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A Fully Resolved Backbone Phylogeny Reveals Numerous Dispersals and Explosive Diversifications Throughout the History of Asteraceae

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A Fully Resolved Backbone Phylogeny Reveals Numerous Dispersals and Explosive Diversifications Throughout the History of Asteraceae 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 molecular data to resolve intrafamilial relationships to understand plant species and displays an incredible diversity of form. its migrations and diversifications has proven difficult. This may be Asteraceae are clearly monophyletic, yet resolving phylogenetic rela- due, at least in part, to its history of hybridization, rapid radiations, tionships within the family has proven difficult, hindering our and rampant polyploidy (3). Large-scale gene and genome duplica- ability to understand its origin and diversification. Recent molec- tions have likely been a significant contributor to the evolutionary ular clock dating has suggested a Cretaceous origin, but the lack of and ecological success of Asteraceae. Transcriptome data have been deep sampling of many genes and representative taxa from across used to document ancient whole genome duplications (WGDs) at ’ – the family has impeded the resolution of migration routes and the base of several of the family s major radiations (4 6), and WGD diversifications that led to its global distribution and tremendous may be associated with increased species diversification rates (7, 8). diversity. Here we use genomic data from 256 terminals to estimate Furthermore, gene families have been identified that play a role in evolutionary relationships, timing of diversification(s), and biogeo- phenotypic evolution for floral symmetry and capitulum develop- graphic patterns. Our study places the origin of Asteraceae at ∼83 ment (9, 10), as well as for the diversity and abundance of secondary metabolites that provide antiherbivory properties (11–13). MYA in the late Cretaceous and reveals that the family underwent a EVOLUTION Early plastid phylogenies (14, 15) definitively placed Asteraceae’s series of explosive radiations during the Eocene which were accom- origin in South America, which remains supported by all subsequent panied by accelerations in diversification rates. The lineages that phylogenies. Several hypotheses of dispersal out of South America gave rise to nearly 95% of extant species originated and began have been proposed that include at least three migration pathways: a diversifying during the middle Eocene, coincident with the ensuing Pacific–Asian route, a North American–Asian route, and direct dis- marked cooling during this period. Phylogenetic and biogeographic persal from South America to Africa (16–18). However, testing these analyses support a South American origin of the family with sub- hypotheses has been challenging because a robust backbone phylog- sequent dispersals into North America and then to Asia and Africa, eny with comprehensive sampling is not available, and the most re- later followed by multiple worldwide dispersals in many directions. cent supertree phylogeny has many areas that are unresolved (19) The rapid mid-Eocene diversification is aligned with the biogeo- graphic range shift to Africa where many of the modern-day tribes Significance 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 Flowering plant species represent at least 95% of all vascular enormous species diversity of Asteraceae. 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 biogeography | Compositae | molecular dating | phylogenomics in size and cosmopolitan in distribution. Using phylogenomics, we were able to fully resolve the backbone of the sunflower steraceae (Compositae), commonly known as the sunflower family tree. We provide evidence for a late Cretaceous origin Aor daisy family, is one of three mega-diverse families that followed by explosive diversifications and dispersals during the together account for more than 25% of all extant angiosperm — ’ + – middle Eocene ultimately resulting in the family s 25,000 ex- species. The family, with an estimated 25,000 35,000 species, tant species. Our results provide a framework to interpret the comprises 10% of all flowering plant species, and is rivaled only spatiotemporal patterns of migration out of South America and by Orchidaceae (orchids) and Fabaceae (legumes). Members of the family’s explosive diversifications out of Africa that led to its the sunflower family occur on every continent including Antarctica global evolutionary and ecological success. (1) and in nearly every type of habitat on Earth with the greatest concentration of its species in deserts, prairies, steppes, montane Author contributions: J.R.M., R.B.D., L.E.W., and V.A.F. designed research; J.R.M., R.B.D., regions, and areas with Mediterranean-like climates. 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 The unique floral and fruit traits of Asteraceae are thought to have V.A.F. analyzed data; and J.R.M., C.M.S., R.T., L.E.W., and V.A.F. wrote the paper. contributed to the evolutionary and ecological success of the family. The authors declare no conflict of interest. Specifically, the flower (floret) develops into a fruit that possesses a This article is a PNAS Direct Submission. highly modified calyx (pappus) with dual functionality for seed dis- This open access article is distributed under Creative Commons Attribution-NonCommercial- persal and antiherbivory (2). While all of the Asteraceae florets es- NoDerivatives License 4.0 (CC BY-NC-ND). sentially share this basic floral plan, tremendous floral diversity has Data deposition: Raw sequencing reads were deposited in the National Center for Bio- arisen from marked differences in corolla size, degree of petal fusion, technology Information (NCBI) Sequence Read Archive and Genbank under BioProject symmetry, and color. The most obvious floral feature of the family is PRJNA540287. The resulting alignments and phylogenetic trees were deposited in its developmentally complex, head-like inflorescence, the capitulum, FigShare at https://doi.org/10.6084/m9.figshare.7697834 and https://doi.org/10.6084/m9. which has a compound receptacle to which many tightly packed florets figshare.7695929. are attached. This is exemplified by the iconic North American sun- 1To whom correspondence may be addressed. Email: [email protected]. flower that mimics a single flower for pollinator attraction (Fig. 1I). This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. The sunflower family is morphologically distinct from its sister 1073/pnas.1903871116/-/DCSupplemental. family and its monophyly has never been disputed; however, using Published online June 17, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1903871116 PNAS | July 9, 2019 | vol. 116 | no. 28 | 14083–14088 Downloaded by guest on September 28, 2021 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, Fig. 1. Floral diversity of tribes. (A) Barnadesieae; (B) Famatinantheae; (C) 13 tribes), maximal support was recovered for
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