Molecular Phylogenetics and Evolution 142 (2020) 106659 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Accelerated diversification correlated with functional traits shapes extant T diversity of the early divergent angiosperm family Annonaceae B. Xuea,b,c,1, X. Guob,d,1, J.B. Landise, M. Sunf,g, C.C. Tangb, P.S. Soltisf,h,i, D.E. Soltisf,g,h,i, ⁎ R.M.K. Saundersb, a College of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, Guangdong, China b Division of Ecology & Biodiversity, School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Hong Kong, China c Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, Guangdong, China d Current address: State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Beishan Industrial Zone, Shenzhen, China e Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA 92521, USA f Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA g Department of Biology, University of Florida, Gainesville, FL 32611, USA h Genetics Institute, University of Florida, Gainesville, FL 32610, USA i Biodiversity Institute, University of Florida, Gainesville, FL 32611, USA ARTICLE INFO ABSTRACT Keywords: A major goal of phylogenetic systematics is to understand both the patterns of diversification and the processes Diversification rates by which these patterns are formed. Few studies have focused on the ancient, species-rich Magnoliales clade and Traits its diversification pattern. Within Magnoliales, the pantropically distributed Annonaceae are by far themost Annonaceae genus-rich and species-rich family-level clade, with c. 110 genera and c. 2,400 species. We investigated the Liana diversification patterns across Annonaceae and identified traits that show varied associations with diversifica- Pollination trap tion rates using a time-calibrated phylogeny of 835 species (34.6% sampling) and 11,211 aligned bases from Seed dispersal eight regions of the plastid genome (rbcL, matK, ndhF, psbA-trnH, trnL-F, atpB-rbcL, trnS-G, and ycf1). Twelve rate shifts were identified using BAMM: in Annona, Artabotrys, Asimina, Drepananthus, Duguetia, Goniothalamus, Guatteria, Uvaria, Xylopia, the tribes Miliuseae and Malmeeae, and the Desmos-Dasymaschalon-Friesodielsia- Monanthotaxis clade. TurboMEDUSA and method-of-moments estimator analyses showed largely congruent re- sults. A positive relationship between species richness and diversification rate is revealed using PGLS. Our results show that the high species richness in Annonaceae is likely the result of recent increased diversification rather than the steady accumulation of species via the ‘museum model’. We further explore the possible role of selected traits (habit, pollinator trapping, floral sex expression, pollen dispersal unit, anther septation, and seed dispersal unit) in shaping diversification patterns, based on inferences of BiSSE, MuSSE, HiSSE, and FiSSE analyses. Our results suggest that the liana habit, the presence of circadian pollinator trapping, androdioecy, and the dispersal of seeds as single-seeded monocarp fragments are closely correlated with higher diversification rates; pollen aggregation and anther septation, in contrast, are associated with lower diversification rates. 1. Introduction time for richness to accumulate, whereas the diversification rate hy- pothesis suggests that clades can undergo speciation at different rates, The asymmetry of species richness is a conspicuous ecological and with high net diversification rates generating greater species diversity evolutionary phenomenon in the Tree of Life. Differences in species irrespective of clade age. Accelerated diversification might be linked to richness among clades have been alternatively explained by the ‘mu- changes in a diversity of traits, such as genomic features, ecology, and/ seum model’ and diversification rate hypotheses (Scholl and Wiens, or morphology (Wiens, 2017, and references therein). 2016; Wiens, 2017): according to the former hypothesis, species di- Although the likely drivers of rapid species radiation have been versity is associated with clade age, with older clades having a longer widely investigated in lineages of eudicots (e.g., Ericaceae: Schwery ⁎ Corresponding author. E-mail address: [email protected] (R.M.K. Saunders). 1 Contributed equally. https://doi.org/10.1016/j.ympev.2019.106659 Received 30 July 2019; Received in revised form 4 October 2019; Accepted 17 October 2019 Available online 19 October 2019 1055-7903/ © 2019 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). B. Xue, et al. Molecular Phylogenetics and Evolution 142 (2020) 106659 et al., 2015; Campanulaceae: Lagomarsino et al., 2016; Proteaceae: Neupane et al., 2017; Roalson and Roberts, 2016), floral traits Onstein et al., 2016; Plantaginaceae: Fernández‐Mazuecos et al., 2019) (Fernández‐Mazuecos et al., 2019; Lagomarsino et al., 2017; Landis and monocots (e.g., Bromeliaceae: Givnish et al., 2014; Arecaceae: et al., 2018; O’Meara et al., 2016; Roalson and Roberts, 2016) and fruit Onstein et al., 2017; Orchidaceae: Pérez‐Escobar et al., 2017; Vello- type (Areces-Berazain and Ackerman, 2017; Beaulieu and Donoghue, ziaceae: Alcantara et al., 2018), diversification patterns in more ancient 2013; Lu et al., 2019; Marcussen and Meseguer, 2017; Onstein et al., angiosperm clades are poorly understood. Within the magnoliid order 2017). We therefore restricted our hypothesis testing to habit and floral Magnoliales, for example, the species-rich family Annonaceae (Guo and fruit traits that are shown here to be strongly correlated with rate et al., 2017a) provides a stark contrast with its sister family, Eu- shifts in Annonaceae. pomatiaceae, which comprises only three species (Jessup, 2002). An- We constructed a phylogeny of 835 Annonaceae species, re- nonaceae are by far the most genus-rich and species-rich family-level presenting the most complete species- and genus-level coverage to date clade in Magnoliales, with c. 110 genera and c. 2400 species (Chatrou (34.6% of species, 98% of genera) and performed lineage diversifica- et al., 2012, 2018; Guo et al., 2017a). Four subfamilies are recognized tion analyses based on this phylogeny using multiple methods, in- in Annonaceae: Anaxagoreoideae (30 spp.) and Ambavioideae (56 spp.) cluding Bayesian Analysis of Macroevolutionary Mixtures (BAMM), are the subsequent sisters to the rest of the family, while most species Modeling Evolutionary Diversification Using Stepwise Akaike are placed in two larger subfamilies, Annonoideae (1515 spp.) and Information Criterion (turboMEDUSA), and method-of-moments esti- Malmeoideae (783 spp.) (Chatrou et al., 2012; Chatrou et al., 2018; Guo mator, to assess patterns of rate variation in Annonaceae. We also et al., 2017a). The family is further subdivided into 15 tribes (Chatrou performed phylogeny-based trait evolution and trait-dependent di- et al., 2012; Guo et al., 2017a). Annonaceae have a pantropical dis- versification analyses to test the influence of morphology on species tribution and are an important ecological component of many lowland diversification patterns across Annonaceae. We specifically address the tropical forest ecosystems (Couvreur et al., 2011; Richardson et al., following questions: (1) Is species richness in Annonaceae better ex- 2004). The family is also well-studied taxonomically and phylogeneti- plained by the clade age or diversification rate hypothesis? (2) Are cally. Hence, Annonaceae is an ideal model system for studying the significant diversification rate shifts evident in Annonaceae? (3)Are causes of asymmetry in species richness, providing an additional case some traits strongly correlated with shifts in diversification rates, and outside monocots and eudicots. what are the possible explanations? Two previous studies focused on diversification patterns within Annonaceae. Couvreur et al. (2011) investigated diversification rates in 2. Materials and methods the family by applying lineage-through-time plots and a maximum likelihood approach based on a 100-taxon phylogeny (83% generic 2.1. Taxon and DNA region sampling sampling). They demonstrated that the family as a whole has under- gone relatively constant, slow diversification with low extinction rates, We adopted a super-matrix approach, using the recently published although this may be an artefact of taxon sampling limitations phylogeny by Guo et al. (2017a), supplemented with additional se- (Magallón et al., 2018). Erkens et al. (2012) subsequently used topo- quences from other sources (Chaowasku et al., 2018; Guo et al., 2017b; logical and temporal methods of diversification analysis to identify Ortiz-Rodriguez et al., 2016; Stull et al., 2017; Thomas et al., 2015; Xue clades that were likely to have undergone radiation, based on one of the et al., 2012, 2014, 2016, 2017, 2018). Eight regions of the plastid 200-taxon trees (83% generic sampling) generated by Chatrou et al. genome that are commonly used in Annonaceae phylogenetics (rbcL, (2012). The topological methods identified three shifts to increased matK, ndhF, psbA-trnH, trnL-F, atpB-rbcL, trnS-G and ycf1) were down- rates: in the Annoneae-Monodoreae-Uvarieae and Miliuseae-Mono-