A fully resolved backbone phylogeny reveals numerous
dispersals and explosive diversifications throughout
the history of Asteraceae
Jennifer R. Mandela,1, Rebecca B. Dikowb, Carolina M. Siniscalchia, Ramhari Thapaa, Linda E. Watsonc, and Vicki A. Funkd
aDepartment of Biological Sciences, University of Memphis, Memphis, TN 38152; bData Science Lab, Office of the Chief Information Officer, Smithsonian
Institution, Washington, DC 20024; cDepartment of Plant Biology, Ecology, and Evolution, Oklahoma State University, Stillwater, OK 74078-3013;
and dDepartment of Botany, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012
Edited by Peter H. Raven, Missouri Botanical Garden, St. Louis, MO, and approved May 14, 2019 (received for review March 5, 2019)
The sunflower family, Asteraceae, comprises 10% of all flowering
plant species and displays an incredible diversity of form.
Asteraceae are clearly monophyletic, yet resolving phylogenetic rela-
tionships within the family has proven difficult, hindering our
ability to understand its origin and diversification. Recent molec-
ular clock dating has suggested a Cretaceous origin, but the lack of
deep sampling of many genes and representative taxa from across
the family has impeded the resolution of migration routes and
diversifications that led to its global distribution and tremendous
diversity. Here we use genomic data from 256 terminals to estimate
evolutionary relationships, timing of diversification(s), and biogeo-
graphic patterns. Our study places the origin of Asteraceae at ∼83
MYA in the late Cretaceous and reveals that the family underwent a
series of explosive radiations during the Eocene which were accom-
panied by accelerations in diversification rates. The lineages that
gave rise to nearly 95% of extant species originated and began
diversifying during the middle Eocene, coincident with the ensuing
marked cooling during this period. Phylogenetic and biogeographic
analyses support a South American origin of the family with sub-
sequent dispersals into North America and then to Asia and Africa,
later followed by multiple worldwide dispersals in many directions.
The rapid mid-Eocene diversification is aligned with the biogeo-
graphic range shift to Africa where many of the modern-day tribes
appear to have originated. Our robust phylogeny provides a frame-
work for future studies aimed at understanding the role of the
macroevolutionary patterns and processes that generated the
enormous species diversity of Asteraceae.
biogeography | Compositae | molecular dating | phylogenomics
Asteraceae (Compositae), commonly known as the sunfloweror daisy family, is one of three mega-diverse families that
together account for more than 25% of all extant angiosperm
species. The family, with an estimated 25,000–35,000 species,
comprises 10% of all flowering plant species, and is rivaled only
by Orchidaceae (orchids) and Fabaceae (legumes). Members of
the sunflower family occur on every continent including Antarctica
(1) and in nearly every type of habitat on Earth with the greatest
concentration of its species in deserts, prairies, steppes, montane
regions, and areas with Mediterranean-like climates.
The unique floral and fruit traits of Asteraceae are thought to have
contributed to the evolutionary and ecological success of the family.
Specifically, the flower (floret) develops into a fruit that possesses a
highly modified calyx (pappus) with dual functionality for seed dis-
persal and antiherbivory (2). While all of the Asteraceae florets es-
sentially share this basic floral plan, tremendous floral diversity has
arisen from marked differences in corolla size, degree of petal fusion,
symmetry, and color. The most obvious floral feature of the family is
its developmentally complex, head-like inflorescence, the capitulum,
which has a compound receptacle to which many tightly packed florets
are attached. This is exemplified by the iconic North American sun-
flower that mimics a single flower for pollinator attraction (Fig. 1I).
The sunflower family is morphologically distinct from its sister
family and its monophyly has never been disputed; however, using
molecular data to resolve intrafamilial relationships to understand
its migrations and diversifications has proven difficult. This may be
due, at least in part, to its history of hybridization, rapid radiations,
and rampant polyploidy (3). Large-scale gene and genome duplica-
tions have likely been a significant contributor to the evolutionary
and ecological success of Asteraceae. Transcriptome data have been
used to document ancient whole genome duplications (WGDs) at
the base of several of the family’s major radiations (4–6), and WGD
may be associated with increased species diversification rates (7, 8).
Furthermore, gene families have been identified that play a role in
phenotypic evolution for floral symmetry and capitulum develop-
ment (9, 10), as well as for the diversity and abundance of secondary
metabolites that provide antiherbivory properties (11–13).
Early plastid phylogenies (14, 15) definitively placed Asteraceae’s
origin in South America, which remains supported by all subsequent
phylogenies. Several hypotheses of dispersal out of South America
have been proposed that include at least three migration pathways: a
Pacific–Asian route, a North American–Asian route, and direct dis-
persal from South America to Africa (16–18). However, testing these
hypotheses has been challenging because a robust backbone phylog-
eny with comprehensive sampling is not available, and the most re-
cent supertree phylogeny has many areas that are unresolved (19)
Significance
Flowering plant species represent at least 95% of all vascular
plants on Earth, and members of the sunflower family com-
prise roughly 10% of this diversity. The family is often con-
sidered taxonomically difficult primarily because it is enormous
in size and cosmopolitan in distribution. Using phylogenomics,
we were able to fully resolve the backbone of the sunflower
family tree. We provide evidence for a late Cretaceous origin
followed by explosive diversifications and dispersals during the
middle Eocene—ultimately resulting in the family’s 25,000+ ex-
tant species. Our results provide a framework to interpret the
spatiotemporal patterns of migration out of South America and
the family’s explosive diversifications out of Africa that led to its
global evolutionary and ecological success.
Author contributions: J.R.M., R.B.D., L.E.W., and V.A.F. designed research; J.R.M., R.B.D.,
C.M.S., R.T., L.E.W., and V.A.F. performed research; J.R.M., R.B.D., C.M.S., R.T., L.E.W., and
V.A.F. analyzed data; and J.R.M., C.M.S., R.T., L.E.W., and V.A.F. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This open access article is distributed under Creative Commons Attribution-NonCommercial-
NoDerivatives License 4.0 (CC BY-NC-ND).
Data deposition: Raw sequencing reads were deposited in the National Center for Bio-
technology Information (NCBI) Sequence Read Archive and Genbank under BioProject
PRJNA540287. The resulting alignments and phylogenetic trees were deposited in
FigShare at https://doi.org/10.6084/m9.figshare.7697834 and https://doi.org/10.6084/m9.
figshare.7695929.
1To whom correspondence may be addressed. Email: jmandel@memphis.edu.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1903871116/-/DCSupplemental.
Published online June 17, 2019.
www.pnas.org/cgi/doi/10.1073/pnas.1903871116 PNAS | July 9, 2019 | vol. 116 | no. 28 | 14083–14088
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(SI Appendix, Fig. S1). Until recently the family was considered to be
relatively young (50–40 MYA) based on its existing fossil record (19,
20), and this time frame is consistent with molecular clock dating
studies focused on the Southern Hemisphere origins of several an-
giosperm orders, including Asterales (21, 22). However, three recent
phylogenetic studies of Asteraceae using new fossil evidence (reviewed
in ref. 23) and a broader sampling of the family provided older age
estimates and placed its origin sometime in the late Cretaceous, 89–69
MYA (6, 23, 24). These studies also used additional markers and
increased our knowledge of the evolutionary history of the family
which called into question its age and the influence of past geological
and paleoclimatic events on early migrations and diversifications.
However, these studies had incomplete sampling of key lineages along
the backbone of the Asteraceae tree, limiting conclusions about
migration routes.
In this study, we used phylogenomic data, targeting roughly 1,000
loci in the nuclear genome, to estimate the most robust and com-
prehensive backbone phylogeny for Asteraceae to date. We employed
molecular clock dating methods and model-based biogeographic and
diversification rate analyses to estimate the ages and ancestral geo-
graphic ranges for all stem nodes along the backbone of the tree and
for crown nodes at the base of major radiations to interpret lineage
diversifications. We aimed to gain a more precise understanding of the
family’s origin and major diversifications in both space and time, as well
as, what role dispersals and the global climate may have played during
the evolution of this tremendously successful angiosperm lineage.
Results
Phylogeny of Asteraceae. The concatenated alignment of 935 nuclear
loci yielded a data matrix of 942,707 bp for 256 species (Dataset S1).
The integration of transcriptome data was successful and is exem-
plified by the four pairs of duplicate taxa (four from the 1KP and
four from our workflow) forming sister group relationships in our
analyses (SI Appendix, Fig. S2). High branch support and resolution
resulted, and near complete congruence between the maximum
likelihood (ML) and Bayesian concatenated trees was recovered
(Fig. 2 and SI Appendix, Figs. S2 and S3). The ASTRAL tree yielded
some topological differences compared with the concatenated phy-
logenies, but in nearly every case, the ASTRAL tree nodes had lower
support (SI Appendix, Fig. S4). We found a few major differences
from previous phylogenies in tribal placements. For example, in our
ML tree, Hyalideae was placed sister to Stifftieae, and Pertyeae
diverged just before the Carduoideae subfamily (thistles) and im-
mediately after the monotypic Hecastocleideae. Two subfamilies
previously circumscribed (17, 25) are not supported as monophyletic:
Carduoideae [here recovered as three clades: (i) Cardueae, (ii) Old-
enburgieae + Tarchonantheae, and (iii) Dicomeae, brown shading in
Fig. 2]; and Cichorioideae [dandelions, here recovered as two clades:
(i) tribe Cichorieae and (ii) six remaining tribes referred to herein as
Vernonioideae (26) blue shading in Fig. 2]. In the enormous subfamily
Asteroideae (17,000+ species), relationships among the five tribes that
comprise nearly 10,000 species, including Anthemideae (chrysanthemums),
Astereae (asters), Gnaphalieae (strawflowers), Calenduleae (pot
marigolds), and Senecioneae (ragworts), were resolved with high
support (Fig. 2). The exception was the sister group relationship
between Anthemideae and Senecioneae with bootstrap support for
this relationship lower than at most other nodes at 75%. The Bayesian
analysis yielded the same topology for these five tribes with posterior
probabilities of 1.0 (SI Appendix, Fig. S3). The ASTRAL analysis
resulted in high support for a different topology for these five tribes
with Senecioneae as the sister group to a clade of the four remaining
tribes (SI Appendix, Fig. S4). Within the large Heliantheae alliance,
which includes sunflowers and coneflowers (supertribe Helianthodae,
13 tribes), maximal support was recovered for most intertribal rela-
tionships (Fig. 2 and SI Appendix, Figs. S2–S4).
Dating Analysis. The ML phylogeny, calibrated in two analyses by
constraining the minimum ages of nodes with either seven or eight
fossils, provided similar estimates that indicate Asteraceae likely
originated during the Late Cretaceous: ∼83 MYA (95% CI, 91–64
MYA, Fig. 3 and SI Appendix, Figs. S5 and S6 for all CIs, and SI
Appendix, Table S1 for all scenarios tested). The earliest diverging
lineage (64 MYA) is tribe Barnadesieae followed by the mono-
specific Famatinantheae, which diverged from the rest of the family
roughly 62 MYA near the Cretaceous–Paleogene (K–Pg) boundary.
Roughly 5–10 MY passed before extant members of tribes Stiffitieae,
Nassauvieae, Mutisieae, Wunderlichieae, and Gochnatieae began to
diverge during the early Eocene (∼53 MYA). Divergence of the large
clade that includes monotypic Hecastocleideae and the rest of the
family occurred in the early Eocene around 50 MYA. Explosive di-
versifications occurred within the remaining three subfamilies
(Carduoideae, Cichorioideae, and Asteroideae) in the middle to late
Eocene (42–37 MYA) that gave rise to most of the present-day tribes
that harbor 95% of Asteraceae’s extant species. Lastly, the radiation of
the Heliantheae alliance began during the late Oligocene, roughly
25 MYA, including the origins of its tribes (SI Appendix, Figs. S5 and
S6). Our age estimates are in general agreement with three recent
publications which also used the newer fossil data (SI Appendix, Table
S1) (6, 23, and 24).
Historical Biogeography. The AIC model selection supports the
BAYAREALIKE model, including the jump (j) speciation param-
eter (Fig. 3 and SI Appendix, Fig. S7 and Table S2). Our ancestral
range estimates support an origin of Asteraceae in southern South
America with subsequent range extensions into the north and central
Andes region and later into the Guiana Shield region and Brazil.
From South America, Asteraceae likely migrated to North America
but a possible dispersal to south central Africa or to Asia is also
estimated (Fig. 3, see stem node leading to Hecastocleideae and SI
Appendix, Fig. S7). Next, the family dispersed either to south and
central Africa or to Asia. Beginning around 42 MYA, all major
nodes along the backbone of the Asteraceae tree have an ancestral
range of south and central Africa. The only exception is the large
New World Heliantheae alliance with a broad ancestral range es-
timate that includes north and central Andes + Mesoamerica–
Caribbean and the north and central Andes region alone. The
Biogeographic Stochastic Mapping (BSM) results indicate the
presence of numerous dispersal events, some requiring long-distance
Fig. 1. Floral diversity of tribes. (A) Barnadesieae; (B) Famatinantheae; (C)
Stifftieae; (D) Mutisieae; (E) Hecastocleideae; (F) Pertyeae; (G) Cardueae; (H)
Vernonieae; and (I) Heliantheae. Photos of A, C, D, and H were provided by
C.M.S.; B, image courtesy of J. Mauricio Bonifacino (photographer); E, by
V.A.F.; F, image courtesy of Tiangang Gao (photographer); G, image courtesy
of Alfonso Susanna (photographer); and I, by J.R.M.
14084 | www.pnas.org/cgi/doi/10.1073/pnas.1903871116 Mandel et al.
dispersal throughout the entirety of the Asteraceae’s evolutionary
history (59% of total events, SI Appendix, Table S3). Among these
dispersals, anagenetic events (i.e., range expansions) were more
prevalent than founder events (73%). The highest number of anagenetic
events occurred out of the north and central Andes region, south and
central Africa, and North America, respectively. The highest number of
anagenetic events was to North America and the north and central
Andes region, respectively, with the fewest events to south and central
Africa. By far, the greatest number of founder events occurred out of
south and central Africa and coincide with the explosive diversifications
during the middle Eocene. Founder events were highest to North
America and mostly resulted from events out of the north and
central Andes region and Mesoamerica–Caribbean regions co-
inciding with dispersal events during the Miocene (20–5 MYA) (Fig.
3 and SI Appendix, Fig. S7 and Table S3).
Diversification Analyses. The diversification analyses revealed five
instances of rate acceleration (shown in red numbered boxes) and
three of deceleration (shown in blue numbered boxes) (Fig. 3 and SI
Appendix, Fig. S8 and Table S4). The rate decreases (nos. 7, 8, and 9)
occur at nodes leading to tribes with only one or two species. The
five accelerations coincide with major diversifications, including the
core of the family following divergence from tribes Barnadesieae and
Famatinantheae (no. 5), the explosive diversifications in Africa
during the middle Eocene (nos. 2 and 6), and on the stems leading to
the Vernonieae (no. 4) and the Heliantheae alliance (no. 3).
Discussion
Asteraceae Phylogeny Backbone. With at least 25,000 named species
and more than 1,700 genera, the backbone phylogeny of the sun-
flower family has been notoriously difficult to resolve. However, with
increasing access to next generation sequencing technologies, re-
solving the phylogenies of megafamilies has become a reality. Our
phylogenomics approach resulted in a highly resolved and well-
supported nuclear phylogeny that shares similarities with the previously
published plastid (23, 24, 27) and phylotranscriptomic (6) phylogenies
despite the substantial differences in sampling of genomes, loci, and
taxa. It is also important to note there is little discordance among our
different analyses (ML, Bayesian, ASTRAL; Fig. 2 and SI Appendix,
Figs. S2–S4), which may be attributed to our use of the conservative
pipeline, PHYLUCE, for assigning orthology (retaining only loci
recovered as single copy for each taxon). Our deep sampling of genes
and broad, dense sampling of select taxa representing each major
lineage resulted in a fully resolved tree for each of the stem nodes along
the backbone, which was previously intractable. In addition, we sam-
pled a number of genera that have been historically difficult to place,
including Stifftia, Hyalis, Hecastocleis, Cavea, Platycarpha, Gundelia,
Cyclolepis, and Corymbium. The inclusion of anomalous and difficult to
place genera (which also tend to be species poor) is important for
biogeographic analyses of the family since, as previously noted (17),
their placement nearly always anchors a large radiation.
While recent progress has been made to better understand the
evolution of the Asteraceae through molecular phylogenetics using
plastid markers (23, 27) and phylotranscriptomics (6), the highly
resolved backbone of our nuclear phylogeny presented here further
alters our perception of evolution in the family and will necessitate
several changes in its classification, particularly for subfamilies
Stifftioideae, Carduoideae (thistles), and Cichorioideae (dandelions).
First, a few taxa (Hyaloseris, Gongylolepis, and Leucomeris), previously
placed in Wunderlichioideae are now in Stifftioideae, which except for
Leucomeris, are placements also supported by Panero and colleagues
(23, 28). This makes more sense biogeographically and adds an in-
teresting potential for long-distance dispersal events from South America
to Asia for Leucomeris and its sister genus, Nouelia (not sampled here).
Second, our data do not support the monophyly of subfamily Car-
duoideae (sensu 17). The southern African tribes Oldenburgieae +
Tarchonantheae and the widespread African Dicomeae no longer
share a most recent common ancestor (MRCA) with Cardueae (core
thistles) and instead form a grade paraphyletic to Cardueae. Thus, the
classification of Carduoideae needs revision to render it monophyletic.
Third, the Asian Pertyeae is now shown to diverge immediately after
the North American Hecastocleideae. This makes the case for an
earlier arrival of the family into Asia than previously considered (see
section below). Finally, our data do not support the monophyly of
subfamily Cichorioideae, which necessitates a more narrowly defined
Fig. 2. Maximum likelihood tree for the Asteraceae family. Tree is color
coded by subfamily with most tribes indicated in text to the right of each.
Diamonds at nodes indicate bootstrap support of 94% or higher. All nodes
along the backbone have maximal bootstrap support of 100%.
Mandel et al. PNAS | July 9, 2019 | vol. 116 | no. 28 | 14085
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subfamily consisting of only tribe Cichorieae. The six remaining tribes
of subfamily Cichorioideae are monophyletic and need to be rec-
ognized as a separate subfamily named Vernonioideae. These
vernonioid members of the currently defined Cichorioideae are atypical
for Cichorieae, and understanding this new relationship may help
identify the defining traits that support a newly defined Vernonioi-
deae (already described in ref. 29).
Evolution of Asteraceae in Space and Time. Our data provide evi-
dence that Asteraceae most likely originated during the late Cretaceous
(∼83 MYA, 95% CI 91–64) in southern South America and underwent
several range extensions, dispersal events, and diversifications (Fig. 3).
During the Cretaceous, the global climate was warmer than today with
tropical forest vegetation at the poles (30). Cooling began at the end of
the Cretaceous, resulting in increased seasonality (31) with subdeserts
beginning to form in central South America. The oldest lineage is the
enigmatic Barnadesieae which is a small South American tribe of about
90 species with a strikingly different morphology than the rest of the
family, which includes the frequent presence of prominent, paired
axillary spines. Our analyses indicate that additional extant lineages
of Asteraceae did not diverge until after the K–Pg. Alternatively,
earlier lineages from other southern hemisphere continents may
have been lost during this mass extinction event. Given the sparse
fossil record for Asteraceae, and the general difficulty in assigning
late Cretaceous/early Eocene pollen to extant angiosperm genera
(23, 31), there are few data to more fully explore this since the only
Cretaceous Asteraceae fossil evidence (Tubuliflorides lilliei type A,
putatively attributed to Barnadesiodeae) is from Antarctica and New
Zealand (76–66 MYA; refs. 24 and 32), whereas the earliest di-
verging extant lineage is restricted to South America.
Fig. 3. Tribe-level chronogram and ancestral range estimates. Probabilities for ancestral ranges are illustrated in pie charts color coded by geographic regions
on the world map. Diversification rate shifts are indicated on the phylogeny with numbered boxes corresponding to the table above the geographic legend.
Rate shift increases in red and downshifts are blue boxes. Species numbers per tribe are indicated to the Right of tribe names.
14086 | www.pnas.org/cgi/doi/10.1073/pnas.1903871116 Mandel et al.
Toward the end of the Cretaceous and following the K–Pg mass
extinction event (when an estimated five out of six species went
extinct), the global temperature cooled while the Earth experienced
several warming intervals characterized by extreme changes in cli-
mate and carbon cycling: the Paleocene–Eocene Thermal Maximum
(PETM, ∼56 MYA), the Early Eocene Climatic Optimum (EECO,
∼53 MYA), and the Middle Eocene Climatic Optimum (MECO,
∼42 MYA) (33). At the Paleocene–Eocene transition, the earliest
apparent diversification from within the basal grade of Asteraceae
occurred where we detected a rate acceleration on the stem lineage
leading to the Mutisieae sensu Ortiz (34) (∼55 MYA). The PETM
and EECO comprise the warmest periods of the Cenozoic and are
associated with dramatic terrestrial biome shifts, plant migrations,
and accelerated rates of species diversification in many major plant
and animal lineages (35–38). Multiple paleopolyploid events have
been identified in Asteraceae after the divergence of the early lineage
Barnadesieae (5) and along the stem nodes of several large tribes (6).
Further, two recent studies have demonstrated a correlation between
diversification accelerations and WGD in Asteraceae (7, 39). In ad-
dition, climatic instability has been associated with significant WGD
events, and similar to other plant lineages (40), Asteraceae may have
undergone explosive diversifications following WGDs that occurred
during these intense climate upheavals.
Dispersal of Asteraceae out of South America occurred at this
time of dramatic climate change roughly 50 MYA. The BioGeoBEARS
analysis was ambiguous for these nodes in our phylogeny with mul-
tiple possibilities estimated for the ancestral ranges and for the dis-
persal out of South America (Fig. 3 and SI Appendix, Fig. S7). However,
our phylogeny, which has Pertyeae diverging after Hecastocleideae,
suggests a route from South America first through North America and
then to Asia. Previous authors have hypothesized a migration route out
of South America by a North American–Asian route or through a direct
route via Africa (16–19, 23). A number of fossil pollen records, and the
only confirmed capitulum macrofossil for the family, have been de-
scribed from the early- to mid-Eocene in the Southern Hemisphere with
similarities between the extant South American and African floras (e.g.,
refs. 18 and 24). Bremer (16) was the first to hypothesize a North
American–Asian route for Asteraceae, and Panero and Funk (17)
proposed Hecastocleideae as a link to Pertyeae in Asia because the two
tribes share morphological similarities in floral and pollen characters.
The phylogenetic placement of Pertyeae in Panero and Funk (17) was
after the divergence of subfamily Carduoideae of African origin ren-
dering the North American–Asian route less likely. Here, the link to
Asia may be more plausible, given the sequential placement of Hecas-
tocleideae followed by Pertyeae. Moreover, Eocene fossil pollen records
suggest a distribution of Asteraceae in China (41), although the first
reliable North American fossil evidence does not appear until the late
Eocene ∼37 MYA (42). Another possibility is concurrent dispersal to
both North America and Africa during the mid-Eocene.
Whichever path Asteraceae took out of South America, it is clear
that once the family reached Africa during the middle Eocene (∼42
MYA, coincident with the MECO), an explosion of diversification
occurred. By the end of the Eocene, continental interiors had begun
to dry, and forests were thinning out considerably. During this time,
Asteraceae experienced its greatest diversification and subsequent
colonization of the globe. The diversification along the backbone
was both rapid and massive. Our data support a substantial rate
acceleration that ultimately resulted in nearly 95% of the family’s
diversity (Fig. 3, red box no. 2). From their African ancestors, these
tribes diversified and colonized vast areas of the earth. These included
tribes Cardueae (core thistles), Cichorieae (chicory, dandelions, and
lettuce), Calenduleae (pot marigold), Senecioneae (ragwort), Anthe-
mideae (chrysanthemums), Astereae (asters), Gnaphalieae (straw-
flowers), and the MRCA of the Heliantheae alliance (sunflowers and
coneflowers). Another major rate acceleration and diversification
occurred near the end of the Eocene around 36 MYA on the stem
leading to the African-based tribes that include Senecioneae,
Anthemideae, Astereae, and Gnaphalieae that today total nearly
10,000 extant species. WGDs have been detected for Gnaphalieae and
Senecioneae and likely played a role in the diversification of these
large tribes (6). Around 23 MYA, the MRCA of the Heliantheae
alliance diverged from the rest of the family and its descendants ar-
rived in the New World coincident with the end of the Oligocene and
another brief warming period and major climatic shift (Late Oligocene
Warming Event). About 21 MYA, diversifications occurred that
resulted in the segregate tribes of the Heliantheae alliance (rep-
resenting more than 5,600 species), and the highest rate acceleration
measured in our study was along this stem (Fig. 3, red box no. 3).
Previous studies also support a WGD event at the crown node of the
Heliantheae alliance (4, 6) that, along with long-distance dispersal into
new habitats, likely played a major role in its diversification.
While we broadly sampled across Asteraceae, our study still rep-
resents a small portion of the total number of genera in the family
(207 of the ∼1,700 genera). Furthermore, extinctions that took place
during the history of Asteraceae are difficult to account for in historical
biogeographic analyses with a sparse pollen record. Nonetheless, our
primary goal was to estimate the ancestral geographic ranges along the
backbone of the tree, i.e., deep biogeographical events, thus we carried
out this analysis at the level of genus to represent as much geographic
diversity as possible. We coded geographic range by genus sampled, as
opposed to species because species-level sampling is not practical given
the size of the family and wide distribution of some sampled taxa.
However, genus-level, rather than species-level coding could bias the
results toward more widespread ancestral range estimates and/or lower
estimates of founder effects. It is important to note that we did not see
this bias in our results along the backbone of the tree, and our esti-
mates are in general agreement with other biogeographic studies of the
family (25, 43). Still we note that some interpretations of the bio-
geographic estimates, especially of lower taxonomic scales, will require
more extensive sampling in future studies. For example, our sampling
of the two very large tribes, Heliantheae and Eupatorieae, represents
less than 0.005% of the ∼5,600 species within the Heliantheae alliance,
and therefore our limitations in sampling and/or coding could explain
why the ancestral range for this lineage is estimated as more wide-
spread than previous studies which hypothesize a North American
origin (25, 43). Given that our Asteraceae-specific probe set has been
successful in resolving phylogenetic relationships within both tribes and
genera (ref. 44; Fig. 2), future studies testing biogeographical hy-
potheses at these levels may yield further insight into the migrations
and dispersals of the family.
Phylogenomics coupled with biogeographic and diversification
rate analyses have revealed that a series of explosive diversifications
that began during the Eocene resulted in the tremendous diversity of
this family. These diversifications were rapid, occurring in a few million
years, and are associated with extensive dispersal events and significant
climatic changes since the Cretaceous. The impact of these diversifica-
tions and dispersals on angiosperm biodiversity is substantial, with
members of Asteraceae found on every continent and comprising
10% of flowering plants thus encompassing a major component of
angiosperms, the world’s most dominant group of terrestrial plants.
Materials and Methods
Taxon Sampling, Hyb-Seq, and Data Processing. We carried out sequence
capture for 238 samples and incorporated 18 transcriptomes representing 13
subfamilies, ∼45 tribes, 207 genera, and three outgroup taxa (Dataset S2).
Sequence capture was performed and data were processed following the
bioinformatic workflow and methods of ref. 45. Raw sequencing reads were
deposited in the National Center for Biotechnology Information (NCBI) Se-
quence Read Archive under BioProject PRJNA540287.
Phylogenomic and Divergence Time Analyses. We generated phylogenetic
trees based on a concatenated data matrix of all loci using a ML approach,
Bayesian estimation, and a pseudocoalescence method to compute a con-
sensus “species” tree based on individual gene trees. We generated a time-
calibrated ML phylogeny and used fossil calibration points (SI Appendix, Table
S1) to constrain nodes in the ML phylogeny. The resulting alignments and phylo-
genetic trees were deposited in FigShare DOIs 10.6084/m9.figshare.7697834 and
10.6084/m9.figshare.7695929 (46, 47).
Historical Biogeography and Diversification Analyses. Ancestral ranges were
estimated using ML implemented on the dated phylogeny pruned to include
only one species per genus (SI Appendix, Table S5). Diversification rates were
estimated using the dated tree described above and pruned to the level of
Mandel et al. PNAS | July 9, 2019 | vol. 116 | no. 28 | 14087
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tribe (SI Appendix, Table S6). Additional details of the methods are available
in SI Appendix.
ACKNOWLEDGMENTS. We thank the Center for Biodiversity, High Perfor-
mance Computing Cluster, and Feinstone Center at the University of
Memphis; and A. Anderberg, M. Barker, R. Bayer, D. McKenna, S. Herrando-
Moraira, G. Johnson, K. Jones, C. Kelloff, C.Mason, N. Matzke, E. Pasini, E. Schilling,
S. Shin, A. Susanna, and S. Wing. We also thank the many who contributed
samples to the project. This project was funded by the National Science
Foundation Division of Environmental Biology DEB-1745197, Undersecretary
for Science Smithsonian Institution, and Fundação de Amparo à Pesquisa do
Estado de São Paulo 2016/12446-1.
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14088 | www.pnas.org/cgi/doi/10.1073/pnas.1903871116 Mandel et al.