AF209622 AF206792 AY674731 AF206957 OT/T (Cronquist
1981; Gentry 1996;
Gengler-Novak
2002)
Malpighiaceae OT/T and TRF
(Cronquist 1981)
(SRFG)
Acridocarpus natali-
tius Adr. Juss. Goldblatt s.n. (PRE) AY788200 AF344455 AY674644 AY674573 OT/T and TRF (Davis
et al. 2002b)
Byrsonima crassifolia
(L.) H.B.K. FTG 81-680A (MICH) AY788206 L01892 AY674658 AY674579 OT/T (Anderson
2001)
Dicella nucifera
Chodat Anderson 13607
(MICH)
AJ235453 AJ235802 AY674681 AF206901 OT/T and TRF (Chase
1981; Gentry 1996)
Thryallis longifolia
Mart. Anderson 13657
(MICH)
AY788258 AF344516 AY674778 AY674638 OT/T (Anderson
1995)
E53
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Medusagynaceae TRF (Robinson et al.
1989; Fay et al.
1997)
Medusagyne opposi-
tifolia Baker Fay s.n. (K) [Kew
1981?2059]
AJ235530 Z75670 AY674733 AF206959 TRF (Robinson et al.
1989; Fay et al.
1997)
Ochnaceae s.s.b OT/T and TRF (Kanis
1968, 1971; Cron-
quist 1981; Amaral
1991)
Cespedesia bonplan-
dii Goudot Chase 1325 (K) AY788208 AJ420168 AY674667 AY674583 TRF (Kanis 1971;
Amaral 1991)
Ochna multiflora
DC. Chase 229 (NCU) AJ235546 Z75273 AY788280 AF206974 OT/T and TRF (Kanis
1968, 1971; Amaral
1991)
Ochna sp. Davis 31-01 (A) AY788240 AY380354 AY674739 AY674620 OT/T and TRF (Kanis
1968, 1971; Amaral
1991)
Oxalidaceaea OT/T and TRF (Rob-
ertson 1975)
Averrhoa carambola
L. Chase 214 (NCU) AJ235404 L14692 AY674651 AF206859 TRF (Veldkamp 1971;
Robertson 1975)
Dapania racemosa
Korth. Ambri & Arifin 1014
(K)
AY788266 AY788196 AY674678 AY674590 TRF (Veldkamp 1967,
1971; Robertson
1975)
Pandaceae TRF (Forman 1966,
1971; Airy Shaw
1975; Cronquist
1981; Webster
1994b)
Galearia filiformis
(Blume) Boerl. Chase 1334 (K) AY788222 AJ418818 AY674698 AY674598 TRF (Forman 1966,
1971; Airy Shaw
1975; Webster
1994b)
Microdesmis spp. Gereau et al. 5654
(MO); Cheek 5986
(K)
AY788238 AJ402975; AJ403029 AY674737 AY674618 TRF (Le?onard 1961;
Forman 1966; Airy
Shaw 1975; Webster
1994b)
Panda oleosa Pierre. Schmidt et al. 2048
(MO)
AY788242 AY663644 AY788281 AY788153 TRF (Forman 1966,
1971; Webster
1994b)
Passifloraceae s.s.b OT/T and TRF (Killip
1938; Brizicky
1961a; de Wilde
1971, 1972; Holm-
Nielsen et al. 1988;
MacDougal 1994)
E54
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Paropsia madagas-
cariensis (Baill.)
H. Perrier Zyhra 949 (WIS) AF209645 AF206802 AY674744 AF206980 OT/T and TRF (Sleu-
mer 1954; de Wilde
1975)
Passiflora spp. Chase 2475 (K); MO
876630
AJ235553 L01940 AY674745 AF206981 OT/T and TRF (Killip
1938; Brizicky
1961a; de Wilde
1972; Holm-Nielsen
et al. 1988; Mac-
Dougal 1994)
Peridiscaceaea TRF (Sandwith 1962)
Peridiscus lucidus
Benth. Soares 205 (CEPEC) AY372816 AY380356 AY674748 AY372815 TRF (Sandwith 1962)
Phyllanthaceae OT/T and TRF (Airy
Shaw 1975; Rad-
cliffe-Smith 1987;
Webster 1994b;
Dorr 1999)
Aporosa frutescens
Blume Chase 1251 (K) AY788201 Z75674 AY674647 AY788147 TRF (Airy Shaw 1975;
Webster 1994b)
Bischofia javanica
Blume Levin 2200 (SD) AY788205 AY663571 AY674654 AY674578 TRF (Webster 1994b)
Croizatia spp. Berry et al. 4121 (US);
Dorr & Yustiz 8555
(US)
AY788213 AY663579 AY674674 AY788148 TRF (Webster 1994b;
Dorr 1999)
Heywoodia lucens
Sim Saufferer et al. 1544
(US)
AY788224 AY663587 AY674704 AY674602 OT/T and TRF (Rad-
cliffe-Smith 1987)
Phyllanthus epiphyl-
lanthus L. Wurdack D56 (US) AY788246 AY380358 AY674749 AY674627 OT/T and TRF (Web-
ster 1994b)
Picrodendraceae OT/T and TRF (Web-
ster 1994b)
Androstachys john-
sonii Prain Chase 1904 (K) AF209527 AJ402922 AY674646 AF206848 OT/T (Webster 1994b)
Austrobuxus mega-
carpus P. I.
Forster Forster 21239 (BRI) AY788204 AY380343 AY788276 AY674576 TRF (Webster 1994b)
Micrantheum hex-
andrum Hook. f. Chase 1940 (K) AY788237 AJ418816 AY674736 AY674617 TRF (Bentham 1873;
Webster 1994b)
Petalostigma pubes-
cens Domin Clifford s.n. (BRI) AY788245 AY380357 AY788283 AY674626 OT/T (Airy Shaw
1980b)
Podocalyx loranthoi-
des Klotzsch Berry & Aymard 7226
(MO)
AY788248 AY663647 AY674752 AY674629 TRF (Webster 1994b)
Tetracoccus dioicus
Parry Levin 2202 (DUKE) AY788256 AY788190 AY674774 AY788158 OT/T (Webster 1994b)
E55
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Podostemaceae OT/T (van Royen
1953, 1954; Graham
and Wood 1975;
Cronquist 1981)
Podostemum cerato-
phyllum Michx. Cusick 30042 (NY);
Horn & Wurdack
s.n. (DUKE)
AY788249 AJ418819 AY674754 AY788155 OT/T (van Royen
1953, 1954; Graham
and Wood 1975;
Cronquist 1981)
Putranjivaceaec TRF (Airy Shaw 1975,
1980a; Webster
1994b)
Drypetes diversifolia
Krug & Urb. Wurdack D57 (US) AY674687 TRF (Airy Shaw 1975,
1980a; Webster
1994b)
Putranjiva roxbur-
ghii Wall. FTG-83463A AF209578 M95757 U42534 TRF (Airy Shaw 1975,
1980a; Webster
1994b)
Quiinaceae TRF (Cronquist 1981;
Schneider et al.
2002)
Quiina pteridophylla
(Radlk.) Pires Pires S. A. (CPATU)d AF209664 Z75689 AY674759 AF207003 TRF (Cronquist 1981;
Schneider et al.
2002)
Rhizophoraceae s.s.b TRF (Cronquist 1981;
Juncosa and Tom-
linson 1988a,
1988b; Schwarzbach
and Ricklefs 2000)
Bruguiera gymnor-
hiza Lam. Chase 12838 (K) AF209547 AF127693 AY674656 AF206875 TRF (Cronquist 1981;
Juncosa and Tom-
linson 1988a,
1988b; Schwarzbach
and Ricklefs 2000)
Carallia brachiata
(Lour.) Merr. Chase 2151 (K) AJ235425 AF206744 AY674660 AF530810 TRF (Cronquist 1981;
Juncosa and Tom-
linson 1988a,
1988b; Schwarzbach
and Ricklefs 2000)
Paradrypetes subin-
tegrifolia G. A.
Levine Acevedo-Rdgz. &
Ceden?o 7560 (US)
AY788243 AY788184 AY788282 AY788154 TRF (Levin 1992;
Webster 1994b)
Salicaceae OT/T and TRF
(Cronquist 1981)
(SRFG)
Abatia parviflora
Ruiz & Pav. Pennington 676 (K) AF209519 AF206726 AY674641 AF206836 OT/T (Sleumer 1980)
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Casearia spp. Chase 337 (K); Litt 17
(NY); Alford 26
(BH)
AF209557 AF206746 AY674663 AF206882 OT/T and TRF (Sleu-
mer 1954, 1980)
Dovyalis rhamnoides
Burch. ex Harv.
& Sond. Chase 271 (NCU) AY788217 Z75677 AY674686 AY674592 TRF (Sleumer 1975)
Flacourtia jangomas
Steud. Chase 2150 (K) AF209588 AF206768 AY674697 AF206912 OT/T and TRF (Sleu-
mer 1954, 1975)
Idesia polycarpa
Maxim. Chase 561 (K); Wur-
dack D22 (US)
AF209604 AF206781 AY674716 AF206936 OT/T (Mabberley
1997)
Lunania sp. Alford 69 (BH) AY788236 AY788182 AY674729 AY674615 OT/T and TRF (Sleu-
mer 1980)
Poliothyrsis sp. Alford 44 (BH) AY788251 AY788186 AY674756 AY674631 OT/T (Mabberly
1997)
Populus spp. Chase 996 (K); Soltis
& Soltis 2552 (WS)
AF209658 AJ418836 AY674757 AF206999 OT/T (Cronquist
1981; Mabberley
1997)
Prockia sp. Alford 85 (BH) AY788252 AY788187 AY674758 AY674632 OT/T and TRF (Sleu-
mer 1980)
Salix reticulata L. Chase 840 (K) AJ235590 AJ235793 AY674767 AF207011 OT/T (Cronquist
1981)
Scyphostegia bor-
neensis Stapf Beaman 911 (BH) AY788254 AJ403000 AY674770 AY674635 TRF (van Steenis
1957)
Trigoniaceae TRF (Cronquist 1981)
Trigonia nivea
Cambess. Anderson 13656
(MICH)
AF209691 AF089761 AY674779 AF207047 TRF (Cronquist 1981)
Turneraceae OT/T (Lewis 1954;
Brizicky 1961a;
Cronquist 1981;
Arbo 1987, 1995)
Turnera ulmifolia L. Chase 220 (NCU);
Wurdack s.n. (US)
AJ235634 Z75691 AY674782 U42817 OT/T (Lewis 1954;
Brizicky 1961a;
Cronquist 1981;
Arbo 1987, 1995)
Violaceae OT/T and TRF (Bri-
zicky 1961b; Cron-
quist 1981; Hekking
1988)
Hybanthus sp. Alford 89 (BH) AY788229 AY788178 AY674712 AY674607 OT/T and TRF (Bri-
zicky 1961b)
Hymenanthera al-
pina Oliv. Chase 501 (K) AJ235499 Z75692 AY674713 AF206933 OT/T (Brizicky 1961b;
Cronquist 1981;
Hekking 1988)
Leonia glycycarpa
Ruiz. & Pav. Pennington 13852 (K) AY788234 Z75693 AY674725 AY674613 TRF (Brizicky 1961b;
Cronquist 1981;
Hekking 1988)
Dating the Origin of Tropical Rain Forests E57
Table B1 (Continued)
Taxon Voucher
Plastid
(atpB)
Plastid
(rbcL)
Mitochondrial
(nad1B?C)
Nuclear
(18S) Habitat
Incertae sedis
(Centroplacaceae)
Centroplacus glauci-
nus Pierre White 128, ser. 1
(MO)
AY788207 AY663646 AY788277 AY674582 TRF (Webster 1994a)
Note: Families follow APG (2003; but see footnoted modifications), and herbarium acronyms follow Holmgren et al. (1990). Primary habitat shown with source
in parentheses: rain forest; tropical/temperate forest. references for genera; stricto.TRF p tropical OT/Tp open SRFG p see s.s. p sensu
a Indicates outgroups.
b Several small segregate families sampled were maintained for the family-level scoring of habitat following the strict circumscriptions of APG (2003). For
example, representatives of Chrysobalanaceae, Dichapetalaceae, Euphroniaceae, and Trigoniaceae were scored separately rather than as Chrysobalanceae sensu lato.
Other similar strict circumscriptions were followed for Ochnaceae, Passifloraceae, and Rhizophoraceae. Peridiscaceae have been excluded from Malpighiales following
Davis and Chase (2004). Recent molecular evidence indicates that holoparasitic Rafflesiaceae s.s. are members of Malpighiales (Barkman et al. 2004; Davis and
Wurdack 2004). They were not included in our data sets due to missing data. This is because the genes sampled here are largely unsuited for phylogenetic placement
of Rafflesiaceae s.s. due to their reduced chloroplast genome (specifically, the loss of atpB and rbcL) and hypothesized horizontal gene transfer of mitochondrial
nad1B-C from their obligate hosts Tetrastigma (Davis and Wurdack 2004).
c Both genera are combined as one family OTU for molecular analysis.
d Empresa Brasileira de Pesquisa Agropecua?ria.
e Newly proposed family affiliation.
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E60
APPENDIX C
Table C1: Clade age estimates
Clade name
Maximum age constraint 125 Ma Maximum age constraint 109 Ma
Minimum Optimal Maximum Minimum Optimal Maximum
1. Malpighiales 110.7 113.8 119.4 101.1 101.6 105.9
2. Euphorbiaceae 110.7 113.8 119.4 101.1 101.6 105.9
3. Rhizophoraceae s.l. 110.2 113.8 119.3 102.1 101.6 105.7
4. Pandaceae 110.2 113.8 118.7 101.9 101.6 105.5
5. Caryocaraceae 108.5 112.3 117.6 99.5 100.7 103.8
6. Humiriaceae 108.9 112.2 117.2 100.3 101.6 102.8
7. Ochnaceae s.l. 108.2 111.2 116.6 98.8 99.6 103.8
8. Ixonanthaceae 105.9 109.2 114.9 97.5 98.7 102.0
9. Phyllanthaceae 105.8 108.1 114.0 95.6 97.1 101.9
10. Picrodendraceae 105.8 108.1 114.0 95.6 97.1 101.9
11. Passifloraceae s.l. 103.7 108.1 113.9 96.5 96.9 102.1
12. Violaceae 102.4 105.7 112.3 94.4 94.8 99.7
13. Irvingiaceae 102.5 105.0 112.5 93.3 94.5 98.4
14. Linaceae 102.5 105.0 112.5 93.3 94.5 98.4
15. Achariaceae 98.1 104.2 108.1 90.9 93.4 96.1
16. Goupiaceae 98.1 104.2 108.1 90.9 93.4 96.1
17. Centroplacus 96.6 101.8 109.6 88.1 91.0 97.1
18. Ctenolophonaceae 96.6 101.8 109.6 88.1 91.0 97.1
19. Lacistemataceae 96.1 99.8 107.7 89.0 90.1 95.9
20. Salicaceae 96.1 99.8 107.7 89.0 90.1 95.9
21. Balanopaceae 95.5 99.6 106.2 88.5 90.2 94.9
22. Chrysobalanceae s.l. 95.5 99.6 106.2 88.5 90.2 94.9
23. Elatinaceae 89.0 98.2 113.2 85.0 89.1 99.6
24. Malpighiaceae 89.0 98.2 113.2 85.0 89.1 99.6
25. Clusiaceae 92.4 94.1 103.7 87.1 89.0 94.7
26. Bonnetiaceae 85.9 88.5 97.2 83.0 83.8 88.3
27. Lophopyxidaceae 82.9 86.7 97.0 74.8 77.8 85.2
28. Putranjivaceae 82.9 86.7 97.0 74.8 77.8 85.2
29. Hypericaceae 68.9 76.4 82.4 66.4 72.4 73.9
30. Podostemaceae 68.9 76.4 82.4 66.4 72.4 73.9
Note: Optimal age estimates, with minimum and maximum error estimates, for major Malpighiales clades (i.e., families
[stem group], except for Centroplacus). Sensu lato (s.l.) designations follow APG (2003). See figure C1 for full penalized
likelihood chronogram and figure C2 for Bayesian tree with likelihood branch lengths.
E61
Figure C1: Complete 124-taxon penalized likelihood chronogram (from main text, fig. 1). Numbered nodes on chronogram correspond to numbered
clades shown in table C1. The K/T boundary (?65 Ma) is marked with a dashed line. The scale bar indicates major Cretaceous and Cenozoic
intervals: , , , , , , , ,B p Barremian A p Aptian Al p Albian Ce p Cenomanian T p Turonian Cp Coniacian S p Santonian Cap Campanian
, , , , , .M p Maastrichtian Pp Paleocene E p Eocene O p Oligocene Mi p Miocene P/Pp Pliocene/Pleistocene
Figure C2: Complete 124-taxon Bayesian tree with likelihood branch lengths used for r8s analysis
Dating the Origin of Tropical Rain Forests E63
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Editor: Jonathan B. Losos
Associate Editor: Susanne S. Renner