Journal of Systematics

JSE and Evolution doi: 10.1111/jse.12265

Short Communication

The Compositae Tree of Life in the age of phylogenomics

Jennifer R. Mandel1,2*, Michael S. Barker3, Randall J. Bayer1, Rebecca B. Dikow4, Tian-Gang Gao5, Katy E. Jones6,
Sterling Keeley7, Norbert Kilian6, Hong Ma8,9, Carolina M. Siniscalchi1,10, Alfonso Susanna11, Ramhari Thapa1,
Linda Watson12, and Vicki A. Funk13
1
Department of Biological Sciences, University of Memphis, Memphis, TN 38152, USA
2
W. Harry Feinstone Center for Genomic Research, University of Memphis, Memphis, TN 38152, USA
3
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
4
Smithsonian Institute for Biodiversity Genomics, Center for Conservation and Evolutionary Genetics, National Zoological Park and Division of
Mammals, National Museum of Natural History, Smithsonian Institution, Washington DC 20013-7012, USA
5
State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 10093, China
6
Freie Universitat Berlin Botanischer Garten und Botanisches Museum Berlin-Dahlem, K onigin-Luise-Strae 6-8, Berlin 14195, Germany
7
Department of Botany, University of Hawaii, Manoa, Honolulu, HI, 96822, USA
8
Department of Biology and the Huck Institutes of the Life Sciences, the Pennsylvania State University, University Park, PA 16802, USA
9
Ministry of Education Key Laboratory of Biodiversity Sciences and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai
200438, China
10
Departamento de Bot^anica, Universidade de S~ ao Paulo, S~ao Paulo, SP, 05508-090, Brazil
11
Botanic Institute of Barcelona (IBB-CSIC-ICUB), Pg. del Migdia s. n., Spain
12
Department of Plant Biology, Ecology, and Evolution, Oklahoma State University, Stillwater, OK 74078, USA
13
Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington DC 20013-7012, USA
*Author for correspondence. E-mail: jmandel@memphis.edu. Tel.: 901-678-5130. Fax: 901-678-4457.
Received 15 May 2017; Accepted 6 June 2017; Article first published online xx Month 2017

Abstract Comprising more than 25 000 species, the Sunower Family (Compositae or Asteraceae) is the largest
family of owering plants. Many of its lineages have experienced recent and rapid radiations, and the family has a
deep and widespread history of large-scale gene duplications and polyploidy. Many of the most important
evolutionary questions about the familys diversity remain unanswered due to poor resolution and lack of support
for major nodes of the phylogeny. Our group has employed a phylogenomics approach using Hyb-Seq that includes
sequencing
1000 low-copy number nuclear markers, plus partial plastomes for large numbers of species. Here we
discuss our progress to date and present two phylogenies comprising nine subfamilies and 25 tribes using
concatenated and coalescence-based analyses. We discuss future plans for incorporating high-quality reference
genomes and transcriptomes to advance systematic and evolutionary studies in the Compositae. While we have
made great strides toward developing tools for employing phylogenomics and resolving relationships within
Compositae, much work remains. Recently formed global partnerships will work to solve the unanswered
evolutionary questions for this megafamily.
Key words: chloroplast, gene-tree, genomes, Hyb-Seq, next-generation sequencing, nuclear, phylogenetics, sequence capture,
transcriptome.

1 Introduction rubber, and anti-malarial treatment, and nally, they are

The Sunower family (Compositae or Asteraceae) comprises
1012% of all owering plants (25 00033 000 species). They
are widespread, occurring throughout the world, and are
arguably the most ecologically successful among angiosperm
lineages. More than 40 species have been domesticated for
food, medicinal, and ornamental purposes (e.g., artichoke,
lettuce, sunower). The family also includes some of the
worlds most noxious weeds as well as being major
components in many threatened ecosystems (e.g., Southern
African). Numerous members produce novel secondary
compounds that have industrial uses such as insecticides,
among the most frequently grown garden plants.
The family originated in South America at least
5070 Mya,
migrated to Africa where it underwent several explosive
radiations, and eventually colonized all continents on Earth
possibly including Antarctica (see fossil pollen evidence of Barreda
et al., 2015). Though no species occur on Antarctica today, the
current distribution of Compositae is cosmopolitan (Funk et al.,
2005, 2009). This remarkable success has been attributed to a
variety of factors including an abundance and diversity of
secondary metabolites that provide anti-herbivory properties, a
unique dual-function fruit structure (achene) that facilitates long-
distance seed dispersal and inhibits herbivory, and a highly

XXX 2017 | Volume 9999 | Issue 9999 | 16 2017 Institute of Botany, Chinese Academy of Sciences
2 Mandel et al.
specialized head-like inorescence (capitulum) comprised of
different ower types and genders (Funk et al., 2009). Compositae
are also an excellent group for studying biogeography (Funk et al.,
2009; Nie et al., 2016), pollen evolution, secondary chemistry,
paleopolyploidy (Barker et al., 2008, 2016), domestication
(Dempewolf et al., 2008), and invasions (Lai et al., 2012).
2 Unresolved Compositae Backbone and
Large-Scale Phylogenomics
One of the major difculties in testing evolutionary hypothe-
ses for the Compositae family has been the lack of a well-
resolved backbone phylogeny. Its rampant polyploid history is
well documented through cytogenetics (reviewed in Semple
& Watanabe, 2009) and recent studies using transcriptome
data (Barker et al., 2008, 2016; Huang et al., 2016). Rampant
polyploidy makes resolving the backbone of the tree
challenging, requiring independent datasets such as tran-
scriptomes and plastomes. Using a 10-locus chloroplast DNA
data set, Funk and colleagues (Funk et al., 2009) constructed a
tree that included 900/1700 genera but many areas of the tree
remained poorly resolved. These unresolved areas have
hampered evolutionary understanding in the family.
Two recent phylogenetic studies of the family employed 12
plastid markers for 85 species (Panero & Crozier, 2016) and 175
markers selected using an orthology detection workow from
transcriptome data for 73 species (see Huang et al., 2016 for
details). These are the rst studies to more fully reconstruct
phylogenies at the family-wide level. Results of both studies
gave similar topologies and likewise the authors invoked
similar hypotheses to explain diversication of the major
lineages: genome duplication, intercontinental dispersal, and
Eocene paleoclimatic events. While these results are encour-
aging, a more comprehensive approach with greater taxon
sampling and more data are needed to resolve the family
phylogeny and uncertain relationships among taxa at lower
levels in this large family. Moreover, these data would allow
for the evaluation of alternative phylogenetic analysis
methods, e.g., concatenation and multi-species coalescent.
Advances in next-generation sequencing (NGS) have
transformed how evolutionary biologists and systematists
approach phylogenetics. Moving beyond cytoplasmic and
nuclear ribosomal gene sequences, NGS allows the efcient,
and cost-effective sequencing of single/low copy nuclear
genes using a variety of approaches, e.g., whole genome
sequencing, targeted enrichment, genotyping-by-sequencing,
genome skimming, and transcriptomics (reviewed in Zimmer
& Wen, 2015). To address the phylogenetic challenges in the
Compositae using NGS, we developed a Hyb-Seq (target
enrichment) method that includes sequencing
1000 low-
copy number nuclear markers, referred to as the conserved
orthologous set (COS II; Fulton et al., 2002) plus plastomes for
large numbers of species (Mandel et al., 2014, 2015). The use of
sequence capture coupled with NGS allows the opportunity to
sample hundreds of loci across many taxa. Furthermore, a
method based on genomic DNA (vs. RNA/transcriptomes) is
preferable when fresh material is not available, particularly
when museum specimens are the sole resource. In addition,
genomic sequences include relatively rapidly evolving regions,
such as introns, thus providing additional phylogenetic
J. Syst. Evol. 9999 (9999): 16, 2017
resolving power, especially for lower taxon levels (Cai &
Ma, 2016). The Compositae COS (CompCOS) loci were
identied via Expressed Sequence Tags (ESTs) from Cartha-
mus tinctorius L. (safower,
20 000 ESTs), Helianthus annuus
L. (sunower,
70 000 ESTs), and Lactuca sativa L. (lettuce,

70 000 ESTs) (Mandel et al., 2014). Ultimately, this probe set
included 9678 baits targeting 1061 orthologous genes. In
addition to targeting
1000 nuclear loci, we are able to
partially assemble plastomes from off-target capture reads
(e.g., Mandel et al., 2015). Application of our approach in a test
case of 23 species from across Compositae resulted in 763
phylogenetically informative loci (Mandel et al., 2015). The
probe set is currently available via MYcroarray: MyBaits (Ann
Arbor, Michigan) as a catalog item (MYbaits_Comp-COS-1Kv1;
http://www.mycroarray.com/mybaits/mybaits-UCEs.html).
3 Compositae Backbone to Date
We have now tested Hyb-Seq methodology across Compositae
(Mandel et al., 2014, 2015, unpublished data) and in detail for nine
tribes (Jones, Pasini, Siniscalchi, Susanna, Thapa, Watson,
unpublished data). Figure 1 and 2 displays our latest trees that
include 70 Asteraceae species and one Calyceraceae outgroup
species (Table S1). Phylogenetic reconstruction here was carried
out using the phyluce conservative workow (Mandel et al., 2014,
2015) in a Bayesian framework in Fig. 1 (PhyloBayes MPI: 4 chains,
CAT-GTR model, discarded rst 200 trees as burnin when
creating the consensus tree, Lartillot et al., 2009). Figure 2
displays a tree with the same taxa but generated using a
coalescent-based method (ASTRAL-II v4.10.2: gene trees with
RAxML v8 [Stamatakis, 2014], GTRGAMMA, 1000 bootstrap
replicates each and then input into ASTRAL-II using default
parameters, Mirarab & Warnow, 2015). The overall topology of
the tree is similar to previous work (Funk et al., 2009; Huang et al.,
2016; Panero & Crozier, 2016) with some differences. One area of
the tree that varies from previous studies is the nding of a
Carduoideae subfamily that is not supported by the data as
monophyletic in the Bayesian analysis but monophyly is
supported in the ASTRAL tree. Taxon sampling is sparse in this
region for now, and it will be interesting to observe how the
addition of samples in this subfamily affects this nding. Previous
work within Cichorioideae has also demonstrated poor resolu-
tion of some tribal and sub-tribal relationships (e.g., Arctotidinae,
Gorteriinae, Heterolepis, Vernonieae, Liabeae, Funk et al., 2009).
In our latest analysis, the two trees disagree with respect to the
monophyly of Cichorioideae (Fig. 1 vs. Fig. 2), and additional
analyses are needed to understand the cause(s) of this discord.
In general, support values for higher-level relationships across
our latest tree are quite strong (stars 0.95 Bayesian posterior
probability Fig. 1, and bootstrap support Fig. 2), but our
methodology is also shedding light on the lower taxonomic
levels in Compositae.
4 Resolving Lower Taxonomic Levels, an
Example from Chresta: Vernonieae
Chresta Vell. ex DC. has ca. 18 species mostly endemic to the
drier regions of Brazil and is the only genus in subtribe
Chrestinae of Vernonieae. A previous phylogeny using ITS and
www.jse.ac.cn
 The Compositae tree of life 3

Fig. 1. Latest Hyb-Seq Compositae Tree of Life (Bayesian concatenated species tree). Our most recent phylogenetic reconstruction
of the family utilizing the Hyb-Seq methods of Mandel et al., 2014, 2015. Shown are 70 Compositae genera and one outgroup,
Calyceraceae species. Major subfamilies are color-coded: pink Asteroideae, blue Cichorioideae, orange Carduoideae,
green Mutisioideae. Bayesian concatenated species tree. Stars represent  0.95 Bayesian posterior probability.

two plastid markers (Loeuille et al., 2015) partially resolved
relationships within the genus, but with low support among
clades. Also, the relationship of Chrestinae with other
Vernonieae subtribes, specically Lychnophorinae and Verno-
niinae, has been unstable in the two studies that included
Chresta (Keeley et al., 2007; Loeuille et al., 2015). In this
ongoing work (Siniscalchi et al., manuscript forthcoming), we
used the CompCOS loci to recover relationships among 17
Chresta species along with 20 representatives of the main
subtribes in Vernonieae. The sequencing recovered 694
informative loci across 37 species. Phylogenetic analysis using
maximum likelihood recovered maximum bootstrap support
in all clades, except one. With respect to other Vernonieae
included in the analysis, most of the clades recovered in
previous phylogenies were maintained. The CompCOS loci are
effective in recovering both relationships among taxa with
relatively recent divergence (Chresta species) and more
distantly related (the rest of the Vernonieae), an important
feature as Vernonieae is in one of the areas on the Compositae
Tree of Life where relationships are still poorly understood.
5 Gene Tree Discordance
Conicting evolutionary histories and phylogenetic discor-
dance are commonplace, if not pervasive, in phylogenomic
analyses (Roch & Warnow, 2015; Smith et al., 2015; Edwards
et al., 2016; Hosner et al., 2016; Springer & Gatesy, 2016). We
know gene-tree incongruence exists in our work and that of
others (reviewed in Gatesy & Springer, 2014). Coalescent-
based methods for resolving species trees may account
for heterogeneous gene trees and hold promise for
phylogenomic data sets, even in the face of deep coalescence,
incomplete lineage sorting, and mutation (see Liu et al., 2015

www.jse.ac.cn J. Syst. Evol. 9999 (9999): 16, 2017

4 Mandel et al.
Fig. 2. Latest Hyb-Seq Compositae Tree of Life (Coalescent-based species tree using ASTRAL-II). Taxa are labeled as in Fig. 1. Stars
represent  0.95 bootstrap support.
for a nice review of coalescent methods). Other approaches
to handling gene tree discordance have been proposed, e.g.,
statistical binning of loci prior to gene tree estimation
(Mirarab et al., 2014). One approach we have taken to begin
to tackle these issues is by analyzing multi-copy genes using a
clustering approach prior to gene-tree phylogenetic analysis
(see Mandel et al., 2015 for details). Another approach would
be to characterize the function of the CompCOS loci and then
group multi-gene clusters by function. This is based on the
hypothesis that duplicated loci with coordinated functions
would be likely to show comparable evolutionary patterns
across Compositae. We expect to test these and other
hypotheses as we are able to make use of newly available data
(additional taxa sequenced for CompCOS, transcriptomes,
and genomes). Much remains to be understood relative to
how genomic data can be best applied to address issues of not
only gene duplication, and polyploidy, but also of ancient
hybridizations and incomplete lineage sorting. To this end, we
have begun to generate new high quality reference genomes
for key Compositae taxa.
J. Syst. Evol. 9999 (9999): 16, 2017
6 Reference Quality Genome Sequencing
Plant genomes pose signicant bioinformatics challenges
because they are often very large, highly repetitive, and
polyploid. Existing reference-quality plant genomes are over-
represented by domesticated species, which have undergone
signicant articial selection. Four reference quality genomes
are publicly available for Compositae in the subfamilies
Asteroideae (horseweed, Conyza Less., Peng et al., 2014;
sunower, Helianthus L., Badouin et al., 2017), Carduoideae
(artichoke, Cynara L., Scaglione et al., 2016), and Cichorioideae
(lettuce, Lactuca L., Reyes-Chin-Wo et al., 2017). Our group is
generating a reference genome for an undomesticated
oilseed crop with economic importance, Centrapalus
pauciorus (Willd.) H.Rob. (Cichorioideae), sequenced via
single-molecule, long-read sequencing (PacBio) (Dikow et al.,
unpublished data). Centrapalus is from an early diverging
lineage, has a diploid chromosome number, and is found in an
area of the phylogeny (Vernonieae: Cichorioideae) that is
crucial for understanding evolution in the family. Members of
www.jse.ac.cn
 The Compositae tree of life
our co-author group are also sequencing the highly invasive
yellow starthistle (Centaurea L.: Carduoideae; Barker et al.,
unpublished data). Orthology assessment and identifying
gene duplication events across the family will benet
from reference genomes from more basal parts of the
tree and Compositaes species-poor sister family, Calycer-
aceae (61 species in 6 genera), and sequencing such genomes
is a long-term goal of our group.
7 CompCOS Probes Version 2
The original CompCOS probes were designed from genomic
resources we had available at the time in 2011. At that time,
70 000 ESTs (Expressed Sequence Tags) were available for
sunower and lettuce, while just under 20 000 ESTs were
available for safower. This resulted in a CompCOS probe set
that targets roughly 1000 nuclear genes. CompCOS version 1
has provided informative phylogenetic trees, but new genomic
data could be used to add more loci and to rene the probe set.
The array of genomic resources available now is much more
extensive, including published genomes and new Compositae
genomes (sequenced by us) and transcriptomic datasets
recently generated for 62 species in Asteraceae (Huang
et al., 2016). Among these 62 species are members of six
subfamilies, including the three largest subfamilies: Asteroi-
deae, Cichorioideae and Carduoideae, as well as two early-
divergent subfamilies (Mutisioideae and Barnadesioideae). The
numbers of contigs assembled from these transcriptomic
datasets range from over 25 000 to nearly 120 000, providing
rich sequence information for probe design. We will utilize
these new datasets to incorporate additional, potentially
informative, loci to our existing probe set.
8 Partnerships for the Compositae Tree
of Life
Other groups have already mobilized efforts toward resolving
large-scale phylogenetic relationships in mega groups, e.g., in
Poaceae (Soreng et al., 2015); in ferns and lycophytes (Lu et al.,
2015). Through global partnerships, we plan to broaden our
taxonomic and geographic coverage of the family as we
develop a comprehensive and more fully resolved Compositae
Tree of Life. Researchers across the globe have extensive
knowledge of Compositae including biogeography, evolution,
morphology, and systematics. Thus far, the Hyb-Seq methods
and additional genomic and transcriptomic approaches
developed for Compositae have brought together Composi-
tae researchers from around the world to address and
understand phylogenetic relationships in the family. The
integration of information and results from multiple ap-
proaches will also maximize the chance for a comprehensive
phylogenetic foundation for the Compositae community and
plant biologists in general. The collaboration thus far has been
quite remarkable and widespread. We hope to continue and
expand this collaborative effort toward resolving evolutionary
relationships of the Compositae. A robust and comprehensive
phylogeny will be crucial for addressing future studies in the
family including character evolution, paleoclimatic changes,
historical biogeography, and polyploidy.
www.jse.ac.cn
5
Acknowledgements
The authors thank the Undersecretary for Science, Smithso-
nian Institution, for the Next Generation Sequencing Small
Grant to VAF. This research was also supported in part by
the W. Harry Feinstone Center for Genomic Research,
University of Memphis. Portions of the computational work
were conducted in and with the support of the L.A.B. facilities
of the National Museum of Natural History and the newly
organized Smithsonian Institute for Biodiversity Genomics.
CMS is supported by a FAPESP scholarship (2016/12446-1). We
thank many additional partners for assistance with sampling
and analyses including Rachel Jabaily, Gabriel Johnson, Carol
Kelloff, Chase Mason, Eduardo Pasini, and Ed Schilling.
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Supplementary Material
The following supplementary material is available online for
this article at http://onlinelibrary.wiley.com/doi/10.1111/
jse.12265/suppinfo:
Table S1. Species sampled and collection information.
www.jse.ac.cn