Evolution of Angiosperm Pollen. 7. Nitrogen-Fixing Clade1

Authors: Jiang, Wei, He, Hua-Jie, Lu, Lu, Burgess, Kevin S., Wang, Hong, et. al. Source: Annals of the Missouri Botanical Garden, 104(2) : 171-229 Published By: Missouri Botanical Garden Press URL: https://doi.org/10.3417/2019337

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EVOLUTION OF ANGIOSPERM Wei Jiang,2,3,7 Hua-Jie He,4,7 Lu Lu,2,5 POLLEN. 7. NITROGEN-FIXING Kevin S. Burgess,6 Hong Wang,2* and 2,4 CLADE1 De-Zhu Li *

ABSTRACT Nitrogen-fixing symbiosis in root nodules is known in only 10 families, which are distributed among a clade of four orders and delimited as the nitrogen-fixing clade. As the seventh in a series that examines pollen morphological distribution and evolution in the angiosperms, this paper focuses on pollen morphological character states of the nitrogen-fixing clade. To illustrate the palynological diversity of the clade, we first examined pollen grains from 26 species with light electron, scanning electron, and transmission electron microscopy. Second, we used a reduced data matrix from Li et al. (2015) to reconstruct a maximum likelihood tree and then optimized 18 pollen character states onto the tree using Fitch parsimony, maximum likelihood, and hierarchical Bayesian inference. Finally, 12 plesiomorphic states for the nitrogen-fixing clade were inferred unambiguously under all methods, and more than 40 clades (or lineages) at or above familial level were characterized by unambiguous pollen character state changes in at least one of the optimizations. We found a number of evolutionary trends for changes in pollen character states. These include increasing grain size, increasing aperture number accompanied by concomitant changes in aperture position (from equatorial to global) and aperture shape (from colpate to colporate), and increasing complexity of tectum ornamentation. There was a strong correlation between some pollen characters (prolate shape class, lobe outline in polar view, colpate ectoaperture, lalongate and lolongate endoaperture, absent supratectal element, reticulate tectum) and insect pollination, while other pollen characters—simple aperture structure, porate ectoaperture, circular endoaperture, present and gemmate or echinate supratectal element, and

1 We thank Dr. Alexandra H. Wortley and Prof. Stephen Blackmore from Royal Botanic Garden Edinburgh for their kind help with earlier versions of the manuscript, Dr. Z. X. Ren for collecting pollen samples and helping with pollen observations under SEM, and Dr. M. Y. Zhang for her suggestions on data analysis. We are also grateful to Kunming Institute of Botany Herbarium (KUN), Royal Botanic Garden Edinburgh Herbarium (E), Australian National Herbarium (CANB), and Xishuangbanna Tropical Botanical Garden Herbarium (XTBG) for providing pollen samples. This study was supported by grants from the Major International Joint Research Project of the National Natural Science Foundation of China (no. 31320103919), National Natural Science Foundation of China (no. 31270272), and the Keynote Project of National Natural Science Foundation of China (no. 40830209). 2 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, CAS, Kunming 650201, People’s Republic of China. 3 The Industrial Crops Research Institute, Yunnan Academy of Agricultural Sciences, Kunming, 650200, People’s Republic of China. 4 Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species, Kunming Institute of Botany, CAS, Kunming 650201, People’s Republic of China. 5 School of Pharmaceutical Sciences and Yunnan Key Laboratory of Pharmacology for Natural Products, Kunming Medical University, Kunming, 650500, People’s Republic of China. 6 Department of Biology, College of Letters & Sciences, Columbus State University, University System of Georgia, Columbus, Georgia 31907, U.S.A. 7 These authors contributed equally to this work. * Authors for correspondence: [email protected]; [email protected]

VERSION OF RECORD FIRST PUBLISHED ONLINE ON 11 JUNE 2019 AHEAD OF SUMMER 2019 ISSUE. – Downloaded From:doi: https://bioone.org/journals/Annals-of-the-Missouri-Botanical-Garden 10.3417/2019337 ANN on.M 01 AprISSOURI 2020 BOT.GARD. 104: 171 229. Terms of Use: https://bioone.org/terms-of-use Access provided by Kunming Institute of Botany, CAS 172 Annals of the Missouri Botanical Garden

imperforate tectum—were strongly correlated with wind pollination. In addition, rugulate tectum was significantly correlated with shrub habit while larger pollen size was significantly correlated with vine habit; the helophytic habitat was significantly correlated with having two apertures. Our study provides rich evidence for the phylogenetic significance of pollen morphological diversity in the nitrogen-fixing clade. Key words: Character evolution, Cucurbitales, Fabales, Fagales, nitrogen-fixing clade, pollen morphology, Rosales, systematic significance.

This study, the seventh in a series investigating Within Rosales, the families Rhamnaceae, Elaeag- pollen character state distribution and evolution across naceae, Barbeyaceae, and Dirachmaceae seem to form the angiosperms in a phylogenetic context, examines the a clade, but relationships within the clade remain diversity of pollen character states in the nitrogen-fixing unresolved. Although a close relationship between clade (Fig. 1). The nitrogen-fixing clade lies within the Rhamnaceae and Elaeagnaceae was reconstructed, the rosids, and the clade is commonly divided into four finding may be due to a lack of sampling for the other two orders: Cucurbitales, Fabales, Fagales, and Rosales families (Wang et al., 2009; Soltis et al., 2011). Some (Soltis et al., 1995), together comprising 28 families, studies have placed the Rhamnaceae as basally branch- approximately 1170 genera, and more than 30,000 ing, with Dirachmaceae and Barbeyaceae forming species (Magallon et al., 1999; Soltis et al., 2005; a clade with Elaeagnaceae (Zhang et al., 2011), while APG IV, 2016). The nitrogen-fixing clade exhibits other studies place Barbeyaceae and Elaeagnaceae enormous heterogeneity in habit, habitat, and life form as weakly supported sister groups, together forming (Soltis et al., 2005), but its most noticeable character- a clade with Rhamnaceae, but Dirachmaceae is the istic is the high number of rhizobial and actinorhizal basal branch (Xiang et al., 2014; Li et al., 2015; Sun plants bearing root nodules that contain nitrogen-fixing et al., 2016). Similarly, relationships within Cucurbi- bacteria, which give these taxa a competitive advantage tales remain unclear except for a firm sister group in nutrient-deficient soils (Soltis et al., 1995; Biswas & relationship between Coriariaceae and Corynocarpa- Gresshoff, 2014; Mus et al., 2016). The clade contains ceae. A clade comprising Datiscaceae and Begoniaceae many economically important families including le- receives at best only moderate support (Zhang et al., gumes (Fabaceae), gourds (Cucurbitaceae), fruit crops 2006; Schaefer et al., 2009; Schaefer & Renner, (Rosaceae), and temperate and tropical forest trees 2011b), and a possible relationship between Tetrame- (e.g., Betulaceae, Cannabaceae, Fabaceae, Fagaceae, laceae and Datiscaceae has also been recovered by and Ulmaceae; Wang et al., 2009). Swensen et al. (1994), Li et al. (2015), and Sun et al. Most previous studies agree on both the composition (2016). In contrast to the lack of family resolution within of the nitrogen-fixing clade and the relationships among the other three orders within this clade, relationships its four orders, with Fabales being the most basally within Fagales are well resolved except for the position branching, Rosales the next diverging, and Fagales and of Myricaceae, which has been placed as sister group to Cucurbitales forming sister groups (Wang et al., 2009; Casuarinaceae–(Ticodendraceae–Betulaceae) (Sauquet Soltis et al., 2011; Li et al., 2015; Sun et al., 2016). et al., 2012; Xiang et al., 2014; Xing et al., 2014; Deep relationships within orders, however, remain Li et al., 2015; Sun et al., 2016), or to Juglandaceae poorly understood (APG I, 1998; APG II, 2003; (Li et al., 2004, 2016; Larson-Johnson, 2016). APG III, 2009; APG IV, 2016); in particular, the The potential of palynological characters to sup- resolution of several families remains ambiguous. port systematic classifications has been discussed by For example, the relationships between the four Blackmore (2000). Several studies have highlighted families placed in Fabales (Fabaceae, Polygalaceae, the taxonomic significance of pollen characters in the Quillajaceae, and Surianaceae) remain unclear nitrogen-fixing clade (Page & Jeffrey, 1975; Zhang & (Stevens, 2001 onward). A sister group relationship Lu, 1989; Huang et al., 1997; Zhu, 2005; Welsh et al., of Quillajaceae and Fabaceae has been recovered with 2010; X.-L. Zhao et al., 2016). For example, a palyno- weak support in a few studies (Persson, 2001; Cannon logical study of Juglandaceae and Rhoipteleaceae using et al., 2015), while an alternative sister group relation- transmission electron microscopy (TEM) and SEM ship between Surianaceae and Quillajaceae has been showed that the exine of pollen grains for the two frequently recovered but not strongly supported families are very similar in morphology (Stone & (Wojciechowski et al., 2004; Mercure et al., 2008; Bello Broome, 1971), supporting the sinking of Rhoiptelea- et al., 2009, 2012; Li et al., 2015, 2016; Sun et al., ceae into Juglandaceae, which is treated by recent APG 2016). In addition, the positions of Polygalaceae and classifications (APG III, 2009; APG IV, 2016). Close Fabaceae are poorly resolved (Wang et al., 2009; Soltis relationships among other families based on molecular et al., 2011). data (Zhang et al., 2011), such as between Cannabaceae,

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Figure 1. Phylogenetic framework for angiosperms, divided into groups following Wortley et al. (2015). Highlighted taxa indicate the nitrogen-fixing clade.

Moraceae, and Urticaceae, have also been well sup- For example, Ferguson and Skvarla (1983) found that ported by a number of pollen character states (Punt & granular infratectum structure evolves from simple to Malotaux, 1984). Further, pollen morphology has been complex in the subfamily Papilionoideae (Legumino- used to classify genera within the nitrogen-fixing clade. sae). In addition, the tribe Hedysareae (Papilionoideae) Scyphosyce Baill., a small genus in the Moraceae, has shows evolutionary shifts in tectum sculpture (perforate been classified in the tribe Dorstenieae due to its pollen to reticulate), shape (subprolate to prolate), and size similarity to Dorstenia L. (both have a thin exine with (small to larger) (Choi & Ohashi, 1996). Similarly, distinct stratification, and a tectum beset with very small tectum sculpture in the Rhamnaceae has been shown granules [Punt, 1978] as well as having pollen that are to evolve by successive fusion and flattening of the unusually poly-pantoporate with the pores often placed supratectal elements. Schirarend and Koehler (1993) on top of an aspis), although to date, their affinity has not and Khunwasi (1998) have summarized 16 trends of been verified by phylogenetic analysis. pollen character evolution in Cucurbitaceae, including The enormous variability in the pollen morphology of colpate to colporate, zonoaperturate to pantoaperturate, the flowering plants can also reveal historical evolu- and tectum psilate to perforate and then reticulate. tionary patterns within the angiosperms (Lu et al., 2015; However, the evolutionary patterns of pollen in many Luo et al., 2015; M.-Y. Zhang et al., 2017; Yu et al., other groups (e.g., Rosaceae, Anisophylleaceae, and 2018). The evolutionary trends of pollen grains in the Cannabaceae) within the nitrogen-fixing clade remain nitrogen-fixing clade have not been discussed since this poorly understood. What is needed is an extensive clade was defined in the APG classification systems sampling of pollen data across the clade to prompt (APG I, 1998; APG II, 2003; APG III, 2009; APG IV, future investigations into the overall trends of pollen 2016). However, a few studies have inferred pollen evolution in the nitrogen-fixing angiosperms. evolutionary trends within families, especially those Using Fitch parsimony (FP), maximum likelihood of high diversity in both species and pollen morphology, (ML), and hierarchical Bayesian (HB) inference, we such as Fabaceae, Rhamnaceae, and Cucurbitaceae. optimized the states of 18 pollen characters of the

nitrogen-fixing clade. Moving on from the basal angio- observed under TEM (JEOL JEM-1011; JEOL, Inc., sperms (Lu et al., 2015), monocots (Luo et al., 2015), Peabody, Massachusetts, U.S.A.). basal eudicots (M.-Y. Zhang et al., 2017), and the early diverging Superasteridae (Yu et al., 2018), we now focus PHYLOGENETIC ANALYSIS on the pollen diversity of the nitrogen-fixing clade. To cover a broad phylogenetic and palynological Through expansive pollen data collection based on range of taxa, we generated a maximum likelihood a densely sampled tree, we infer pollen character state (ML) tree derived from the most recent comprehensive transitions and diagnostic states, and assess their sys- phylogenetic analysis of the nitrogen-fixing clade (Li tematic significance, particularly for unresolved phylo- et al., 2015) based on data for 1008 genera for three genetic issues, such as relationships within Fabales, the plastid loci (rbcL, matK, and trnL-F). Of these 1008 position of Myricaceae, the relationships of Rhamna- genera, we selected 307 genera according to their ceae, Elaeagnaceae, Dirachmaceae, and Barbeyaceae, phylogenetic positions and typical pollen characters. and relationships within Cucurbitales excluding Cor- The new dataset therefore included 313 genera repre- ynocarpaceae and Coriariaceae. We infer possible ple- senting all families of the nitrogen-fixing clade and six siomorphic pollen morphology of the nitrogen-fixing outgroups: Crossosomataceae, Zygophyllaceae, Melian- clade, and examine possible evolutionary patterns for thaceae, Oxalidaceae, Ranunculaceae, and Lepidobo- selected pollen characters in the context of a phyloge- tryaceae. The Apodanthaceae were not included in this netic tree based on ML. dataset because plastid loci were unavailable in this holoparasite family. GenBank accession numbers are MATERIALS AND METHODS listed in Appendix 2; taxonomic treatment follows Li et al. (2015). Using ModelTest v3.7, the GTR 1 I 1 G OBSERVATIONS ON REPRESENTATIVE POLLEN GRAINS model was selected as the best fit for each region We selected pollen samples from 26 species distrib- (Posada & Crandall, 1998). ML analysis was performed uted across 26 genera (17 families) in all four orders of in RAxML v8.0.1 (Stamatakis, 2006), utilizing CIPRES; the nitrogen-fixing clade. Fresh anthers were collected 1000 non-parametric bootstrap replicates were exe- from Xishuangbanna Tropical Botanic Garden (XTBG), cuted to assess uncertainty in the topology and branch and dry samples from the Kunming Institute of Botany length estimation. Herbarium (KUN), the Royal Botanic Garden Edin- burgh Herbarium (E), and the Australian National POLLEN DATA COLLECTION Herbarium (CANBR) (see Appendix 1 for voucher in- Pollen morphological data for 313 genera were formation). We used a combination of LM, SEM, and recorded from the literature (mostly SEM and TEM transmission electron microscope (TEM) to observe the data), websites, and our own observations. Literature pollen grains. Most pollen grains were prepared follow- sources are presented in Appendix 3. Eighteen pollen ing a modified acetolysis method after Erdtman (1952). characters were scored (see Table 1). Character coding Pollen grains with a very thin, fragile exine (e.g., Pilea mainly follows the criteria in Wortley et al., 2015, verrucosa Killip, Ficus tikoua Bureau, Nothofagus incorporating comprehensive and democratic coding dombeyi (Mirb.) Oerst., Alnus nepalensis D. Don., and strategies (see Appendices 4 and 5). Palynological Mimosa pudica L.) were directly dehydrated through features were coded as unordered, binary, or multistate five concentrations of ethanol (50%, 65%, 75%, 85%, characters, with inapplicable states coded as an extra and 95%). For TEM, anthers were embedded in 5% agar numbered state and missing data coded as “?”. and then fixed with 2% glutaraldehyde at pH 7.4,

buffered with 0.05 mol/L sodium cacodylate. Samples ANALYSES OF CHARACTER EVOLUTION were then dehydrated in a graded ethanol series and block stained with 1% phosphotungstic acid (PTA) in The 18 pollen characters for 313 genera were opti- 100% ethanol before embedding in LR white resin. mized on the reconstructed phylogenetic tree using Finally, ultra-thin (670-nm) sections were stained with three methods of inference: Fitch parsimony (FP, which uranyl acetate and lead citrate in an LKB 2168 Ultro- specifies character states as unordered and equally stainer (LKB-Produkter, AB, Bromma, Sweden). The weighted and minimizes the number of character state average pollen sizes (taken as the maximum diameter of changes [Fitch, 1971; Cunningham et al., 1998]), ML single grains at the equatorial or longitudinal axis) of 20 (which uses an explicit model of character evolution to pollen grains were measured under LM. Samples were estimate the probabilities of all possible character state examined using a Hitachi S-4800 SEM (Hitachi, Ltd., reconstructions at every node on the tree [Cunningham Tokyo, Japan) at 10.0 KV (Kunming Institute of Botany, et al., 1998]), and hierarchical Bayesian (HB, which KIB). Pollen wall structure from 25 species was further uses Markov chain Monte Carlo [MCMC] modeling to

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Table 1. The 18 pollen characters and three ecological traits and their states as defined in the two matrices in this study.

Character Character states 1. Dispersal unit C, D: 0, monads; 1, tetrads; 2, polyads 2. Polarity C, D: 0, apolar; 1, heteropolar; 2, isopolar 3. Symmetry (in polar view) C, D: 0, bilateral; 1, radial 4. Shape class C, D: 0, oblate (P/E 0.5–0.75); 1, subspheroidal (P/E 0.75–1.33); 2, prolate (P/E 1.33–2); 3, perprolate (P/E . 2) 5. Outline in polar view (amb) C, D: 0, polygonal; 1, circular; 2, lobed; 3, elliptic 6. Size (diameter of largest axis) C, D: 0, very small (, 10 mm); 1, small (10–24 mm); 2, medium (25–49 mm); 3, large (50–99 mm); 4, very large (100–199 mm) 7. Aperture number C, D: 0, one; 1, two; 2, three; 3, more than three 8. Aperture position C, D: 0, equatorial; 1, global 9. Aperture structure C, D: 0, simple; 1, compound 10. Ectoaperture shape C, D: 0, colpate; 1, porate 11. Endoaperture shape C, D: 0, circular; 1, endocingulate; 2, lalongate; 3, lolongate; 4, inapplicable data 12. Aperture membrane ornamentation C, D: 0, granulate; 1, smooth 13. Operculum C, D: 0, absent; 1, present 14. Supratectal element C, D: 0, absent; 1, present 15. Supratectal element shape C, D: 0, gemmate (including verrucate); 1, echinate; 2, rugulate; 3, striate; 4, inapplicable data 16. Tectum sculpture C, D: 0, imperforate; 1, perforate; 2, foveolate/fossulate; 3, rugulate; 4, reticulate (including striato-reticulate); 5, striate; 6, intectate; 7, areolate 17. Infratectum structure C, D: 0, columellate; 1, granulate 18. Foot layer C, D: 0, absent; 1, present 19. Pollination type C, D: 0, self-pollination; 1, wind pollination; 2, water pollination; 3, insect pollination; 4, other animal pollination 20. Habitat moisture C, D: 0, xerophytic (adapted to arid and low water availability soils); 1, mesophytic (adapted to soils of moderate moisture content); 2, helophytic (adapted to wet but marshy habitats); 3, hydrophytic (adapted to aquatic environments) 21. Plant growth form C, D: 0, herbaceous; 1, shrub; 2, vine; 3, arborescent

C, Comprehensive method of coding; D, democratic method of coding; P/E, polar and equatorial axes.

calculate the relative probability for each possible analyses, the state with the highest likelihood or prob- character state at each node on a set of trees sampled ability at each node was taken to be the state inferred for from a distribution [Huelsenbeck & Bollback, 2001]). this node. Pollen character state change along a branch Data coded using the comprehensive strategy (including was identified if the states (FP) or the states with the polymorphic states) were reconstructed using FP and highest probability (proportional likelihood, ML, and HB inference (hereafter abbreviated as CFP and CHB, HB) at above and below nodes were different. To detect respectively; ML analysis in Mesquite was not appli- the topology from Li et al. (2015) with the minimum cable to data with polymorphic states). Data coded using number of steps, the parsimony step number among the democratic strategy (removing polymorphic states by different topologies based on maximum parsimony coding for the most common state) were reconstructed under all three methods (hereafter abbreviated as DFP, method (Mesquite 3.2 [Maddison & Maddison, 2017]) DML, and DHB). Fitch parsimony and ML (using the was calculated. We summarized the alternative topolo- one-parameter Markov [Mk-1] model) optimizations were gies within the Fabales phylogeny from Persson (2001) conducted with Mesquite 3.2 (Maddison & Maddison, and Bello et al. (2009), the alternative topologies 2017). HB inference was implemented using BayesTraits within the Rosales phylogeny from Zhang et al. (2011) 3.0 (available from ,http://www.evolution.rdg.ac.uk/.). and Soltis et al. (2011), the alternative topologies within For CHB and DHB analyses, parameters were set as the phylogenetic tree of Cucurbitales from Zhang et al. follows: rate variations ranging from 2 to 100 across the (2006) and Schaefer and Renner (2011b), and the 18 characters, sampling frequency from 300 to 800 alternatve topologies within conflicting phylogenetic generations; and a burn-in of 10,000 generations, for relationships of Fagales from Li et al. (2002) and a total of 5,000,000 generations. For ML and HB Li et al. (2004).

TESTS OF CORRELATED EVOLUTION medium, P ranged from 36.2 to 53.5 mm (mean 41.5 mm), E ranged from 42.6 to 52.8 mm (mean BayesDiscrete tests for correlated evolution between 46.5 mm); grains tricolporate, apertures compound, the palynological characters and ecological data were equatorial, with granulate membranes, endoapertures conducted for 767 pair-wise comparisons, using two ML lolongate, operculum absent; tectum reticulate with models: an independent model (I) and a dependent pili visible in the lumina, supratectal elements ab- model (D). A likelihood score representing goodness sent; infratectum structure columellate; foot layer of fit was calculated for the two models. The likelihood present. ratio (LR) was determined by LR 5 2*(likelihood [D] – Mimosa pudica L. (Fabales, Fabaceae, Fig. 3A–D). likelihood [I]) and was tested against a x2 distribution Pollen grains dispersed as tetrads; diameter of polyads with four degrees of freedom (following Pagel, 1994). 8.5–16 mm, oblate; grains heteropolar, pollen size small Finally, if pair-wise comparisons were significant, they (ca. 5.5–8.5 mm for single-pollen grains); grains tripo- were subsequently analyzed using the MCMC method rate, apertures compound, aperture membranes smooth, under the Discrete option in BayesTraits 3.0. A total endoapertures circular; tectum rugulate or areolate, of 5,000,000 generations with a burn-in period of supratectal elements absent; infratectum structure gran- 50,000 generations, and a sampling frequency of 500 ulate; foot layer and endexine present. generations, was used for both the dependent and in- Polygala arillata Buch.-Ham. ex D. Don (Fabales, dependent models: these were based on a reversible Polygalaceae, Fig. 3E–H). Pollen dispersed as monads; jump hyperior model, exponential prior distribution, grains isopolar, radially symmetrical, oblate, amb circular; and rate variations ranging from 3 to 10. The difference size medium, P ranged from 42.5 to 53 mm(mean in harmonic means of the log likelihoods between the 42.5 mm), E ranged from 35.2 to 41.6 mm (mean two models was calculated twice. The log Bayes factor 38.5 mm); grains zonocolporate, 14 apertures, aper- value (log BF) was calculated to indicate the degree of tures compound, equatorial, with granulate membranes, evolutionary correlation between two characters: values endoapertures endocingulate, operculum absent; tectum of two to five represented a positive correlation, values fossulate, supratectal elements absent; infratectum struc- greater than five a strong correlation, and a value greater ture generally columellate, becoming granulate in aper- than 10 represented a very strong correlation (Pagel & tural regions; foot layer absent. Meade, 2006). Shepherdia canadensis (L.) Nutt. (Rosales, Elaeagna- ceae, Fig. 3I–L). Pollen dispersed as monads; grains RESULTS isopolar, radially symmetrical, prolate, amb lobate; pollen size medium, P ranged from 29.8 to 39.6 mm NEW PALYNOLOGICAL OBSERVATIONS (35.7 mm), E ranged from 20.9 to 28.6 mm (mean Acacia concinna (Willd.) DC. (Fabales, Fabaceae, 23.4 mm); grains tricolporate, apertures compound, Fig. 2A–D). Pollen grains dispersed as polyads com- equatorial, with granulate membranes, endoapertures prising 16 pollen grains; diameter of polyads 42.5–49.5 circular, operculum absent; tectum perforate, supra- mm, oblate; grains heteropolar, pollen size small (ca. tectal elements present, verrucate; infratectum structure 12.5–15.5 mm for single pollen grains); grains triporate, columellate; foot layer absent. apertures simple, aperture membranes granular, no Pilea verrucosa Killip (Rosales, Urticaceae, Fig. 4A, B). endoapertures; tectum foveolate, supratectal elements Pollen dispersed as monads; grains isopolar, bilaterally absent; infratectum structure granulate; foot layer and symmetrical, prolate, amb circular; pollen size small, P endexine present. ranged from 13.2 to 19.6 mm (mean 16.7 mm), E ranged Bauhinia brachycarpa Wall.exBenth.(Fabales, from 11.5 to 15.6 mm (mean 12.4 mm); grains 2-porate, Fabaceae, Fig. 2E–H). Pollen dispersed as monads; apertures simple, equatorial, with granulate membranes, grains isopolar, radially symmetrical, oblate to sub- operculum present; tectum perforate, supratectal ele- spheroidal, amb circular; pollen size medium, length ments present, echinate; infratectum structure granulate; of polar view (P) ranged from 42.5 to 53 mm (mean foot layer not visible. 46.5 mm), length of equatorial view (E) ranged from 40.2 Ficus tikoua Bureau (Rosales, Moraceae, Fig. 4C, D). to 52.6 mm (mean 43.5 mm); grains tricolporate, aper- Pollen dispersed as monads; grains isopolar, bilaterally tures compound, equatorial, with granulate membranes, symmetrical, oblate, amb elliptic; pollen size small, P endoapertures circular, operculum absent; tectum ranged from 7.2 to 9.6 mm (mean 8.7 mm), E ranged striato-reticulate, supratectal elements absent; infratec- from 10.9 to 15.6 mm (mean 12.4 mm); grains 2-porate, tum structure columellate; foot layer present. apertures simple, equatorial, with granulate mem- Caesalpinia minax Hance (Fabales, Fabaceae, Fig. branes, operculum absent; tectum rugulate, supratectal 2I–L). Pollen dispersed as monads; grains isopolar, elements absent; infratectum columellate; foot layer radially symmetrical, subspheroidal, amb lobate; size present.

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Figure 2. SEM and transmission electron micrographs (TEM) of pollen from the nitrogen-fixing clade, arranged alphabetically. A–D. Acacia concinna (Willd.) DC. —A. Polar view, showing polyads. —B. Equatorial view. —C. Showing exine surface. —D. Mesocolpial exine showing tectum (T), granular infratectum structure (G), foot layer (F), and thin endexine (E; TEM). E–H. Bauhinia brachycarpa Wall. ex Benth. —E. Polar view (SEM), showing monad, oblate, monoporate pollen grain, 3-colporate. —F. Equatorial view, showing aperture membrane ornamentation granulate. —G. Exine surface, showing tectum striato- reticulate. —H. Mesocolpial and mesoaperturate exines, the former showing tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; TEM). I–L. Caesalpinia minax Hance. —I. Distal polar view (SEM), showing monad, lobate, monoporate pollen grain, 3-colporate. —J. Equatorial view, showing tectum reticulate. —K. Showing endoaperture lolongate (arrowed), aperture membrane ornamentation granulate. —L. Mesocolpial exine showing tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; TEM).

Nothofagus dombeyi (Mirb.) Oerst. (Fagales, Notho- endoapertures lalongate, operculum absent; tectum fagaceae, Fig. 4E–H). Pollen dispersed as monads; rugulate, supratectal elements absent; infratectum grains isopolar, radially symmetrical, oblate, amb po- structure columellate; foot layer present. lygonal; pollen size medium, P ranged from 16.8 to Quercus augustinii Skan (Fagales, Fagaceae, Fig. 22.8 mm (mean 19.3 mm), E ranged from 25.2 to 5A–D). Pollen dispersed as monads; grains isopolar, 29.6 mm (mean 26.4 mm); grains 5- to 6-colpate, radially symmetrical, subspheroidal to prolate, amb apertures simple, equatorial, with smooth membrane, lobate; pollen size medium, P ranged from 33.5 to operculum absent; tectum imperforate, supratectal el- 46.6 mm(mean39.5mm), E ranged from 27.5 to ements present, microechinate; infratectum structure 44.8 mm (mean 35.6 mm); grains tricolporate, columellate; foot layer present. apertures compound, equatorial, with granulate Chrysolepis sempervirens (Kellogg) Hjelmq. (Fagales, membranes, endoapertures lalongate, operculum Fagaceae, Fig. 4I–L). Pollen dispersed as monads; absent; tectum fossulate, supratectal elements ab- grains isopolar, radially symmetrical, subspheroidal, sent; infratectum structure columellate; foot layer amb circular; pollen size small, P ranged from 9.8 present. to 19.8 mm (mean 13.3 mm), E ranged from 7.2 to 12.6 Allocasuarina diminuta L. A. S. Johnson (Fagales, mm (mean 9.4 mm); grains tricolporate, apertures Casuarinaceae, Fig. 5E–H). Pollen dispersed as mo- compound, equatorial, with granulate membranes, nads; grains isopolar, radially symmetrical, oblate, amb

Figure 3. SEM and transmission electron micrographs (TEM) of pollen from the nitrogen-fixing clade, continued. A–D. Mimosa pudica L. —A. Polar view, showing tetrads. —B. Equatorial view. —C. Showing exine surface. —D. Mesocolpial exine showing tectum (T), granular infratectum structure (G), foot layer (F), and thin endexine (E; TEM). E–H. Polygala arillata Buch.- Ham. ex D. Don (Fabales, Polygalaceae). —E. Polar view, showing monad, subspheroidal, monoporate pollen grain, 8- to 14- colporate. —F. Equatorial view. —G. Showing exine surface. —H. Mesocolpial and mesoaperturate exines, the former showing tectum (T), infratectum columellate (C), foot layer (F), and endexine (E); the latter (AP) showing thin foot layer and a little thickening of endexine (TEM). I–L. Shepherdia canadensis (L.) Nutt. —I. Polar view, showing monad, lobate, monoporate pollen grain, 3-colporate. —J. Equatorial view. —K. Exine surface. —L. Mesocolpial exine showing supratectal element (S) verrucate, tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; TEM).

circular; pollen size medium, P ranged from 20.3 to Myrica esculenta Buch.-Ham. ex D. Don (Fagales, 28.6 mm (mean 24.4 mm), E ranged from 28.8 to Myricaceae, Fig. 6A, B). Pollen dispersed as monads; 35.8 mm (mean 30.1 mm); grains triporate, apertures grains isopolar, radially symmetrical, oblate, amb po- simple, equatorial, with smooth membranes, operculum lygonal; pollen size medium, P ranged from 17.6 to absent; tectum imperforate, supratectal elements pres- 24.5 mm (mean 21.0 mm), E ranged from 22.5 to ent, microechinate; infratectum structure columellate; 32.5 mm (mean 26.5 mm); grains tripororate, apertures foot layer present. compound, equatorial, with granulate membranes, Alnus nepalensis D. Don (Fagales, Betulaceae, Fig. endoapertures circular, operculum absent; tectum im- 5I–L). Pollen dispersed as monads; grains isopolar, perforate, supratectal elements present, microechinate; radially symmetrical, oblate to subspheroidal, amb infratectum structure columellate; foot layer present. polygonal; pollen size medium, P ranged from 40.3 to Rhoiptelea chiliantha Diels & Hand.-Mazz. (Fagales, 44.5 mm (mean 43.5 mm), E ranged from 29.5 to Juglandaceae, Fig. 6C, D). Pollen dispersed as monads; 35.6 mm (mean 32.5 mm); grains (4- to)5-pororate, grains isopolar, radially symmetrical, oblate, amb po- apertures compound, equatorial, with granulate mem- lygonal; pollen size medium, P ranged from 19.1 to branes, endoapertures circular, operculum absent; tectum 28.3 mm (mean 23.4 mm), E ranged from 28.4 to rugulate, supratectal elements present, microechinate; 38.6 mm (mean 32.2 mm); grains tricolporate, apertures infratectum structure columellate, becoming granulate compound, equatorial, with granulate membranes, adjacent to the apertures; foot layer present. endoapertures circular, operculum present; tectum

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Figure 4. SEM and transmission electron micrographs (TEM) of pollen from the nitrogen-fixing clade, continued. A, B. Pilea verrucosa Killip. —A. Polar view, showing monad, subspheroidal, monoporate pollen grain, 2-porate (AP). —B. Equatorial view, showing tectum echinate. C, D. Ficus tikoua Bureau. —C. Equatorial view, showing monad, oblate, monoporate pollen grain, 2- porate. —D. Mesocolpial exine showing tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; TEM). E–H. Nothofagus dombeyi (Mirb.) Oerst. —E. Polar view, showing monad, oblate, monoporate pollen grain, 4- to 9-colpate. —F. Equatorial view. —G. Showing aperture and exine surface. —H. Mesocolpial and mesoaperturate exines, the former showing tectum (T), columellae (C), foot layer (F), and endexine (E), the latter (AP) showing foot layer and thickenings of endexine (TEM). I–L. Chrysolepis sempervirens (Kellogg) Hjelmq. —I. Polar view, showing monad, oblate, monoporate pollen grain, 3-colporate. —J. Equatorial view. —K. Exine surface. —L. Mesocolpial exine showing tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; TEM).

imperforate, supratectal elements present, microechi- 24.6 mm); grains tripororate, apertures compound, nate; infratectum structure generally columellate (some equatorial, with granulate membranes, endoapertures columellae reduced to granules); foot layer present. circular, operculum absent; tectum perforate and are- Juglans mandshurica Maxim. (Fagales, Juglanda- olate, supratectal elements present, microechinate; ceae, Fig. 6E–H). Pollen dispersed as monads; grains infratectum structure columellate; foot layer present. apolar, radially symmetrical, oblate, amb circular; pol- Corynocarpus laevigatus J. R. Forst. & G. Forst. len size medium, P ranged from 32.5 to 40.5 mm (mean (Cucurbitales, Corynocarpaceae, Fig. 7A–D). Pollen 35 mm), E ranged from 38 to 46 mm (mean 41 mm); dispersed as monads; grains weakly heteropolar, bi- grains 5- to 10-pororate, apertures compound, global, laterally symmetrical, prolate, amb elliptic; pollen size with granulate membranes, endoapertures circular, medium; P ranged from 22.9 to 27.3 mm (mean operculum absent; tectum imperforate, supratectal el- 25.3 mm), E ranged from 14.5 to 16.3 mm (mean ements present, microechinate; infratectum structure 15.6 mm); grains 2-colporate, apertures compound, granulate; foot layer present. equatorial, with granulate membranes, endoapertures Coriaria sinica Maxim. (Cucurbitales, Coriariaceae, lolongate, operculum absent; tectum rugulate, supra- Fig. 6I–L). Pollen dispersed as monads; grains isopolar, tectal elements absent; infratectum structure granulate; radially symmetrical, subspheroidal, amb circular; pol- foot layer present. len size medium, P ranged from 17.9 to 32.3 mm (mean Cucurbita pepo L. (Cucurbitales, Cucurbitaceae, Fig. 25.3 mm), E ranged from 17.9 to 32.3 mm (mean 7E–H). Pollen dispersed as monads; grains apolar,

Figure 5. SEM and transmission electron micrographs (TEM) of pollen from the nitrogen-fixing clade, continued. A–D. Quercus augustinii Skan. —A. Polar view (SEM), showing monad, lobate, monoporate pollen grain, 3-colporate. —B. Equatorial view. —C. Exine surface. —D. Mesocolpial exine showing gemmate supratectal element (S), tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; TEM). E–H. Allocasuarina diminuta L. A. S. Johnson. —E. Polar view, showing monad, oblate, monoporate pollen grain, 3-porate. —F. Equatorial view. —G. Showing aperture and exine surface. —H. Mesocolpial exine showing echinate supratectal element (S), tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; TEM). I–L. Alnus nepalensis D. Don. —I. Polar view, showing monad, oblate-subspheroidal, monoporate pollen grain, 4- to 5-porate. —J. Equatorial view. —K. Showing aperture and exine surface. —L. Mesocolpial and mesoaperturate exines, the former showing echinate supratectal element (S), tectum (T), columellae (C), foot layer (F), and endexine (E), the latter (AP) showing annulus vestibulate, foot layer, and thickenings of endexine (TEM).

radially symmetrical, subspheroidal, amb circular; pol- Lagenaria siceraria (Molina) Standl. (Cucurbitales, len size very large, P ranged from 56.8 to 68.7 mm (mean Cucurbitaceae, Fig. 8A–D). Pollen dispersed as mo- 61.3 mm), E ranged from 60.2 to 69.6 mm (mean nads; grains isopolar, radially symmetrical, oblate to 65.6 mm); grains pantoporate, apertures simple, global, subspheroidal, amb circular; pollen size large, P ranged with granulate membrane, operculum present; atectate, from 58.8 to 68.7 mm (mean 62.5 mm), E ranged from echinate, infratectum structure columellate; foot layer 60.5 to 70.6 mm (mean 66.5 mm); grains tricolporate, present. apertures compound, equatorial, with granulate mem- Dendrosicyos socotranus Balf. f. (Cucurbitales, Cucur- branes, endoapertures lalongate, operculum absent; bitaceae, Fig. 7I–L). Pollen dispersed as monads; grains tectum fossulate, supratectal elements absent; infratec- isopolar, radially symmetrical, oblate to subspheroidal, tum structure columellate; foot layer present. amb circular; pollen size large, P ranged from 56.8 to Marah macrocarpa Greene (Cucurbitales, Cucurbi- 68.7 mm (mean 61.3 mm), E ranged from 60.2 to taceae, Fig. 8E–H). Pollen dispersed as monads; grains 69.6 mm (mean 65.6 mm); grains tricolporate, apertures isopolar, radially symmetrical, prolate, amb lobate; compound, equatorial, with granulate membranes, pollen size large, P ranged from 58.8 to 77.6 mm (mean endoapertures circular, operculum absent; tectum re- 67.2 mm), E ranged from 32.2 to 49.6 mm (mean ticulate with apparent pili in the lumina, supratectal 38.9 mm); grains 4-colporate, apertures compound, elements absent; infratectum structure columellate; foot equatorial, with granulate membranes, endoapertures layer present. lalongate, operculum absent; tectum reticulate, supratectal

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Figure 6. SEM and transmission electron micrographs (TEM) of pollen from the nitrogen-fixing clade, continued. A, B. Myrica esculenta Buch.-Ham. ex D. Don (Fagales, Myricaceae). —A. Equatorial view (SEM), showing single free, globose pollen grain, tripororate and imperforate tectum. —B. Mesocolpial exine showing echinate supratectal element (S), tectum (T), granular infratectum structure (G), foot layer (F), and thin endexine (E; TEM). C, D. Rhoiptelea chiliantha Diels & Hand.-Mazz. —C. Equatorial view. —D. Mesocolpial and mesoaperturate exines, the former showing echinate supratectal element (S), tectum (T), granular infratectum structure (G), foot layer (F), and endexine (E), the latter (AP) showing annulus vestibulate, foot layer and thickenings of endexine (TEM). E–H. Juglans mandshurica Maxim. —E. Polar view, showing single free pollen grain, 5- to 10- pororate. —F. Equatorial view, showing polarity subisopolar. —G. Aperture and exine surface, showing ora circular. —H. Mesocolpial and mesoaperturate exines, the former showing echinate supratectal element (S), tectum (T), granular infratectum structure (G), foot layer (F), and endexine (E), the latter (AP) showing annulus vestibulate, foot layer and thickenings of endexine (TEM). I–L. Coriaria sinica Maxim. (Cucurbitales, Coriariaceae). —I. Polar view. —J. Equatorial view. —K. Aperture and exine surface, showing ora circular. —L. Mesocolpial and mesoaperturate exines, the former showing gemmate supratectal element (S), tectum (T), columellae (C), foot layer (F), and endexine (E), the latter (AP) showing annulus vestibulate, foot layer, and thickenings of endexine (TEM).

elements absent; infratectum structure columellate; foot grains isopolar, radially symmetrical, prolate, amb cir- layer present. cular; pollen size small, P ranged from 12.1 to 20.3 mm Begonia cucurbitifolia C. Y. Wu (Cucurbitales, Bego- (mean 16.3 mm), E ranged from 8.4 to 17.0 mm (mean niaceae, Fig. 8I–L). Pollen dispersed as monads; grains 11.5 mm); grains tricolporate, apertures compound, isopolar, radially symmetrical, perprolate, amb lobate; equatorial, with granulate membranes, endoapertures pollen size medium, P ranged from 18.5 to 32.0 mm circular, operculum absent; tectum imperforate, supra- (mean 26.0 mm), E ranged from 8.5 to 12.6 mm (mean tectal elements present, striate; infratectum structure 11.9 mm); grain tricolporate, apertures compound, columellate; foot layer present. equatorial, with granulate membranes, endoapertures Datisca cannabina L. (Cucurbitales, Datiscaceae, circular, operculum absent; tectum striate and perfo- Fig. 9E–H). Pollen dispersed as monads; grains iso- rate, supratectal elements absent; infratectum structure polar, radially symmetrical, prolate, amb circular; pol- columellate; foot layer present. len size small, P ranged from 132.8 to 148.7 mm (mean Hillebrandia sandwicensis Oliv. (Cucurbitales, Bego- 138.5 mm), E ranged from 135.2 to 145.6 mm (mean niaceae, Fig. 9A–D). Pollen dispersed as monads; 138.6 mm); grains tricolporate, apertures compound,

Figure 7. SEM and transmission electron micrographs (TEM) of pollen from the nitrogen-fixing clade, continued. A–D. Corynocarpus laevigatus J. R. Forst. & G. Forst. —A. Distal polar view (SEM), showing monad, oblate, monoporate pollen grain, 2-colporate. —B. Equatorial view. —C. Showing exine surface. —D. Mesocolpial exine showing tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; TEM). E–H. Cucurbita pepo L. —E. Showing single free, globose pollen grain, spheroidal, polarity apolar, pantoporate. —F. Showing exine surface. —G. Showing exine surface and operculum (O). —H. Mesocolpial exine showing echinate supratectal element (S), tectum (T), foot layer (F), and thin endexine (E; TEM). I–L. Dendrosicyos socotranus Balf. f. —I. Polar view, showing monad, subspheroidal, monoporate pollen grain, 3-colporate. —J. Equatorial view. —K. Showing exine surface. —L. Mesocolpial exine showing tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; TEM).

equatorial, with granulate membranes, endoapertures [BS]), followed by Rosales, and Fagales and Cucurbi- circular, operculum absent; tectum rugulate, supractal tales, which form sister groups (77% BS). In general, elements absent; infratectum structure columellate; foot the topology of the nitrogen-fixing clade is consistent layer present. with that of Li et al. (2015) at or above family level Tetrameles nudiflora R. Br. (Cucurbitales, Tetrame- except in the placements of Barbeyaceae and Myri- laceae, Fig. 9I–L). Pollen dispersed as monads; grains caceae (Supplementary Fig. S1). In our phylogeny, isopolar, radially symmetrical, prolate, amb circular; Barbeyaceae and Dirachmaceae form a clade, as do pollen size very small, P ranged from 8.5 to 12.3 mm Myricaceae and Juglandaceae, whereas Li et al. (2015) m m (mean 9.8 m), E ranged from 5.4 to 8.5 m (mean found that Barbeyaceae is closely positioned to m 6.5 m); grains tricolporate, apertures compound, equa- Elaeagnaceae, and Myricaceae is nested within a clade torial, with granulate membranes, endoapertures circu- that includes Casuarinaceae, Ticodendraceae, and lar, operculum absent; tectum fossulate, supratectal Betulaceae. However, the placements of Barbeyaceae elements absent; infratectum structure columellate; foot and Myricaceae were poorly supported in both the layer present. present study and Li et al. (2015; BS , 65%). Ninety percent of the genera placements in our tree were PHYLOGENY OF THE NITROGEN-FIXING CLADE consistent with those of Li et al. (2015), and all In our reconstructed ML tree, the Fabales was found to inconsistent positions were poorly supported in both be the first branching clade (with 100% bootstrap support phylogenies (BS usually , 50%).

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Figure 8. SEM and transmission electron micrographs (TEM) of pollen from the nitrogen-fixing clade, continued. A–D. Lagenaria siceraria (Molina) Standl. —A. Polar view (SEM), showing monad, subspheroidal, monoporate pollen grain, 3-colporate. —B. Equatorial view. —C. Showing aperture and exine surface. —D. Mesocolpial exine showing tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; TEM). E–H. Marah macrocarpa Greene. —E. Polar view, showing single free, prolate pollen grain, 4-colporate. —F. Equatorial view. —G. Showing exine surface. —H. Mesocolpial exine showing tectum (T), infratectum columellate (C), foot layer (F), and thin endexine (E; SEM). I–L. Begonia cucurbitifolia C. Y. Wu. —I. Polar view, showing monad, perprolate, monoporate pollen grain, 3-colporate. —J. Equatorial view. —K. Showing tectum sculpture perforate. —L. Mesocolpial exine showing echinate supratectal element (S), tectum (T), foot layer (F), endexine (E), the latter (AP) showing annulus vestibulate, foot layer and thickenings of endexine (TEM).

POLLEN DIVERSITY and have an imperforate, perforate, or rugulate tectum (Appendix 4). The diversity of pollen grain character states varies In contrast, Fabales and Cucurbitales are more vari- across the nitrogen-fixing clade; Rosales and Fagales able in pollen form. Fabaceae display the highest show relatively conservative pollen morphologies. In palynological variation of all the families studied, with Rosales, the morphology of pollen in Moraceae, grains varying in dispersal unit (character 1, including Cannabaceae, Ulmaceae, and Urticaceae is gener- monads, tetrads, and polyads), shape class (character 4, ally similar and varies little within families; all the families are commonly characterized by small or including oblate, subspheroidal, prolate, and perpro- medium-sized pollen that is porate with gemmate late), polar view (character 5, including circular and or echinate supratectal elements, and an imperforate polygonal), pollen size (character 6, ranging from very or perforate or rugulate tectum (Appendix 4). In small to very large), aperture number (character 7, Fagales, pollen grains of most taxa are dispersed bearing a great number of varieties that range from as isopolar or apolar (in only a few members of three to more than 20), aperture position (character 8, Juglandaceae) monads, are subspheroidal in shape, including global or equatorial), aperture shape (char- polygonal in outline, and of small or medium size. The acters 9 and 10, including colporate, porate, and col- pollen grains have apertures that range in number pate), and tectum sculpture (character 16, including all from three to 37 (usually three), are porate or colpo- seven types coded in our study) (Appendix 4). Poly- rate, with gemmate or echinate supratectal elements, galaceae have the high diversity in aperture number

Figure 9. SEM and transmission electron micrographs (TEM) of pollen from the nitrogen-fixing clade, continued. A–D. Hillebrandia sandwicensis Oliv. —A. Polar view (SEM), showing monad, lobate, monoporate pollen grain, 3-colporate. —B. Equatorial view. —C. Showing exine surface striate. —D. Mesocolpial exine showing tectum (T), infratectum columellate (C), foot layer (F), endexine (E), the latter (AP) showing annulus vestibulate, foot layer, and thickenings of endexine (TEM). E–H. Datisca cannabina L. —E. Showing single free, globose pollen grain, lobate, 3-colporate. —F. Equatorial view. —G. Showing exine surface. —H. Mesocolpial exine showing supratectal element (S) gemmate, tectum (T), infratectum columellate (C), foot layer (F), endexine (E), the latter (AP) showing annulus vestibulate, foot layer, and thickenings of endexine (TEM). I–L. Tetrameles nudiflora R. Br. —I. Polar view, showing monad, lobate, monoporate pollen grain, size very small, 3-colporate. —J. Equatorial view. —K. Showing exine surface. —L. Mesocolpial exine showing tectum (T), infratectum columellate (C), thickenings of foot layer (F), and thin endexine (E; TEM).

(from three to more than 30) and tectum sculpture numbers ranging from three to seven, apertures that (imperforate, perforate, fossulate, and rugulate); endo- are colporate or porate, supratectal elements absent or aperture fusion to form an endocingulum is also common gemmate, striate, or echinate, and tectum sculpture that at the interspecific level in this family. In Cucurbitales, is perforate or reticulate (Appendix 4). Cucurbitaceae also show pollen morphological variation in dispersal unit (including monad and tetrad), aperture INFERENCES OF ANCESTRAL STATES shape (including colporate, porate, and colpate), and tectum sculpture (reticulate and striate being domi- When plesiomorphic states for the nitrogen-fixing nant types, but perforate and rugulate types are also clade as a whole were reconstructed, 12 out of 18 found). Notably, some members of Cucurbitaceae are characters displayed a congruent state across all five characterized by large atectate pollen grains that are methods of inference (CFP, DFP, DML, CHB, and significantly different from others observed in the DHB; counting ambiguous states as congruent). Thus, nitrogen-fixing clade (Appendix 4). the consistent plesiomorphic states inferred for the Within genera, pollen morphology is generally con- nitrogen-fixing clade are as follows: pollen dispersal sistent, but some species within genera show high as monads; polarity that is isopolar; medium pollen size; diversity in pollen grain morphology. For example, aperture number equal to three; equatorial aperture pollen grains of species from Bauhinia L. (Fabaceae) position; compound aperture structure; ectoaperture disperse as monads or tetrads and have aperture shape that is colpate; aperture membrane ornamentation:

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granulate; operculum and supratectal elements: absent; (CHB, DHB) or ambiguous (CFP, DFP, DML); and foot supratectal element shape: inapplicable data; and infra- layer present under all methods. tectum structure that is columellate (ambiguous under For Cucurbitales, 12 pollen characters showed con- DML). The remaining six characters were inconsistently sistent states in their most recent common ancestors resolved across the five methods: symmetry in polar view across the five analytical methods except polarity (char- was plesiomorphically radial (under the CFP, DFP, DML, acter 2), symmetry in polar view (character 3), shape DHB models) or bilateral (under CHB); shape class was class (character 4), amb (character 5), aperture number subspheroidal (CFP, DFP, DML, CHB) or oblate (DHB); (character 7), and tectum sculpture (character 16). Ten outline in polar view was plesiomorphically circular plesiomorphic states (dispersal unit, size, aperture po- (CFP, DFP, DML, DHB) or polygonal (CHB); endoaper- sition, aperture structure, ectoaperture shape, presence ture shape was inapplicable data (CFP, DFP, DML) or of operculum, aperture membrane, presence of supra- circular (CHB, DHB); tectum sculpture was reticulate tectal elements, supratectal element shape, and infra- (CFP, DFP), rugulate (CHB), foveolate or fossulate tectum structure) were consistent with ancestral states (DHB), or ambiguous (DML); and foot layer was either of this clade. The remaining eight characters included absent (CFP, CHB), present (DFP, DHB), or ambiguous polarity that was isopolar (CFP, DFP, DML) or hetero- (DML). polar (CHB, DHB); radial polar view that was sym- For Fabales, all the pollen characters showed con- metric (CFP, DFP, DML) or bilateral (CHB, DHB); and sistent states in their most recent common ancestors shape class that was subspheroidal (DML), prolate across the five analytical methods except endoaperture (CFP, CHB, DHB) or ambiguous (FDP). In addition, shape (character 11) and tectum sculpture (character the outline in polar view was plesiomorphically cir- 16). Twelve plesiomorphic states were consistent with cular (CFP, DFP, DML) or lobed (CHB, DHB); aper- ancestral states of this clade. These include: dispersal ture number was three (CFP, DFP, DML) or two (CHB, unit, polarity, size, aperture number, aperture posi- DHB); endoaperture shape was circular; tectum sculp- tion, aperture structure, ectoaperture shape, aperture ture was rugulate (DML, CHB, DHB), perforate (CFP) membrane ornamentation, presence of an operculum, or ambiguous (DFP); and foot layer was present under presence of supratectal elements, supratectal element all methods. shape, and infratectum structure. The remaining six For Rosales, 12 pollen characters showed consistent character states included: symmetric in radial polar states in their most recent common ancestors across the view; subspheroidal in shape; plesiomorphically cir- five analytical methods except symmetry in polar view cular in polar view; endoaperture shape that was (character 3), amb (character 5), size (character 6), circular (CFP, DFP), lalongate (CHB, DHB), or am- aperture shape (character 11), supratectal element biguous (DML); tectum sculpture that was perforate shape (character 15), and tectum sculpture (character (CFP, CHB), areolate (DHB), or ambiguous (DFP, 16). Ten plesiomorphic states were consistent with DML); and foot layer that was present under all ancestral states of this clade, namely dispersal unit, methods. polarity, aperture number, aperture position, aperture For Fagales, 15 pollen characters showed consis- structure, ectoaperture shape, presence of an opercu- tent states in their most recent common ancestors lum, aperture membrane, presence of supratectal ele- across the five analytical methods used, except for ments, and infratectum structure. The remaining eight shape class (character 4), amb (character 5), and characters included symmetry in radial polar view (CFP, aperture membrane (character 12). Eleven plesiomor- DFP, DML, DHB) or bilateral (CHB); subspherioidal phic states were inferred as being consistent with shape class; outline in polar view that was plesiomorph- ancestral states of this clade, namely dispersal unit, ically circular (CFP, DFP, DML, DHB) or polygonal polarity, size, aperture number, aperture position, (CHB); pollen size that was medium (CFP, DFP, DML, aperture structure, ectoaperture shape, presence of DHB) or small (CHB); endoaperture shape that was an operculum, presence of supratectal elements, circular (DFP, DML, CHB), lolongate (CFP), or lalon- supratectal element shape, and infratectum structure. gate (DHB); supratectal element shape that was in an The remaining seven character states included sym- inapplicable state (CFP, DFP, DML) or gemmate (CHB, metry in radial polar view; shape class that was DHB); tectum sculpture that was perforate (CFP), am- subspheroidal (CFP, DFP, DML) or oblate (CHB, biguous (DFP), rugulate (DML), striate (CHB), foveolate DHB); plesiomorphically circular outline in polar or fossulate (DHB); and foot layer that was present but view (CFP), polygonal (DFP, CHB, DHB), or ambig- ambiguous under CHB. uous (DML); aperture membrane that was granulate The character state changes inferred under all methods (CFP, DFP, DML, CHB) or smooth (DHB); circular of analysis were also broadly similar. For brevity, we focus endoaperture shape (DFP, DML, DHB) or ambiguous on the result of one analysis, the CHB optimization, which (CFP, DML); tectum sculpture that was imperforate is both consistent with previous papers in the series and

Figure 10. A–C. Character state changes for 18 pollen morphology characters reconstructed with hierarchial Bayesian inference using comprehensive coding on a maximum likelihood phylogeny, based on a reduced molecular data matrix from Li et al. (2015).

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Figure 10. Continued.

produces the fewest equivocal states at internal nodes. and Cucurbitales (96) (Fig. 10). Fagales showed the least The state changes of pollen characters are illustrated in number of pollen state changes (49). Of the pollen Figure 10. Fabales displayed the highest number of characters, two characters (1 and 8) only changed their pollen state changes (190), followed by Rosales (101) state nine times; six characters changed their state 10 to

Figure 10. Continued.

19 times; five characters showed 20 to 28 incidents of of the orders; the remainder of these changes was found state changes; four characters changed their state 30 to 46 on the stem lineages of the 18 families. The rate of times; and character 16, tectum sculpture, showed the pollen character state change varied between inter- highest number of occurrences for character state changes nodes: one was inferred with eight transitions (namely 70 times (Fig. 10) the branch subtending the clade comprising Ulmaceae, Pollen character state changes at or above family Cannabaceae, Moraceae, and Urticaceae). Another two level within the nitrogen-fixing clade are shown in Table internodes were inferred to bear seven state changes 2. In total, 150 pollen character states were recorded at (namely the branch subtending Elaeagnaceae, and the this level. Of these, 22 state changes occurred on the branch leading to Ulmaceae). Other internodes had branches subtending the most recent common ancestors fewer changes: eight internodes had only two changes

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for the branches subtending a particular taxonomic group. analyses conducted (Table 2; Fig. 10). These changes These include the branches subtending the Fabaceae; provide new systematic insights into pollen character state the Fabales; the Begoniaceae; the Moraceae; the clade evolution and show great potential for delineating lineages. comprising Cannabaceae, Moraceae, and Urticaceae; the Below, we discuss in detail some of the interesting patterns clade comprising Ticodendraceae and Betulaceae; the of pollen character states that we found in our study. Anisophylleaceae and Cucurbitaceae; and the branch subtending the clade comprising Rosales, Fagales, and Fabales Cucurbitales. Six internodes had only a single change. The circumscription of Fabales has remained stable These include the branch subtending: the Betulaceae; the since APG I (1998); however, relationships within the Cucurbitaceae; the Rhamnaceae; the Juglandaceae, group remain unclear. The three main conflicting topol- Myricaceae, Casuarinaceae, Ticodendraceae, and Betu- ogies within the order (Persson, 2001; Bello et al., 2009; laceae; the Fagaceae, Juglandaceae, Myricaceae, Casu- Li et al., 2015) are summarized in Figure 11A–C. Among arinaceae, Ticodendraceae, and Betulaceae; and the the three alternative topologies tested, topology C (namely Begoniaceae, Datiscaceae, and Tetramelaceae. One Fabaceae and Polygalaceae forming one clade, and branch, that subtends Rosales, was not characterized Quillajaceae and Surianaceae forming another), found by any inferred character state changes. in the latest large-scale phylogenetic analysis of Li et al. (2015), invoked the fewest pollen character state changes ANALYSES OF CORRELATED EVOLUTION in the CFP analysis, which makes it most compatible with the theory of parsimony. Our optimization Of the 767 pair-wise comparisons to assess correlated studies found that the sister group relationship be- evolution between the palynological character states tween Quillajaceae and Surianaceae (as indicated by and ecological data, 25 pairs showed strong support Wojciechowski et al., 2004; Mercure et al., 2008; Bello (P , 0.005) for correlated evolution between pollen et al., 2009, 2012; Li et al., 2015, 2016; Sun et al., characters and ecological traits (Table 3). Twenty-two 2016) share transitions to polygonal outline in polar pairs were significantly correlated with eight pollen view (character 5; DHB), lalongate endoapertures (char- characters including shape class, outline in polar view, acter 11; CFP, DFP), and striate tectum sculpture aperture structure, ectoaperture and endoaperture (character 16; DHB). Similarly, the sister groupings shape, the presence of supratectal element, supratectal of Polygalaceae and Fabaceae (indicated by Li element shape, tectum sculpture, and pollination type. et al., 2015, 2016; L. Zhao et al., 2016) share tran- Specifically, taxa with prolate shape class (LBF 5 sitions to bilaterally symmetrical pollen grains (char- 16.76), outline in polar view that was lobe shaped acter 3; CHB), endocingulate endoapertures (character (LBF 5 20.31), colpate ectoaperture (LBF 5 19.11), 11; CHB, DHB), and perforate tectum sculpture (char- lalongate (LBF 5 24.97) and lolongate endoaperture acter 16; DHB). (LBF 5 18.20), and the absence of a supratectal element (LBF 5 28.59), were all correlated with insect Rosales pollination. Alternatively, taxa with simple rather than Within Rosales, the relationships between Dirachma- compound aperture structure (LBF 5 20.09), porate ceae, Rhamnaceae, Barbeyaceae, and Elaeagnaceae re- ectoaperture (LBF 5 22.01), circular endoaperture main unclear (Zhang et al., 2011; Li et al., 2015). The two (LBF 5 18.28), present (LBF 5 29.26) and echinate main topologies for these taxa (Zhang et al., 2011; Li et al., (LBF 5 22.04) supratectal elements, and imperforate 2015), and a third (reconstructed in Wang et al., 2009, rather than reticulate tectum sculpture (LBF 5 20.19), and Soltis et al., 2011), are shown in Figure 11D–F. Of the were all correlated with wind pollination. Furthermore, three alternative topologies tested, topology E (Li et al., rugulate tectum was significantly correlated with shrub 2015; Sun et al., 2016) was the most parsimonious in habit (LBF 5 19.86), while larger pollen size was sig- terms of pollen character state changes. The grouping of nificantly correlated with vine habit (LBF 5 17.00), and Elaeagnaceae, Barbeyaceae, and Dirachmaceae, found in helophytic habitat was significantly correlated with two our study, as well as in that of Zhang et al. (2011), is apertures (LBF 5 19.72). distinguished by a circular amb (character 5; CHB, DHB), large-sized pollen grains (character 6; DML, DISCUSSION CHB), lalongate endoapertures (character 11; CHB, DHB), presence of a supratectal element (character 14; SYSTEMATIC SIGNIFICANCE OF POLLEN MORPHOLOGY IN THE CHB, DHB), gemmate supratectal element (character NITROGEN-FIXING CLADE 15; CHB, DHB), and a rugulate tectum sculpture (char- More than 40 clades at or above familial level in the acter 16; CHB, DHB). The larger grouping of Barbeya- nitrogen-fixing clade were characterized by unambiguous ceae, Dirachmaceae, Elaegnaceae, and Rhamnaceae, pollen character state changes in at least one of the five which is not phylogenetically disputed, may be

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Table 2. State changes of the 18 studied pollen characters for lineages at or above family level inferred from Fitch parsimony, maximum likelihood, the of Annals and hierarchical Bayesian inference on 190 comprehensive and democratic datasets. Pollen characters and state numbers follow Table 1.

Taxon C01 C02 C03 C04 C05 C06 C07 C08 C09 C10 C11 C12 C13 C14 C15 C16 C17 C18 Fabales 2e 1d 1e 1de 2e Fabaceae 0e 3e Polygalaceae 1d 3abcde 1ab 1e 2d;0e Surianaceae 0e 1e 3de Fagales 2e 1e Betulaceae 3b Casuarinaceae 0e 0c 4c 0de 1e Fagaceae 1d;2e 2e 0de 2d 0abcde Juglandaceae 2e 0de 2de 1de Cucurbitales 1d 2e 1d Anisophylleaceae 2c 1de 1de Begoniaceae 2c 5bcd Cucurbitaceae 1de Tetramelaceae 1de 1de 0de 4de 0d Cannabaceae 1e 2e 2de 0abc 1e 1d Elaeagnaceae 2de 2de 2de 0d 0abc 0de 0e isuiBtnclGarden Botanical Missouri Moraceae 1d 1d Rhamnaceae 0abc Rosaceae 1d 1d 3abe 4de 5ae Ulmaceae 1de 0de 3abcde 0abcde 4abce 3d 1e Urticaceae 0abcde 4abce 0e 0ae Quillajaceae–Surianaceae 0e 2ab 5e Fabaceae–Polygalaceae 0d 1de 1e Elaeagnaceae–Barbeyaceae–Dirachmaceae 1de 3de 3de 1de 0de 3de Rhamnaceae–Elaeagnaceae–Barbeyaceae– 1d 0e 2e 2e 0de 2d Dirachmaceae Moraceae–Urticaceae 1abd 1e 1de 0d Cannabaceae–Moraceae–Urticaceae 1e 0de Ulmaceae–Cannabaceae–Moraceae–Urticaceae 0e 1d 2e 1d 1abcde 1a 1abcde 1d;3e (Elaeagnaceae–Rhamnaceae–Barbeyaceae– 1e 0e 2d Dirachmaceae)–(Ulmaceae–Cannabaceae– Moraceae–Urticaceae) Ticodendraceae–Betulaceae 1de 0de Casuarinaceae–Ticodendraceae–Betulaceae 1de 1e 0de 4de 1d;3e Terms ofUse: https://bioone.org/terms-of-use Access provided by Kunming Institute of Botany, CAS Downloaded From: https://bioone.org/journals/Annals-of-the-Missouri-Botanical-Garden on 01 Apr 2020

Table 2. Continued. 2019 2 Number 104, Volume

Taxon C01 C02 C03 C04 C05 C06 C07 C08 C09 C10 C11 C12 C13 C14 C15 C16 C17 C18 Juglandaceae–Myricaceae 0a 0a 0ab (Juglandaceae–Myricaceae)–(Casuarinaceae– 1abc Ticodendraceae–Betulaceae) Fagaceae–(Juglandaceae– 1de Myricaceae)–(Casuarinaceae–Ticodendraceae– Betulaceae) Coriariaceae–Corynocarpaceae 0de 3de 1b 3de Begoniaceae–Datiscaceae–Tetramelaceae 3e Anisophylleaceae–Cucurbitaceae 1de 2de (Anisophylleaceae–Cucurbitaceae)–(Begoniaceae– 2de 1de 2ad 1de 2de 5de Datiscaceae–Tetramelaceae) Fagales–Cucurbitales 0d 2d;0e 1e 0de 1d Rosales–(Fagales–Cucurbitales) 1d 0de Fabales–(Rosales–(Fagales–Cucurbitales)) 1e 2e 1e 0ab 1a

CFP. a b DFP. c DML. 191 Nitrogen- Clade 7. fixing Pollen. Angiosperm of Evolution al. et Jiang d CHB. e DHB. 192 Annals of the Missouri Botanical Garden

Table 3. Correlation test between pollen characters and ecological factors using maximum likelihood (ML) and Markov chain Monte Carlo (MCMC) methods.

ML MCMC

Likelihood Harmonic mean of log-likelihood

Independent Dependent Likelihood Independent Dependent Log Bayes Trait pair (pollen trait_ecological trait) model model ratio (LR) model model factor (LBF) Shape class prolate_insect pollination 2230.96 2220.30 21.32* 2240.40 2232.02 16.76* Polar view lobe_wind pollination 2105.18 296.40 17.56* 2115.99 2106.74 18.50* Polar view lobe_insect pollination 2125.95 2113.58 24.75* 2133.82 2123.67 20.31* Aperture structure simple_wind 2162.13 2149.92 24.44* 2170.50 2160.46 20.09* pollination Aperture structure compound_wind 2155.29 2142.38 25.82* 2165.85 2152.37 26.96* pollination Ectoaperture colpate_wind pollination 2157.30 2143.36 27.87* 2165.92 2152.88 26.07* Ectoaperture colpate_insect pollination 2178.71 2164.09 29.25* 2183.68 2174.13 19.11* Ectoaperture porate_wind pollination 2153.77 2142.49 22.55* 2162.49 2151.49 22.01* Endoaperture circular_wind pollination 2242.16 2233.25 17.83* 2257.44 2248.30 18.28* Endoaperture lalongate_wind pollination 2230.39 2221.36 18.06* 2241.61 2230.68 21.87* Endoaperture lalongate_insect 2251.79 2241.37 20.85* 2261.09 2248.61 24.97* pollination Endoaperture lolongate_insect 2232.74 2222.17 21.15* 2243.87 2234.77 18.20* pollination Supratectal element absent_wind 2198.88 2177.75 42.26* 2204.00 2188.23 31.52* pollination Supratectal element absent_insect 2220.30 2198.08 44.44* 2225.08 2210.78 28.59* pollination Supratectal element present_wind 2201.84 2179.31 45.06* 2206.41 2191.78 29.26* pollination Supratectal element present_insect 2223.26 2200.27 45.97* 2228.06 2213.17 29.79* pollination Supratectal element shape gemmate 2166.04 2151.90 28.29* 2179.27 2168.89 20.75* (including verrucate)_wind pollination Supratectal element shape gemmate 2187.33 2169.20 36.27* 2202.04 2189.16 25.77* (including verrucate)_insect pollination Supratectal element shape echinate_wind 2141.42 2131.60 19.64* 2150.74 2139.72 22.04* pollination Tectum sculpture imperforate_wind 2139.40 2129.96 18.88* 2148.98 2138.88 20.19* pollination Tectum sculpture reticulate_wind 2189.96 2181.46 17.00* 2198.53 2188.08 20.91* pollination Tectum sculpture reticulate_insect 2211.37 2199.79 23.18* 2220.23 2210.63 19.21* pollination Tectum sculpture rugulate_shrub 2354.91 2342.55 24.71* 2361.85 2351.92 19.86* Size_vine 2272.29 2258.06 28.47* 2276.67 2268.17 17.00* Aperture number two_helophytic 2106.44 296.06 20.75* 2112.97 2103.11 19.72*

*P , 0.005.

distinguished from its closest relatives by symmetrical Cucurbitales pollen grains (character 3; CHB), a circular amb (char- A new circumscription of Cucurbitales was defined in acter 5; CHB), triaperturate pollen grains (character 7; the most recent APG classification (APG IV, 2016). CHB) with lalongate endoapertures (character 11; Within the order, three conflicting topologies have been DHB), a lack of supratectal elements (character 14; recovered in recent years (Zhang et al., 2006; Schaefer CHB, DHB), and a rugulate supratectal element (char- & Renner, 2011b; Li et al., 2015; Fig. 11G–I). Of these, acter 15; CHB). the topology recovered by Li et al. (2015) invoked the

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Figure 11. Alternative topologies for the phylogeny of the nitrogen-fixing clade. A–C, Fabales; D–F, Rosales; G–I, Cucurbitales; J–L, Fagales. Faba, Fabaceae; Quil, Quillajaceae; Suri, Surianaceae; Poly, Polygalaceae; Barb, Barbeyaceae; Dira, Dirachmaceae; Elae, Elaeagnaceae; Rham, Rhamnaceae; Dati, Datiscaceae; Bego, Begoniaceae; Tetr, Tetramelaceae; Cucu, Cucurbitaceae; Cori, Coriariaceae; Cory, Corynocarpaceae; Anis, Anisophylleaceae; Tico, Ticodendraceae; Betu, Betulaceae; Casu, Casuarinaceae; Jugl, Juglandaceae; Myri, Myricaceae.

fewest pollen character state changes under CFP, sug- other morphological synapomorphies, including the gesting it to be the most parsimonious. Relationships presence of one basal orthotropous ovule, peltate, among Begoniaceae, Datiscaceae, and Tetramelaceae glandular hairs, and the absence of stipules (Li remain controversial, with several studies moderately et al., 2004). supporting Datiscaceae and Begoniaceae as sister groups. The alternative grouping of Datiscaceae and PATTERNS OF POLLEN CHARACTER STATE CHANGE Tetramelaceae was weakly supported (BS , 50%) in Most of the derived states found in this study were Swensen et al. (1994), Li et al. (2015), and Sun et al. inferred to have evolved independently multiple times (2016). A change to rugulate tectum sculpture (charac- (see Fig. 10). The frequency of state changes, however, ter 6, DHB) was found to distinguish the branch leading varied greatly between characters. A high frequency of to Begoniaceae, Datiscaceae, and Tetramelaceae. character state change was observed in shape class, A sister relationship between Cucurbitaceae and outline in polar view, pollen size, endoaperture shape, Anisophylleaceae, as found by Li et al. (2015), was and tectum sculpture, but a comparatively low fre- distinguished in our study by two shared pollen char- quency was observed in dispersal unit, aperture po- acter state changes: to circular outline in polar view sition, and aperture membrane (Fig. 10). Below we (character 5; CHB, DHB), and to medium pollen size discuss previously postulated evolutionary trends (character 6; CHB, DHB). The clade of Cucurbitales, (reviewed by Punt, 1975) for a number of pollen char- excluding Corynocarpaceae and Coriariaceae, was characters that showed interesting character state changes acterized by the following character state changes: to in our study. isopolar polarity (character 2; CHB, DHB), to radial symmetry (character 3; CHB, DHB), to prolate pollen shape (character 4; CFP, CHB), to small pollen size Dispersal unit (character 6; CHB, DHB), to 3-aperture (character 7; The pollen of the nitrogen-fixing clade is usually CHB, DHB), and to striate tectum sculpture (character dispersed as monads, with a few transitions to tetrad and 16; CHB, DHB). Furthermore, four character states polyad dispersal in Cucurbitaceae and Fabaceae. This were acquired in the branch leading to Corynocarpaceae is in line with the angiosperms as a whole, in which and Coriariaceae. These include oblate pollen shape monad dispersal is plesiomorphic and permanent tet- (character 4; CHB, DHB), elliptic polar view (character rads are the most common form of aggregation, having 5; CHB, DHB), two apertures (character 7; DFP), and arisen independently several times during the evolution lolongate endoapertures (character 11; CHB, DHB). of flowering plants (Lora et al., 2014). According to recent classifications of Fabaceae (LPWG, 2017) and Fagales Cucurbitaceae (Schaefer & Renner, 2011a), tetrad dis- The current circumscription of Fagales has been persal characterizes four distinct lineages: Cercidoideae recognized since APG II (2003). However, there are at and Caesalpinioideae in the Fabaceae, and Coniandreae least three conflicting topologies regarding the posi- and Benincaseae in the Cucurbitaceae. Polyads occur tion of Myricaceae within this order (Li et al., 2002, only in Caesalpinioideae in the nitrogen-fixing clade. A 2004, 2015; the latter being consistent with the present study of pollen aggregation of Annona L. (Annonaceae) study; Fig. 11J–L). Of the three alternative topologies suggests that key events occurring in pollen development tested, topology L (i.e., Myricaceae plus Juglandaceae result in clear morphological changes in pollen dispersal as sister to the clade of Casuarinaceae, Betulaceae, and time and propose a possible selective advantage of pollen Ticodendraceae) invoked the fewest pollen character aggregation (Lora et al., 2014). state changes under the CFP analysis and is therefore favored by pollen morphology based on parsimony. This Polarity and symmetry is consistent with relationships found in Li et al. (2004), The plesiomorphic states of polarity and symmetry for but not in the latest phylogeny of the nitrogen-fixing the pollen of both basal angiosperms and monocots were clade (Li et al., 2015). Interestingly, Li et al.’s (2004) inferred to be heteropolar and bilateral, respectively (Lu grouping of Juglandaceae and Myricaceae received et al., 2015; Luo et al., 2015), while that of eudicots were higher (albeit low, 66%) BS support than alternative re- inferred to be isopolar and radial (M.-Y. Zhang et al., lationships. The sister group of Myricaceae and Juglan- 2017). It therefore comes as no surprise that the pollen daceae was characterized by three character state of the nitrogen-fixing clade, which is nested within changes: to polygonal pollen outline in polar view (char- eudicots, is also plesiomorphically isopolar and radially acter 5; CFP), to circular endoapertures (character 11; symmetrical. Furthermore, apolarity and heteropolarity CFP), and to imperforate tectum sculpture (character 16; have evolved in several lineages, for instance in Cucurbita CFP, DFP). Li et al. (2004) point out that the clade L. (Cucurbitaceae; apolar), Juglans L. (Juglandaceae; comprising Myricaceae and Juglandaceae also shares apolar), Dorstenia (Moraceae; apolar), Heterosamara

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Kuntze (Polygalaceae; heteropolar), and Corynocar- they commonly occur in the eudicots. Although their paceae (heteropolar). observation may be indicative of a general shift from simple to compound aperture structure in the angio- Aperture system sperms, compound aperture structures may also be An increase in pollen aperture number is considered correlated with pollen tube germination and emergence, to be a general trend in angiosperms (Furness & Rudall, and/or harmomegathic form and function (M. Y. Zhang 2004). Under all the models used in our study, the et al., 2017). However, in our study, reversions from transition from few to multiple apertures was inferred compound to simple aperture structure were detected in to occur in several distinct lineages, i.e., the branch three branches within Fabaceae, one branch within leading to Ulmaceae in Rosales and the branch leading Fagales, five branches within Cucurbitaceae, and to Polygalaceae in Fabales. Increasing aperture number two branches within Rosales (Fig. 10). Although the in angiosperms has been assumed to be associated with nitrogen-fixing clade appears to be a transition clade an increase in fitness (Punt, 1975; Dajoz et al., 1991). from compound to simple aperture structure, ecology Despite a decrease in pollen survival with increasing may also be influencing the transition of this state. We aperture number (Mignot et al., 1994), it has been also found that insect pollination was strongly corre- hypothesized that contact between at least one aperture lated with compound aperture structure, and wind and the stigmatic surface can facilitate pollen germina- pollination was significantly correlated with taxa that tion (Furness & Rudall, 2004). Although these hypoth- have simple aperture pollen. Collectively, these results eses remain untested, in our study taxa with two aperture suggest that the evolution of aperture structure in pollen grains were significantly correlated with helo- the angiosperms may be quite complex, where polli- phytic habitats. This finding provides support that habitat nation syndrome likely imposes an important selective moisture may provide a selective pressure affecting the pressure on this pollen character in some nitrogen- evolution of pollen morphology not only in monocots, but fixing taxa. also in other angiosperm taxa (Luo et al., 2015). Colpate ectoaperture is the plesiomorphic state in the A shift from equatorial to global apertures has pre- basal angiosperms, monocots, basal eudicots, and the viously been considered to be an evolutionary trend superasteridaes and is not an exception in the nitrogen- for angiosperm pollen (reviewed by Van Campo, 1976; fixing clade (Lu et al., 2015; Luo et al., 2015; M. Y. Furness & Rudall, 2004). In our study, this trend was Zhang et al., 2017; Yu et al., 2018). However, we found found to occur within the Cucurbitaceae on the branch a shift from colpate to porate ectoaperture under CHB in subtending Cucurbita–Tecunumania Standl. & Steyerm. more than 20 branches in the nitrogen-fixing clade. (under all models). While increases in aperture number, Although the plesiomorphic state of endoaperture shape from the three equatorial apertures of eudicots, may be was inapplicable data under CFP, DFP, and DML, it associated with a shift to globally positioned apertures was circular under CHB and DHB in the nitrogen-fixing in this family, other shifts from equatorial to global clade, and the number of state changes was the second apertures also appeared on other branches within highest under CHB. These results suggest that for both the nitrogen-fixing clade. For example, shifts were the ecto- and endoaperture state, the nitrogen-fixing detected in the Polygalaceae, Polygala–Comesperma– clade represents a significant change in pollen mor- Heterosamara (under CHB and DHB); the Fabaceae, on phology compared to other angiosperm clades. Further- the branch subtending Cranocarpus–Dalbergia (under more, we found that insect pollination is significantly CHB and DHB); the Juglandaceae, on the branch leading correlated with colpate ectoaperture as well as lalongate to Annamocarya–Platycarya–Cyclocarya–Pterocarya– and lolongate endoaperture, while porate ectoaperture Carya–Juglans (under CHB and DHB); the Cucurbita- and circular endoaperture are correlated with wind ceae, on the branch subtending Cucurbiteae–Benincaseae pollination. Coupled with the endo- and ectoaperture (under CHB and DHB); and the Moraceae, on the branch character state changes observed in our study, these leading to Brosimum–Dorstenia. Our results indicate that results suggest that pollen aperture system may also be patterns in aperture position shifts in the nitrogen-fixing less influenced by phylogenetic history and more af- clade are similar to those found in the basal eudicots, fected by pollination syndrome, providing a plausible suggesting that selection pressures on aperture position is explanation for the selection of character states in the relatively conserved across the angiosperm phylogeny. nitrogen-fixing clade. The plesiomorphic state of aperture structure is compound in the nitrogen-fixing clade, compared to Surface sculpture the plesiomorphy of a simple aperture in the basal Previous studies have demonstrated correlations be- eudicots (M. Y. Zhang et al., 2017). Harley (2004) tween pollen morphological features and pollination and Furness (2007) showed that compound apertures syndrome (Lee, 1978; Stroo, 2000; Banks & Rudall, do not exist in monocots or in the basal angiosperms, but 2016). Within the nitrogen-fixing clade, both presence/

absence and shape of supratectal elements and tectum clade, with the character changing frequently as seen sculpture were inferred to have changed state more than in previous studies (Lu et al., 2015; Luo et al., 2015; 20 times (under CHB). Fabaceae, in particular, showed M.Y. Zhang et al., 2017). There is no obvious in- the high diversity and the highest frequency of state creasing or decreasing trend in pollen size within or change in tectum sculpture among all sampled charac- across the clade. It has been suggested that the pres- ters. Interestingly, this family is characterized by a di- ence of (very) large pollen may be associated with versity of pollination syndromes, including pollination specialist pollinators (Van der Ham et al., 2010; by generalist bees (the most common pollinators) and Schaefer & Renner, 2011a). We do find here, for other insects (such as butterflies, beetles, and moths) example, that within Cucurbitaceae, Gurania (Schltdl.) (Ferguson & Skvarla, 1982), vertebrates (birds, bats, Cogn. and Psiguria Neck. ex Arn. (tetrad diameter 5 and primates) (Arroyo, 1981; Ferguson & Skvarla, 1982), 49–100 mm) are butterfly- or hummingbird-pollinated, and anemophily (Lewis et al., 2000; Banks & Rudall, and Calycophysum Triana and Cayaponia Silva Manso 2016). In Papilionoideae, pollen-epihydrophilous spe- (pollen size 5 61–208 mm) are bat-pollinated (Van der cies show adaptive convergence in pollen exine sculpture Ham et al., 2010). Although no significant trends were as a result of sharing the same pollination mechanism found in our study with regards to pollen size and (Ferguson & Skvarla, 1982). In Cucurbitaceae, which pollination syndrome, we did find that vines were also display high pollen diversity and character state strongly correlated with non-small pollen size in our change frequency in tectum sculpture (character 16), we data matrix and that plant growth form is correlated note a transition from striate (i.e., in Actinostemma Griff.) with pollen size, which also has been revealed by to reticulate (i.e., in Thladiantha Bunge) that is concor- M. Y. Zhang et al. (2017). dant with a transition from unspecialized pollinators (honeybees) to those that are specialist such as oil bees CONCLUSIONS AND FUTURE PROSPECTS (Renner & Schaefer, 2010; Van der Ham et al., 2010). The frequency of surface sculpture state change is lower In general, the nitrogen-fixing clade displays high in Fagales, which are mostly wind pollinated. The pollen pollen diversity, in particular within Fabaceae and exine of wind-pollinated taxa such as Betulaceae, Notho- Cucurbitaceae. Highly variable characters include pol- fagaceae, and Myricaceae in our study is generally len size, endoaperture shape, and tectum sculpture. scabrate and relatively thin, with a uniformly thick sexine Twelve plesiomorphic states have been inferred un- composed of a 2-layered (homogeneous/granular) tectum ambiguously for the clade as a whole, and more than 40 and distinct columellae. In addition, wind pollination was lineages at or above familial level are characterized by strongly correlated with taxa in which pollen had gem- unambiguous pollen character state changes in at least mate or echinate supratectal element and imperforate one of the five analyses. Pollen character state changes tectum. Collectively, these results indicate that the view therefore provide systematic insights for diagnosing of wind-pollinated taxa having exclusively smooth pollen some lineages. Furthermore, the correlation between grains is oversimplified (Hesse, 2000). pollen characters and their potential ecological factors indicate that pollination types are potentially a major Shape and size driver of pollen character evolution in the nitrogen- fixing clade. Although more extant and fossil pollen In the nitrogen-fixing clade, subspheroidal shape was morphological data may better facilitate our understand- inferred as the plesiomorphic state, with derived states ing of pollen morphological evolution and diversifica- including oblate, prolate, and perprolate, a trend rep- tion, a more robust phylogenetic framework for the licated in other eudicot groups such as basal eudicots nitrogen-fixing clade based on increased genetic data (M. Y. Zhang et al., 2017) and Superasteridae (Yu et al., and deeper taxon sampling may also be required for 2018). In basal eudicots, M. Y. Zhang et al. (2017) future pollen character optimization, with particular found that tests of correlated evolution suggest that emphasis on large families with high pollen diversity, the herbaceous growth form is significantly associated such as Fabaceae and Cucurbitaceae. with (sub-)spheroidal pollen shape and the arborescent growth form with oblate pollen shape. In the nitrogen-fixing clade, however, we found that prolate Literature Cited shape was correlated with insect pollination. To Abu-Hammour, K. & D. Wittmann. 2010. Pollination and our knowledge, this relationship has not been pre- pollinators of Cucurbita pepo (Cucurbitaceae) in the Jordan viously discussed and should be considered in future Valley to improve seed set. Advances Hort. Sci. 24: studies. 249–256. In terms of size, medium pollen grain size was found Aftab, R. & A. Perveen. 2006. A palynological study of some to be the plesiomorphic state in the nitrogen-fixing cultivated trees from Karachi. Pakistan J. Bot. 38: 15–28.

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Appendix 1. Voucher details for pollen samples shown in Figures 2–9.

Taxon Collection Locality Herbarium Figure Acacia concinna (Willd.) DC. (Fabaceae) 08CS542 Yunnan, China KUN 2A–D Bauhinia brachycarpa Wall. ex Benth. APE007 Kunming Botanic Garden KUN 2E–H (Fabaceae) (cultivated) Caesalpinia minax Hance (Fabaceae) XTBG001 Yunnan, China XTBG 2I–L Mimosa pudica L. (Fabaceae) SCSB-A-029 Yunnan, China KUN 3A*–D* Polygala arillata Buch.-Ham. ex D. Don HeHJ0014 Kunming Botanic Garden KUN 3E–H (Polygalaceae) (cultivated) Shepherdia canadensis (L.) Nutt. NC91-74 s. loc. E 3I–L (Elaeagnaceae) Pilea verrucosa Killip. (Urticaceae) WuZY-10367 Yunnan, China KUN 4A*, B* Ficus tikoua Bureau (Moraceae) APE004 Kunming Botanic Garden KUN 4C*, D* (cultivated) Nothofagus dombeyi (Mirb.) Oersted H. F. Coubes 812 Lago Lolog, Aeaev TINA CANB 4E*–H* (Nothofagaceae) Chrysolepis sempervirens (Kellogg) Hjelmq. S. M. Kaune 560 California, U.S.A. E 4I–L (Fagaceae) Quercus augustinii Skan (Fagaceae) APE025 Yunnan, China KUN 5A–D Allocasuarina diminuta L. A. S. Johnson I. R. Telford 6833 Australian New CANB 5E–H (Casuarinaceae) South Wales, South Coast Alnus nepalensis D. Don (Betulaceae) JDNR09094 Yunnan, China KUN 5I*–L* Myrica esculenta Buch.-Ham. ex D. Don 1797 Yunnan, China KUN 6A, B (Myricaceae) Rhoiptelea chiliantha Diels & Hand.-Mazz. 3206 Yunnan, China KUN 6C, D (Juglandaceae) Juglans mandshurica Maxim. (Juglandaceae) ShuiYM 93.4.2 Yunnan, China KUN 6E–H Coriaria sinica Maxim. (Coriariaceae) MY326 Sichuan, China KUN 6I–L Corynocarpus laevigatus J. R. Forst. & G. Forst. F. J. Breteler 13605 Australian New Zealand, CANB 7A–D (Corynocarpaceae) North Island Cucurbita pepo L. (Cucurbitaceae) HeHJ0013 Kunming Botanic Garden KUN 7E–H (cultivated) Dendrosicyos socotranus Balf. f. A. R. Smith & Socotra E 7I–L (Cucurbitaceae) J. Lavranos 299-71411967 Lagenaria siceraria (Molina) Standl. 09342 Kunming Botanic Garden KUN 8A–D (Cucurbitaceae) (cultivated) Marah macrocarpa Greene (Cucurbitaceae) C. B. Wolf 1829 s. loc. E 8E–H Begonia cucurbitifolia C. Y. Wu (Begoniaceae) HeHJ0052 Kunming Botanic Garden KUN 8I–L (cultivated) Hillebrandia sandwicensis Oliv. (Begoniaceae) O. Degeuer 9766 s. loc. E 9A–D Datisca cannabina L. (Datiscaceae) Davis 44860 Ezp Gorge, Hzkkvi, Turkey E 9E–H Tetrameles nudiflora R. Br. (Tetramelaceae) W. Jiang 0125 Xishuangbanna Tropical XTBG 9I–L Botanical Garden (cultivated)

*Images obtained without acetolysis.

Appendix 2. Genus names and Genbank accession numbers.

Family Species matK rbcL trnL-F Ingroups Anisophylleaceae Anisophyllea corneri Ding Hou AY968444 AF027109 AY968559 Anisophylleaceae Combretocarpus rotundatus (Miq.) Danser AY968447 AF127698 AY968561 Barbeyaceae Barbeya oleoides Schweinf. JF317418 U60314 — Begoniaceae Begonia poculifera Hook. f. GU397108 — JN133338

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Appendix 2. Continued.

Family Species matK rbcL trnL-F Begoniaceae Hillebrandia sandwicensis Oliv. GU397085 — AY968564 Betulaceae Alnus japonica (Thunb.) Steud. AB038176 FJ844577 AY211427 Betulaceae Betula platyphylla Sukaczev AY372023 AY263927 AY147068 Betulaceae Carpinus betulus L. AJ417513 AY263928 AY211398 Betulaceae Corylus avellana L. AY373441 AY263929 AY147072 Betulaceae Ostrya virginiana (Mill.) K. Koch AB015460 HQ590198 AY211425 Betulaceae Ostryopsis davidiana Decne. AB015461 AF081515 AY147071 Cannabaceae Aphananthe aspera (Thunb.) Planch. AF345320 AF500339 AF501594 Cannabaceae Celtis sinensis Pers. AF345316 HQ427254 — Cannabaceae Chaetachme aristata Planch. JF270688 D86310 — Cannabaceae Gironniera subaequalis Planch. AF345319 AF500340 — Cannabaceae Humulus lupulus L. AY257528 AF206777 AF501599 Cannabaceae Trema micrantha (L.) Blume GQ982115 U03844 AY488708 Casuarinaceae Allocasuarina verticillata (Lam.) L. A. S. Johnson AY191657 X69527 — Casuarinaceae Casuarina equisetifolia L. AB015462 AY263930 AY147090 Casuarinaceae Gymnostoma webbianum (Miq.) L. A. S. Johnson AY191680 X69531 — Coriariaceae Coriaria sarmentosa G. Forst. AB016464 AF149000 AY968381 Corynocarpaceae Corynocarpus laevigatus J. R. Forst. & G. Forst. NC014807 NC014807 NC014807 Cucurbitaceae Abobra tenuifolia (Gillies) Cogn. DQ536629 AF008961 — Cucurbitaceae Actinostemma tenerum Griff. DQ536631 DQ535779 — Cucurbitaceae Alsomitra macrocarpa (Blume) M. Roem. DQ536632 DQ535780 — Cucurbitaceae Ampelosycios humblotii (Cogn.) Jum. & H. Perrier DQ521608 DQ501254 — Cucurbitaceae Baijiania yunnanensis (A. M. Lu & Zhi Y. Zhang) DQ469138 DQ501258 — A. M. Lu & J. Q. Li Cucurbitaceae Bayabusua clarkei (King) W. J. de Wilde DQ536635 DQ535741 — Cucurbitaceae Benincasa hispida (Thunb.) Cogn. DQ536636 AY862549 — Cucurbitaceae Borneosicyos simplex W. J. de Wilde DQ536638 DQ535785 DQ535869 Cucurbitaceae Bryonia dioica Jacq. DQ536641 DQ535786 EU102368 Cucurbitaceae Ceratosanthes palmata (L.) Urb. DQ536646 DQ535788 — Cucurbitaceae Cogniauxia podolaena Baill. DQ536653 DQ535794 — Cucurbitaceae Cucumeropsis mannii Naudin EU436402 GU799534 — Cucurbitaceae Cucumis melo L. JF412791 JF412791 HM597025 Cucurbitaceae Cucurbita ecuadorensis H. C. Cutler & Whitaker HQ438598 HQ438630 HQ438676 Cucurbitaceae Cucurbitella asperata (Gillies ex Hook. & Arn.) Walp. — DQ535748 — Cucurbitaceae Cyclanthera brachystachya (Ser.) Cogn. DQ536667 DQ535749 — Cucurbitaceae Cyclantheropsis parviflora (Cogn.) Harms EF634361 EF634363 EF634364 Cucurbitaceae Dendrosicyos socotranus Balf. f. AY973018 AY973022 — Cucurbitaceae Diplocyclos palmatus (L.) C. Jeffrey DQ536671 AY862552 — Cucurbitaceae Ecballium elaterium (L.) A. Rich. AY973019 AF534746 EU102416 Cucurbitaceae Echinocystis lobata (Michx.) Torr. & A. Gray AY491653 DQ535809 — Cucurbitaceae Fevillea pergamentacea Cogn. DQ536679 DQ535813 — Cucurbitaceae Gerrardanthus grandiflorus Gilg ex Cogn. GQ163343 DQ535805 — Cucurbitaceae Gurania (Schltdl.) Cogn. sp. FJ037901 FJ038016 FJ039220 Cucurbitaceae Gymnopetalum chinense (Lour.) Merr. EU155606 EU155601 EU155630 Cucurbitaceae Gynostemma pentaphyllum (Thunb.) Makino AY968451 AY968523 — Cucurbitaceae Helmontia leptantha (Schltdl.) Cogn. — DQ535757 DQ521607 Cucurbitaceae Hemsleya heterosperma (Wall.) C. Jeffrey DQ536686 DQ535817 — Cucurbitaceae Herpetospermum pedunculosum (Ser.) C. B. Clarke DQ536687 DQ535818 — Cucurbitaceae Hodgsonia heteroclita (Roxb.) Hook. f. & Thomson EU155607 — EU155631 Cucurbitaceae Kedrostis africana (L.) Cogn. DQ536692 AJ235782 — Cucurbitaceae Lagenaria breviflora (Benth.) Roberty AY935934 AY935747 AY968570 Cucurbitaceae Luffa acutangula (L.) Roxb. DQ536695 DQ535826 — Cucurbitaceae Marah fabacea (Naudin) Greene AY968453 AY968524 AY968571 Cucurbitaceae Melancium campestre Naudin GU799545 GU799537 — Cucurbitaceae Momordica cochinchinensis (Lour.) Spreng. GQ163378 EF487554 EF487577 Cucurbitaceae Nothoalsomitra suberosa (F. M. Bailey) I. Telford DQ536709 DQ535762 —

Appendix 2. Continued.

Family Species matK rbcL trnL-F Cucurbitaceae Papuasicyos papuanus (Cogn.) Duyfjes EU590121 EU590122 EU590123 Cucurbitaceae Peponium vogelii (Hook. f.) Engl. HQ608272 DQ535835 — Cucurbitaceae Psiguria bignoniacea (Poepp. & Endl.) Wunderlin FJ037900 FJ038017 FJ039219 Cucurbitaceae Schizocarpum palmeri Cogn. & Rose DQ536725 DQ535769 — Cucurbitaceae Schizopepon bryoniifolius Maxim. AY968456 AY973025 — Cucurbitaceae Sicydium tamnifolium (Kunth) Cogn. DQ536731 DQ535846 — Cucurbitaceae Sicyos angulatus L. DQ536732 AY862554 — Cucurbitaceae Siolmatra brasiliensis (Cogn.) Baill. DQ536735 DQ535849 — Cucurbitaceae Siraitia grosvenorii (Swingle) C. Jeffrey ex A. M. Lu & DQ536736 DQ535850 — Z. Y. Zhang Cucurbitaceae Solena heterophylla Lour. DQ536737 DQ535851 — Cucurbitaceae Tecunumania quetzalteca Standl. & Steyerm. DQ536738 DQ535852 — Cucurbitaceae Trichosanthes villosa Blume EU037007 EU037005 EU037008 Cucurbitaceae Xerosicyos danguyi Humbert AY968459 AY973026 AY968573 Cucurbitaceae Zehneria anomala C. Jeffrey EU541412 EU541411 EU541413 Datiscaceae Datisca glomerata (C. Presl) Baill. AY968449 L21940 AY968567 Dirachmaceae Dirachma socotrana Schweinf. ex Balf. f. JF317423 AJ225789 — Elaeagnaceae Elaeagnus umbellata Thunb. AY257529 HM849968 HM769678 Elaeagnaceae Hippophae rhamnoides L. subsp. sinensis Rousi JF317428 JF317488 GU561430 Elaeagnaceae Shepherdia canadensis (L.) Nutt. — U17039 GQ245525 Fabaceae Acacia schweinfurthii Brenan & Exell AF523101 JF265257 AF522979 Fabaceae Adenanthera pavonina L. AF521808 — AF278486 Fabaceae Albizia kalkora (Roxb.) Prain AF523083 HQ427141 AF522945 Fabaceae Aldina latifolia Spruce ex Benth. — U74252 — Fabaceae Alysicarpus ovalifolius (Schumach.) J. L´eonard — JN628036 — Fabaceae Amorpha fruticosa L. AF270861 U74212 AF208899 Fabaceae Anadenanthera colubrina (Vell.) Brenan EU812064 — AF278481 Fabaceae Anthyllis vulneraria L. JN894822 JN892206 HQ323827 Fabaceae Astragalus adsurgens Pall. HM142258 EF685984 AF126980 Fabaceae Augouardia letestui Pellegr. EU361862 — AF365164 Fabaceae Baphia massaiensis Taub. AF142683 U74196 AF309860 Fabaceae Bauhinia galpinii N. E. Br. EU361875 AM234262 — Fabaceae Bocoa prouacensis Aubl. FJ037904 FJ038032 FJ039261 Fabaceae Brenierea insignis Humbert EU361889 AM234269 AF365060 Fabaceae Browneopsis ucayalina Huber EU361894 AM234233 AF365199 Fabaceae Burkea africana Hook. EU361895 JF265317 EU361755 Fabaceae Caesalpinia calycina Benth. EU361899 AM234236 AY899691 Fabaceae Cajanus cajan (L.) Huth EU717414 EU717273 — Fabaceae Calopogonium caeruleum (Benth.) C. Wright — AF308723 — Fabaceae Camptosema coccineum (Mart. ex Benth.) Benth. ——FJ613485 Fabaceae Campylotropis macrocarpa (Bunge) Rehder EU717418 EU717277 — Fabaceae Canavalia rosea (Sw.) DC. HQ707517 AB045793 — Fabaceae Caragana arborescens Lam. AF142737 FJ537211 DQ311691 Fabaceae Ceratonia siliqua L. EU361911 U74203 AF365075 Fabaceae Cercis canadensis L. EU361912 U74188 AF365054 Fabaceae Chamaecrista nictitans (L.) Moench EU361914 GQ248565 — Fabaceae Cicer arietinum L. EU835853 EU835853 DQ315487 Fabaceae Clathrotropis brachypetala (Tul.) Kleinhoonte ——AF309827 Fabaceae Collaea argentina Griseb. ——FJ613490 Fabaceae Colophospermum mopane (J. Kirk ex Benth.) EU361915 JF265343 AF365165 J. L´eonard Fabaceae Cordyla africana Lour. JF270724 U74204 — Fabaceae Coronilla varia L. — U74222 — Fabaceae Cranocarpus martii Benth. AF270875 AB045796 AF208951 Fabaceae Crotalaria trichotoma Bojer HM049507 GQ436334 — Fabaceae Crudia gabonensis Pierre ex Harms EU361922 AM234230 AF365172

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Appendix 2. Continued.

Family Species matK rbcL trnL-F Fabaceae Cyathostegia matthewsii (Benth.) Schery HM347487 — AF309841 Fabaceae Cyclolobium nutans Rizzini & Heringer AF142686 — AF309857 Fabaceae Dalbergia sissoo Roxb. ex DC. AF203582 GU135159 EF451118 Fabaceae Dalea wrightii A. Gray AY391802 —— Fabaceae Daviesia latifolia R. Br. AY386887 —— Fabaceae Delonix elata (L.) Gamble EU361928 AM234235 AY899731 Fabaceae Desmanthus bicornutus S. Watson AF523108 — AF522939 Fabaceae Desmodium pauciflorum (Nutt.) DC. EU717421 EU717280 — Fabaceae Dinizia excelsa Ducke AF521827 — AF278479 Fabaceae Dioclea reflexa Hook. f. HQ707540 —— Fabaceae Diptychandra aurantiaca Tul. EU361935 — AF309478 Fabaceae Dolichos oliveri Schweinf. JN008183 —— Fabaceae Dumasia villosa DC. EU717406 EU717265 — Fabaceae Duparquetia orchidacea Baill. EU361937 — EU361800 Fabaceae Eperua falcata Aubl. EU361945 FJ038036 FJ039125 Fabaceae Erythrina sousae Krukoff & Barneby EU717411 EU717270 — Fabaceae Erythrophleum ivorense A. Chev. EU361948 U74205 AF365102 Fabaceae Exostyles venusta Schott ex Spreng. ——AF309838.2 Fabaceae Galega orientalis Lam. AF522083 — DQ311694 Fabaceae Genista monspessulana (L.) L. A. S. Johnson AY386862 HM850024 JF338274 Fabaceae Gigasiphon macrosiphon (Harms) Brenan EU361953 — EU361810 Fabaceae Glycine max (L.) Merr. DQ317523 DQ317523 DQ131547 Fabaceae Glycyrrhiza lepidota Pursh AF142730 AB126685 AF124238 Fabaceae Hedysarum vicioides Turcz. HM142267 U74246 — Fabaceae Holocalyx balansae Micheli AY553714 U74244 EF466269 Fabaceae Indigofera fulgens Baker JF270831 JF265484 — Fabaceae Inga edulis Mart. AF523078 FJ173737 AF522957 Fabaceae Jacqueshuberia brevipes Barneby EU361984 — EU361815 Fabaceae Lecointea peruviana Standl. ex J. F. Macbr. EU361990 AM234260 AF365039 Fabaceae Leucaena leucocephala (Lam.) de Wit AY574102 GU135204 AF522942 Fabaceae Lotus japonicus (Regel) K. Larsen NC002694 NC002694 NC002694 Fabaceae Macrotyloma uniflorum (Lam.) Verdc. EU717410 EU717269 — Fabaceae Medicago lupulina L. HM159569 AY395551 JQ041869 Fabaceae Microlobius foetidus (Jacq.) M. Sousa & G. Andrade AF523095 — AF522960 Fabaceae Mildbraediodendron excelsum Harms ——AF309847 Fabaceae Millettia pinnata (L.) Panigrahi NC016708 NC016708 NC016708 Fabaceae Mimosa pigra L. GU135076 GU135239 DQ344560 Fabaceae Mora gonggrijpii (Kleinhoonte) Sandwith EU362005 — AF365104 Fabaceae Mucuna Adans. sp. EU717422 EU717281 — Fabaceae Neptunia monosperma F. Muell. ex Benth. AF523090 — AF522944 Fabaceae Ormosia macrocalyx Ducke GQ982056 GQ981822 — Fabaceae Ornithopus compressus L. AF142727 HM850215 — Fabaceae Oxystigma msoo Harms EU362011 — AF365168 Fabaceae Pachyelasma tessmannii (Harms) Harms EU362013 — AF365105 Fabaceae Parapiptadenia rigida (Benth.) Brenan AF521849 — AF278505 Fabaceae Peltophorum pterocarpum (DC.) Backer ex K. Heyne EU362023 AM234243 AY899713 Fabaceae Pentaclethra macrophylla Benth. AF521853 AM234250 AF278485 Fabaceae Phanera outimouta (Aubl.) L. P. Queiroz EU361877 — EU361745 Fabaceae Phyllodium pulchellum (L.) Desv. HM049524 —— Fabaceae Piliostigma thonningii (Schumach.) Milne-Redh. — JF265551 FJ801153 Fabaceae Piptadeniopsis lomentifera Burkart AY944559 —— Fabaceae Poeppigia procera C. Presl EU362026 AM234246 AY899682 Fabaceae Prioria copaifera Griseb. EU362030 — AF365171 Fabaceae Psoralea cinerea Lindl. AF142699 —— Fabaceae Pueraria phaseoloides (Roxb.) Benth. EU717404 EU717263 — Fabaceae Robinia pseudoacacia L. AF142728 U74220 AF529391

Appendix 2. Continued.

Family Species matK rbcL trnL-F Fabaceae Senna alata (L.) Roxb. EU362042 U74250 AF365091 Fabaceae Sophora flavescens Aiton HM049520 AB127037 AB127029 Fabaceae Spatholobus parviflorus (Roxb.) Kuntze EU106113 AB045825 — Fabaceae Swartzia cardiosperma Spruce ex Benth. EU362053 AM234259 AF365040 Fabaceae Teleseme fassoglensis (Schweinf.) Torre & Hillc. EU361874 — EU361743 Fabaceae Trifolium burchellianum Ser. AF522118 AM235018 DQ311759 Fabaceae Ulex minor Roth HM851133 HM850432 AF385419 Fabaceae Umtiza listeriana Sim EU362062 AM234237 AF365126 Fabaceae Vaughania perrieri (R. Vig.) Du Puy, Labat & Schrire ——AF274372 Fabaceae Vicia villosa Roth AF522161 HM850464 DQ311955 Fabaceae Vigna unguiculata (L.) Walp. AY589510 EU717266 GQ411554 Fabaceae Wisteria sinensis (Sims) DC. AF142732 Z95544 — Fabaceae Xylia torreana Brenan JF271001 JF265660 — Fabaceae Zapoteca tetragona (Willd.) H. M. Hern. AF523097 — AF522966 Fabaceae Zollernia splendens Wied-Neuw. & Nees ——AF311372 Fagaceae Castanea crenata Siebold & Zucc. AB107636 AB060565 AF344181 Fagaceae Castanopsis fissa (Champ. ex Benth.) Rehder & FJ185053 JF941177 EF057141 E. H. Wilson Fagaceae Chrysolepis sempervirens (Kellogg) Hjelmq. U92863 AF206750 — Fagaceae Colombobalanus excelsa (Lozano, Hern. Cam. & AY042456 —— Henao) Nixon & Crepet Fagaceae Fagus crenata Blume AB046496 AB060567 AF533693 Fagaceae Formanodendron doichangensis (A. Camus) FJ185046 —— Nixon & Crepet Fagaceae Lithocarpus henryi (Seemen) Rehder & EF057119 AY147097 AY147086 E. H. Wilson Fagaceae Quercus robur L. AJ491718 AB125025 AF268937 Fagaceae Trigonobalanus verticillata Forman AB084770 AB084768 AY147085 Juglandaceae Alfaroa williamsii Ant. Molina U92849 —— Juglandaceae Annamocarya sinensis (Dode) J.-F. Leroy AY263919 AY263935 AY147080 Juglandaceae Carya ovata (Mill.) K. Koch U92850 AY263931 AY147074 Juglandaceae Cyclocarya paliurus (Batalin) Iljinsk. AY147098 AY147094 AY147075 Juglandaceae Engelhardia fenzelii Merr. AY147099 AY147095 AY147076 Juglandaceae Juglans mandshurica Maxim. AF118033 AY263932 AY147077 Juglandaceae Platycarya strobilacea Siebold & Zucc. AY147100 AY263933 AY147078 Juglandaceae Pterocarya hupehensis Skan AY263918 AY263934 AY147079 Moraceae Batocarpus costaricensis Standl. & L. O. Williams ——FJ917065 Moraceae Brosimum alicastrum Sw. GQ981947 AF500346 AF501601 Moraceae Dorstenia mannii Hook. f. — AF500349 AF501604 Moraceae Ficus pumila L. HM851109 AF500352 AF501606 Moraceae Helicostylis tomentosa (Poepp. & Endl.) J. F. Macbr. FJ514761 FJ038122 FJ039339 Moraceae Maclura tricuspidata Carri`ere JF317421 JF317480 JN006418 Moraceae Morus rubra L. GU145566 U06812 HM747181 Myricaceae Canacomyrica monticola Guillaumin — DQ310504 — Myricaceae Comptonia peregrina (L.) J. M. Coult. U92856 DQ310505 — Myricaceae Myrica gale L. AY191715 X69530 GQ245142 Nothofagaceae Nothofagus antarctica (G. Forst.) Oerst. AY263924 AY263939 AY147091 Polygalaceae Acanthocladus guayaquilensis B. Eriksen & B. Stahl˚ — AM234190 — Polygalaceae Badiera fuertesii Urb. ——GQ889058 Polygalaceae Barnhartia floribunda Gleason — AM234168 — Polygalaceae Carpolobia alba G. Don EU604053 AM234176 GQ889064 Polygalaceae Comesperma esulifolium (Gand.) Prain EU596516 AM234179 GQ889068 Polygalaceae Heterosamara tatarinowii (Regel) Paiva — AM234208 — Polygalaceae Monnina xalapensis Kunth EU604047 AM234184 GQ889088 Polygalaceae Moutabea aculeata (Ruiz & Pav.) Poepp. & Endl. — AM234169 — Polygalaceae Polygala senega L. EU604034 AM234189 GQ889195

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Appendix 2. Continued.

Family Species matK rbcL trnL-F Polygalaceae Xanthophyllum Roxb. sp. EU604044 AJ235799 — Quillajaceae Quillaja saponaria Molina AY386843 U06822 — Rhamnaceae Adolphia infesta (Kunth) Meisn. — AJ390055 — Rhamnaceae Alphitonia Reissek ex Endl. — AJ390049 — Rhamnaceae Berchemia discolor (Klotzsch) Hemsl. JF270655 AJ225786 — Rhamnaceae Ceanothus sanguineus Pursh AF049815 U06795 — Rhamnaceae Colletia ulicina Gillies & Hook. — U59819 — Rhamnaceae Colubrina asiatica (L.) Brongn. GU135023 AJ390047 — Rhamnaceae Crumenaria erecta Reissek — AJ390042 — Rhamnaceae Gouania mauritiana Lam. JF317427 AJ390040 — Rhamnaceae Hovenia trichocarpa Chun & Tsiang var. robusta JF317429 JF317489 — (Nakai & Y. Kimura) Y. L. Chen & P. K. Chou Rhamnaceae Karwinskia humboldtiana (Schult.) Zucc. — AJ390031 — Rhamnaceae Lasiodiscus mildbraedii Engl. — AJ390050 — Rhamnaceae Maesopsis eminii Engl. — AJ390034 — Rhamnaceae Noltea africana (L.) Endl. — AJ390054 AY460407 Rhamnaceae Phylica arborea Thouars GQ248177 GQ248666 AF327603 Rhamnaceae Pomaderris rugosa Cheeseman — AJ390063 — Rhamnaceae Reissekia smilacina (Sm.) Steud. — AJ390041 — Rhamnaceae Retanilla patagonica (Speg.) Tortosa ——AY460424 Rhamnaceae Reynosia uncinata Urb. — AJ390029 — Rhamnaceae Rhamnidium elaeocarpum Reissek — AJ390030 — Rhamnaceae Rhamnus cathartica L. AY257533 L13189.2 — Rhamnaceae Sageretia thea (Osbeck) M. C. Johnst. — AJ225785 — Rhamnaceae Schistocarpaea johnsonii F. Muell. — AJ390046 — Rhamnaceae Scutia buxifolia Reissek — AJ390033 — Rhamnaceae Ziziphus jujuba Mill. GQ434248 GQ436666 — Rhoipteleaceae Rhoiptelea chiliantha Diels & Hand.-Mazz. U92852 AF017687 AY147081 Rosaceae Acaena latebrosa W. T. Aiton EU914270 — AY634702 Rosaceae Alchemilla glabra Neygenf. JN894582 JN891525 — Rosaceae Armeniaca zhenghensis J. Y. Zhang & M. N. Lu JF955833 —— Rosaceae Bencomia caudata (Aiton) Webb & Berthel. ——AY634719 Rosaceae Chaenomeles cathayensis (Hemsl.) C. K. Schneid. DQ860453 JQ391326 DQ863225 Rosaceae Cotoneaster pannosus Franch. AF288098 JQ391291 AF348540 Rosaceae Dichotomanthes tristaniicarpa Kurz DQ860460 JQ391335 DQ863232 Rosaceae Dryas octopetala L. JF317424 JF317483 DQ860555 Rosaceae Duchesnea indica (Andrews) Focke HM850689 HM850286 — Rosaceae Exochorda racemosa (Lindl.) Rehder AF288100 — AF348542 Rosaceae Filipendula vulgaris Moench JN894238 JN891051 — Rosaceae Fragaria vesca L. AF288102 HM850009 AF348545 Rosaceae Geum rivale L. JN895978 JN893446 HM590295 Rosaceae Hagenia abyssinica (Bruce) J. F. Gmel. ——AY634727 Rosaceae Holodiscus discolor (Pursh) Maxim. AF288105 U06807 AF348546 Rosaceae Kerria japonica (L.) DC. AB073686 DQ250749 — Rosaceae Leucosidea sericea Eckl. & Zeyh. EU914265 — AY634728 Rosaceae Malus sargentii Rehder DQ860466 JQ391365 DQ863238 Rosaceae Margyricarpus pinnatus (Lam.) Kuntze ——AY634730 Rosaceae Neillia thibetica Bureau & Franch. JF317430 JF317490 AF487227 Rosaceae Oemleria cerasiformis (Torr. & A. Gray) AF288110 — AF348551 J. W. Landon Rosaceae Photinia parvifolia (E. Pritz.) C. K. Schneid. HQ427355 HQ427206 — Rosaceae Physocarpus insularis (Nakai) Nakai GU217789 GU217791 GU217792 Rosaceae Potentilla anserina L. AF288113 JN893482 AF348556 Rosaceae Prunus laurocerasus L. AF288116 U06809 AF348559 Rosaceae Pygeum topengii Merr. DQ851230 —— Rosaceae Pyrus communis L. DQ860473 JQ391382 DQ863245

Appendix 2. Continued.

Family Species matK rbcL trnL-F Rosaceae Rosa woodsii Lindl. EU025926 U06824 DQ778893 Rosaceae Sanguisorba officinalis L. AB073696 AY395560 AY634774 Rosaceae Sarcopoterium spinosum (L.) Spach ——AY634777 Rosaceae Sorbaria sorbifolia (L.) A. Braun AF288125 GQ436611 AF348569 Rosaceae Sorbus aucuparia L. JN896162 HQ590284 AF327596 Rosaceae Stranvaesia davidiana Decne. DQ860476 JQ391397 DQ863248 Surianaceae Cadellia pentastylis F. Muell. EU604056 L29491 — Surianaceae Guilfoylia monostylis (Benth.) F. Muell. EU604031 L29494 — Surianaceae Recchia mexicana Moc. & Sessé ex DC. EU604045 AM234270 — Surianaceae Stylobasium spathulatum Desf. EU604032 U06828 — Surianaceae Suriana maritima L. AY386950 U07680 — Tetramelaceae Octomeles sumatrana Miq. AY968455 L21942 AY968574 Tetramelaceae Tetrameles nudiflora R. Br. AY968458 AF206828 — Ticodendraceae Ticodendron incognitum Gómez-Laur. & AB015463 AF061197 AY147073 L. D. Gómez Ulmaceae Ampelocera hottlei (Standl.) Standl. — AF500335 AF501592 Ulmaceae Hemiptelea davidii (Hance) Planch. AF345322 AF500336 — Ulmaceae Zelkova serrata (Thunb.) Makino AB572557 AF206835 — Urticaceae Boehmeria macrophylla Hornem. var. scabrella JF317436 JF317496 — (Roxb.) D. G. Long Urticaceae Cecropia obtusifolia Bertol. GQ981958 GQ981694 DQ179377 Urticaceae Coussapoa ovalifolia Trécul ——AF501616 Urticaceae Cypholophus macrocephalus (Blume) Wedd. ——FJ432254 Urticaceae Droguetia ambigua Wedd. — AM235161 — Urticaceae Elatostema parvum (Blume) Blume ex Miq. — AY208703 AY208733 Urticaceae Laportea canadensis (L.) Wedd. AY257537 AF500356 — Urticaceae Lecanthus peduncularis (Wall. ex Royle) Wedd. ——DQ179370 Urticaceae Maoutia puya (Hook.) Wedd. ——FJ432259 Urticaceae Parietaria debilis G. Forst. HM851112 HM850235 FJ432256 Urticaceae Pellionia daveauana (Godefroy) N. E. Br. — AF500358 AF501612 Urticaceae Pilea cadierei Gagnep. & Guillaumin JF317431 JF317491 DQ179359 Urticaceae Pipturus argenteus (G. Forst.) Wedd. — JF738411 — Urticaceae Urera baccifera (L.) Gaudich. ex Wedd. HM446752.2 GQ981911 — Urticaceae Urtica dioica L. GU266610 AF500361 AY208725 Outgroups Crossosomataceae Crossosoma bigelovii S. Watson DQ443456 DQ307100 DQ307148 Zygophyllaceae Guaiacum guatemalense Planch., Rydb. & Vail DQ401366 Y15019 EU253461 Melianthaceae Melianthus villosus Bolus JQ479132 JQ479189 JQ581537 Oxalidaceae Oxalis latifolia Kunth EU437339 EU002282 JN639571 Ranunculaceae Ranunculus macranthus Scheele NC008796 NC008796 NC008796 Lepidobotryaceae Ruptiliocarpon caracolito Hammel & N. Zamora AY935918 AJ402997 EU328801

Appendix 3. Literature sources for palynological and ecolog- Oberlander et al., 2009; L´opez & Rosenfeldt, 2016); Ranun- ical data, listed alphabetically by taxon (asterisks indicate culales/Ranunculaceae/Ranunculus L. (Utelli & Roy, ecological literature). 2000*; Culley et al., 2002*; Perveen & Qaiser, 2006; Yang et al., 2006*); Zygophyllales/Zygophyllaceae/Guaiacum L. OUTGROUPS (Aftab & Perveen, 2006; Sheahan, 2007*). Celastrales/Lepidobotryaceae/Ruptiliocarpon Hammel THE NITROGEN-FIXING CLADE & N. Zamora (Link, 1991*; Hammel & Zamora, 1993; Kubitzki, 2004*); Crossosomatales/Crossosomataceae/ Cucurbitales/Anisophylleaceae/Anisophyllea R. Br. ex Crossosoma Nutt. (Culley et al., 2002*; Matthews & Endress, Sabine (Erdtman & Sorsa, 1971; Vezey et al., 1988; Matthews 2005; Sosa, 2007*); Geraniales/Melianthaceae/Melianthus et al., 2001; Schwarzbach & Tomlinson, 2011*); Combreto- L. (Erdtman, 1952; Linder, 2007*); Oxalidales/Oxalida- carpus Hook. f. (Vezey et al., 1988; Matthews et al., 2001; ceae/Oxalis L. (Weller, 1981*; Bernhardt, 1990*; Dreyer & Schwarzbach & Tomlinson, 2011*); Begoniaceae/Begonia L. Van Wyk, 1998; Perveen & Qaiser, 2003; Cocucci, 2004*; (Berg, 1985; Agren˚ & Schemske, 1991*; Schemske et al.,

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1996*; Li et al., 2008; Song & Yang, 2009; Wyatt & Sazima, (Khunwasi, 1998; Schaefer & Renner, 2011*); Momordica 2011*); Hillebrandia Oliv. (Erdtman & Sorsa, 1971; de Wilde, L. (Marticorena, 1963; Zhang & Lu, 1989; Khunwasi, 1998; 2011*); Coriariaceae/Coriaria L. (Garg, 1980; Perveen & Garc´ıa et al., 2003; Oronje et al., 2012*); Nothoalsomitra I. Qaiser, 1998a; Culley et al., 2002*; Kubitzki, 2011a*); Cor- Telford (Khunwasi, 1998; Schaefer & Renner, 2011*); Para- ynocarpaceae/Corynocarpus J. R. Forst. & G. Forst. (Nowicke sicyos Dieterle (Lira, 1994; Khunwasi, 1998; Schaefer & & Skvarla, 1983; Kubitzki, 2011b*); Cucurbitaceae/Abobra Renner, 2011*); Peponium Engl. (Marticorena, 1963; Page Naudin (Khunwasi, 1998; Culley et al., 2002*; Stanghellini & Jeffrey, 1975; Khunwasi, 1998; Pruesapan & Van der Ham, et al., 2002*; Schaefer & Renner, 2011*; Thomas et al., 2005; de Wilde & Duyfjes, 2010*); Psiguria Neck. ex Arn. 2015*); Actinostemma Griff. (Xia et al., 1994; Van der Ham (Murawski, 1987*; Ayala-Nieto et al., 1988; Hampshire, et al., 2010; Schaefer & Renner, 2011*); Alsomitra (Blume) 1992b*; Khunwasi, 1998); Schizocarpum Schrad. (Khunwasi, Spach (Nevkryta, 1937*; Van der Ham, 1999; Van der Ham 1998; Garc´ıa et al., 2003; Schaefer & Renner, 2011*); Schiz- et al., 2010; Schaefer & Renner, 2011a); Ampelosycios Thouars opepon Maxim. (Lu & Zhang, 1985*; Khunwasi, 1998; Akimoto (Marticorena, 1963; Khunwasi, 1998; Pruesapan & Van der et al., 1999; Schaefer & Renner, 2011*); Sicydium Schltdl. Ham, 2005; Duchen & Renner, 2010*; Schaefer & Renner, (Ayala-Nieto et al., 1988; Khunwasi, 1998); Sicyos L. (Khun- 2011a); Baijiania A. M. Lu & J. Q. Li (Zhang & Lu, 1989; de wasi, 1998; Garc´ıa et al., 2003; de Wilde & Duyfjes, 2010*; Wilde & Duyfjes, 2010*; Schaefer & Renner, 2011a); Baya- Lima & Miotto, 2011); Siolmatra Baill. (Khunwasi, 1998; A. P. busua W. J. de Wilde (Van der Ham, 1999; de Wilde & Lima et al., 2010*; Van der Ham et al., 2010); Siraitia Merr. Duyfjes, 2010*; Schaefer & Renner, 2011a); Benincasa Savi (Zhang & Lu, 1989; Khunwasi, 1998; Liu et al., 2010*; Tang (Khunwasi, 1998; Schaefer & Renner, 2011a; Liu et al., et al., 2016*); Solena Lour. (Marticorena, 1963; Khunwasi, 2014*); Borneosicyos W. J. de Wilde (Van der Ham & Van 1998; Perveen & Qaiser, 2008; Schaefer & Renner, 2011*); Heuven, 2003; de Wilde & Duyfjes, 2010*); Bryonia L. (Nepi Tecunumania Standl. & Steyerm. (Khunwasi, 1998; Schaefer & & Lisci, 1996*; Khunwasi, 1998); Ceratosanthes Adans. Renner, 2011*); Trichosanthes L. (Sachan et al., 1990*; Huang (Nevkryta, 1937*; Khunwasi, 1998); Cogniauxia Baill. et al., 1997; Khunwasi, 1998; Pruesapan & Van der Ham, 2005); (Marticorena, 1963; Khunwasi, 1998; de Wilde & Duyfjes, 2010*); Xerosicyos Humbert (Khunwasi, 1998; Schaefer & Renner, Cucumeropsis Naudin (Marticorena, 1963; Khunwasi, 1998; 2011*); Zehneria Endl. (Van der Ham & Pruesapan, 2006; Ndola et al., 2017*); Cucumis L. (Marticorena, 1963; Handel, Schaefer & Renner, 2011*); Datiscaceae/Datisca L. (Davidson, 1983*; Ayala-Nieto et al., 1988; Khunwasi, 1998; Garc´ıa et al., 1973; Culley et al., 2002*; Swensen & Kubitzki, 2011*); 2003; Santos et al., 2008*); Cucurbita L. (Marticorena, 1963; Tetramelaceae/Octomeles Miq. (Erdtman & Sorsa, 1971; Prom- Saad, 1964; Ayala-Nieto et al., 1988; Garc´ıa et al., 2003; Abu- dej, 1994*; Swensen & Kubitzki, 2011*); Tetrameles R. Br. (this Hammour & Wittmann, 2010*; Ashworth & Galetto, 2010*; study; Promdej, 1994*; Swensen & Kubitzki, 2011*). Serra & Campos, 2010*); Cucurbitella Walp. (Marticorena, Fabales/Fabaceae/Acacia Mill. (Sorsa, 1969; Jumah, 1963; Khunwasi, 1998; de Wilde & Duyfjes, 2010*); Cyclan- 1991; Perveen & Qaiser, 1998c*; Caccavari & Dome, 2000; thera Schrad. (Marticorena, 1963; Vogel, 1981*; Stafford & Arce & Banks, 2001; Stone et al., 2003*; Fleming et al., Sutton, 1994; Khunwasi, 1998); Cyclantheropsis Harms 2007*); Adenanthera L. (Sorsa, 1969; Aluri, 2002*; Eynard & (Nevkryta, 1937*; Khunwasi, 1998; de Wilde & Duyfjes, 2010*; Galetto, 2002; Banks et al., 2010); Albizia Durazz. (Sorsa, Van der Ham et al., 2010); Dendrosicyos Balf. f. (Marticorena, 1969; Jumah, 1991; Perveen & Qaiser, 1998c; Lewis et al., 1963; Khunwasi, 1998; Newton, 2004a*; Schaefer & Renner, 2005*); Aldina Endl. (Ferguson & Skvarla, 1991; Lewis et al., 2011*); Diplocyclos (Endl.) T. Post & Kuntze (Nevkryta, 2005*); Alysicarpus Neck. ex Desv. (Chen & Huang, 1993; 1937*; Marticorena, 1963; Khunwasi, 1998; de Wilde & Perveen & Qaiser, 1998b; Pokle, 2018*); Amorpha L. (Ferguson, Duyfjes, 2010*); Ecballium A. Rich. (Marticorena, 1963; 1990; Song, 2007; Linares & Koptur, 2008*); Anadenanthera Khunwasi, 1998; Schaefer & Renner, 2011*); Echinocystis Speg. (Sorsa, 1969; Caccavari, 2002; Buril et al., 2010; Torr. & A. Gray (Nevkryta, 1937*; Stafford & Sutton, 1994; Borges et al., 2017*); Anthyllis L. (D´ıez & Ferguson, 1990; Khunwasi, 1998; de Wilde & Duyfjes, 2010); Fevillea L. Navarro, 2000*); Astragalus L. (Green & Palmbald, 1975*; (Khunwasi, 1998; L. F. P. Lima et al., 2010; Van der Ham Youngguk et al., 2000*; Akan et al., 2005; Pinar et al., 2009; et al., 2010; Schaefer & Renner, 2011*); Gerrardanthus Harv. Ceter et al., 2013; Faraj et al., 2013; Tanner et al., 2013*); ex Benth. & Hook. f. (Khunwasi, 1998; Newton, 2004b*; Van Augouardia Pellegr. (Banks & Gasson, 2000; Banks, 2003; der Ham et al., 2010); Gurania (Schltdl.) Cogn. (Hampshire, Lewis et al., 2005*); Baphia Afzel. ex Lodd. (Soladoye & 1992a*; Khunwasi, 1998); Gymnopetalum Arn. (Khunwasi, Crane, 1985; Lewis et al., 2005*); Bauhinia L. (Heithaus, 1998; Pruesapan & Van der Ham, 2005; de Wilde & Duyfjes, 1974*; Hokche & Ramirez, 1990*; Ferguson & Banks, 1994; 2010*; Van der Ham et al., 2010); Gynostemma Blume Santos et al., 2012; Banks et al., 2013, 2014; Moreira et al., (Nevkryta, 1937*; Khunwasi, 1998; de Wilde et al., 2007; 2013; Matsila & Mokganya, 2017*); Bocoa Aubl. (Ferguson & de Wilde & Duyfjes, 2010*); Helmontia Cogn. (Nevkryta, Skvarla, 1988; Lewis et al., 2005*); Brenierea Humbert (Lewis 1937*; Khunwasi, 1998; de Wilde & Duyfjes, 2010*); Hem- et al., 2005*; Banks et al., 2013, 2014); Browneopsis Huber sleya Cogn. ex F. B. Forbes & Hemsl. (Li, 1990; Khunwasi, (Klitgaard & Ferguson, 1992; Knudsen & Klitgaard, 1998*); 1998; de Wilde et al., 2007; de Wilde & Duyfjes, 2010*); Burkea Hook. (Lewis et al., 2005*; Banks & Lewis, 2009; Herpetospermum Wall. ex Benth. & Hook. f. (Khunwasi, 1998; Banks et al., 2010); Caesalpinia L. (Cruden & Hermannparker, Pruesapan & Van der Ham, 2005; Schaefer & Renner, 2011*); 1979*; Wang et al., 1995; Kim & Song, 1998; Vasudeva, 1999; Hodgsonia Hook. f. & Thomson (Khunwasi, 1998; Pruesapan Correa,ˆ 2003); Cajanus Adans. (Srivastava, 1978; Bhatia et al., & Van der Ham, 2005; Schaefer & Renner, 2011*); Kedrostis 1981*; Chaturvedi & Datta, 2000); Calopogonium Desv. Medik. (Marticorena, 1963; Khunwasi, 1998; de Wilde & (Kavanagh & Ferguson, 1981; Ferguson & Skvarla, 1983; Duyfjes, 2010; Amutha. & Lalitha, 2012*); Lagenaria Ser. Lewis et al., 2005*); Camptosema Hook. & Arn. (Kavanagh (Marticorena, 1963; Keraudren, 1968; Ayala-Nieto et al., & Ferguson, 1981; Lewis et al., 2005*); Campylotropis Bunge 1988; Khunwasi, 1998; Morimoto & Maundu, 2004*; Kumar, (Huang & Ma, 1987; Chen & Huang, 1993; Lewis et al., 2005*; 2005*); Luffa Mill. (Saad, 1964; Ayala-Nieto et al., 1988; Xu et al., 2011); Canavalia Adans. (Stirton, 1977*; Kavanagh Khunwasi, 1998; Mensah & Kudom, 2010*; Bodlah & Waqar, & Ferguson, 1981; Guedes et al., 2009*); Caragana Fabr. 2013*); Marah Kellogg (Stafford & Sutton, 1994; Khunwasi, (Zhang & Tian, 1996; Pi et al., 2016*); Ceratonia L. (Ferguson, 1998; Schaefer & Renner, 2011*); Melancium Naudin 1980; Graham et al., 1980; Dafni et al., 2011*); Cercis L. (Kim

& Song, 1998; Lewis et al., 2005*; Banks et al., 2013, 2014); 2015*, 2017*); Neptunia Lour. (Lewis et al., 2005*; Buril Chamaecrista (L.) Moench (Wolfe & Estes, 1992*; Luz et al., et al., 2010; Bhunia & Mondal, 2012); Ormosia Jacks. (Lewis 2013; Campbell et al., 2018*); Cicer L. (Richards, 1986*; et al., 2005*; de Souza et al., 2014); Ornithopus L. (Wojcie- Chaturvedi et al., 1995); Clathrotropis Harms (Lewis et al., chowska, 1975*; D´ıez & Ferguson, 1996); Oxystigma Harms 2005*; de Souza et al., 2014); Collaea DC. (Kavanagh & (Banks & Gasson, 2000; Omokhua & Ukoimah, 2008*); Ferguson, 1981; Gelvezzúñiga et al., 2016*); Colophospermum Pachyelasma Harms (Lewis et al., 2005*; Banks & Lewis, Kirk ex J. Léonard (Banks & Gasson, 2000; Lewis et al., 2009); Parapiptadenia Brenan (Sorsa, 1969; Caccavari, 2002; 2005*); Cordyla Lour. (Ferguson & Skvarla, 1988; Lewis et al., Lewis, 2005*; Buril et al., 2010); Peltophorum (Vogel) Benth. 2005*); Coronilla L. (D´ıez & Ferguson, 1996; Aronne (Aluri & Reddi, 1996*; Bhattacharya et al., 2015); Penta- et al., 2012*); Cranocarpus Benth. (Harley, 1978*; Ferguson clethra Benth. (Banks et al., 2010; Zukin, 2011*); Phanera & Skvarla, 1979); Crotalaria L. (Gupta & Gupta, 1979; Lour. (Lewis, 2005*; Santos et al., 2012; Banks et al., 2014); Etcheverry et al., 2003*; Bhattacharya et al., 2015); Crudia Phyllodium Desv. (Chen & Huang, 1993; Ye et al., 2011; Schreb. (Banks & Gasson, 2000; Lewis et al., 2005*); Cya- Saisorn & Chantaranothai, 2015); Piliostigma Hochst. (Lewis thostegia (Benth.) Schery (Ferguson & Skvarla, 1988; Lewis et al., 2005*; Banks et al., 2013, 2014); Piptadeniopsis Burkart et al., 2003*); Cyclolobium Benth. (Lewis et al., 2005*; de (Caccavari, 2002; Lewis et al., 2005*); Poeppigia C. Presl Souza et al., 2014); Dalbergia L. f. (Gibbs & Sassaki, 1998*; (,https://www.paldat.org/.; Lewis et al., 2005*); Prioria Silva & Santos, 2009; Vasudeva & Sareen, 2009*; Luz et al., Griseb. (Banks & Gasson, 2000; Lewis et al., 2005*); Psoralea 2013); Dalea L. (Mahler, 1970, 1976; Meeson, 1977; Ferguson, L. (Ferguson & Skvarla, 1983; Perveen & Qaiser, 1998b; Wang 1990; Cane, 2006*; Cane et al., 2012*); Daviesia Sm. et al., 2010*; Fazal et al., 2013); Pueraria DC. (Fu et al., 1996; (Beardsell et al., 1986*; Prenner, 2004); Delonix Raf. (Banks, Perveen & Qaiser, 1998b; Lewis et al., 2005*); Robinia L. 1997; Lewis et al., 2005*; Bhattacharya et al., 2015); Des- (Yang et al., 2007; Malayeri et al., 2012; Sun et al., 2012*; manthus Willd. (Rangel, 2005*; Buril et al., 2010); Desmo- Jiang et al., 2016*); Senna Mill. (Williams, 1998*; Carvalho & dium Desv. (Ferguson & Skvarla, 1983; Chen & Huang, 1993; Oliveira, 2003*; Wolowski & Freitas, 2011*; Luz et al., 2013; Perveen & Qaiser, 1998b; Lewis et al., 2005*); Dinizia Ducke Fernandez-Pacella, 2014); Sophora L. (Perveen & Qaiser, (Sorsa, 1969; Banks et al., 2010; Dick et al., 2010*); Dioclea 1998b; Yang et al., 2005; Nogueira & Arruda, 2006*; Song, Kunth (Kavanagh & Ferguson, 1981; Amaral-Neto et al., 2007; Malayeri et al., 2012); Spatholobus Hassk. (Ridder- 2015*); Diptychandra Tul. (Graham et al., 1980; Ferguson Numan & Van der Ham, 1997; Lewis et al., 2005*); Swartzia & Schrire, 1994); Dolichos L. (Ferguson & Skvarla, 1983; Schreb. (Ferguson & Skvarla, 1991; Moço & Pinheiro, 1999*); Velayudhan et al., 1985*; Munyenyembe & Bisby, 1997; Trifolium L. (Morley, 1963*; Turner, 1993*; Rodet et al., Zhang et al., 2007); Dumasia DC. (Perveen & Qaiser, 1998*; Gazar, 2003; Taia, 2004; Lashin, 2006; Koçyigit 1998b; Liu & Huang, 2003; Lewis et al., 2005*); Duparquetia et al., 2013); Tylosema (Schweinf.) Torre & Hillc. (Frey Baill. (Graham et al., 1980; Lewis et al., 2005*; Banks et al., et al., 1992*; Banks et al., 2013, 2014); Ulex L. (Cubas & 2006); Eperua Aubl. (Banks & Rico, 1999*; Banks, 2003); Pardo, 1992; Pardo et al., 1994; Lewis et al., 2005*); Umtiza Erythrina L. (Hemsley & Ferguson, 1985; Basso-Alves et al., Sim (Banks & Rico, 1999; Lewis et al., 2005*); Vaughania S. 2011; Etcheverry et al., 2012*); Erythrophleum Afzel. ex R. Br. Moore (Schrire & Sims, 1997; Lewis et al., 2005*); Vicia L. (Banks & Lewis, 2009; Banks et al., 2010; Zhu et al., 2013*); (Porceddu et al., 1980*; Ferguson & Stirton, 1993*; Knudsen Exostyles Schott (Ferguson & Skvarla, 1988; Vidal de Freitas & & Poulsen, 2001*; Kahraman et al., 2013; Liu et al., 2013; Lewis, 2004*); Galega L. (Zhang et al., 2008; Lopes, 2011*); Binzat et al., 2014); Vigna Savi (Bronckers et al., 1972; Ohashi Genista L. (Parker et al., 2002*; Longo et al., 2010); Gigasiphon & Takahashi, 1981; Ferguson & Skvarla, 1983; Benachour Drake (Lewis et al., 2005*; Banks et al., 2013, 2014); Glycine et al., 2007*); Wisteria Nutt. (Song, 2007; Zhao et al., 2014*); Willd. (Schoen & Ahd, 1991*; Zhuang et al., 1994, 1997; Xylia Benth. (Sorsa, 1969; Guinet, 1990; Jumah, 1991; Lewis Chiari et al., 2005*); Glycyrrhiza L. (Perveen & Qaiser, 1998b; et al., 2005*; Banks et al., 2010); Zapoteca H. M. Hern. Meng & Zhu, 2010; Tian et al., 2012*); Hedysarum L. (Mitra & (Hernandez, 1989; Lewis et al., 2005*); Zollernia Wied-Neuw. Mondal, 1982; McGuire, 1993*; Choi & Ohashi, 1996; Satta & Nees (Ferguson & Skvarla, 1988; Carvalho & Barneby, et al., 2000*; Ghanavati & Amirabadizadeh, 2012); Holocalyx 1993*); Polygalaceae/Acanthocladus Klotzsch ex Hassk. Micheli (Ferguson & Skvarla, 1988; Lewis et al., 2005*); (Culley et al., 2002*; Eriksen & Persson, 2007*; Banks Indigofera L. (Hutton, 1960*; Wu & Huang, 1995; Schrire et al., 2008); Badiera DC. (Eriksen & Persson, 2007*; Banks & Sims, 1997; Perveen & Qaiser, 1998b; X. L. Zhao et al., et al., 2008); Barnhartia Gleason (Eriksen & Persson, 2007*; 2016); Inga Mill. (Sorsa, 1969; Buril et al., 2010); Jacque- Banks et al., 2008); Carpolobia G. Don (Culley et al., 2002; shuberia Ducke (Graham et al., 1980; Patel et al., 1985; Lewis Eriksen & Persson, 2007*; Banks et al., 2008); Comesperma et al., 2005*); Lecointea Ducke (Ferguson & Skvarla, 1988; Labill. (Culley et al., 2002*; Banks et al., 2008); Heterosamara Ferguson & Schrire, 1994; Lewis et al., 2005*); Leucaena Kuntze (Culley et al., 2002*; Banks et al., 2008); Monnina Ruiz Benth. (Jumah, 1991; Hughes, 1997; Ngongolo, 2014*); Lotus & Pav. (Culley et al., 2002*; Banks et al., 2008); Moutabea L. (Ferguson & Skvarla, 1983; Taylor, 1986*; Crompton & Aubl. (Banks et al., 2008; Silveira & Secco, 2015*); Polygala L. Grant, 1993; D´ıez & Ferguson, 1994; Kasumi & Sakuma, (Massey, 1971*; Banks et al., 2008; Castro et al., 2009*; 1998*; Perveen & Qaiser, 1998b); Macrotyloma (Wight & Krachai et al., 2009); Xanthophyllum Roxb. (Banks et al., Arn.) Verdc. (Ferguson, 1981; Lewis et al., 2005*); Medicago 2008; Krachai et al., 2009; Suresh & Sreekala, 2018*); Quil- L. (Sangduen et al., 1983*; Taia, 2004; Lashin, 2006; lajaceae/Quillaja Molina (Claxton et al., 2005; Kubitzki, Fridriksson & Bolton, 2011*); Microlobius C. Presl (Caccavari, 2007*); Surianaceae/Cadellia F. Muell. (Culley et al., 2002; Lewis et al., 2005*); Mildbraediodendron Harms 2002*; Claxton et al., 2005; Schneider, 2007*); Guilfoylia F. (Ferguson & Skvarla, 1988; Lewis et al., 2005*); Millettia Muell. (Claxton et al., 2005; Schneider, 2007*); Recchia Sessé& Wight & Arn. (Ferguson & Skvarla, 1982; Hsu & Huang, 2001; Moc. ex DC. (Claxton et al., 2005; Schneider, 2007*); Styloba- Arpiwi et al., 2015*); Mimosa L. (Jumah, 1991; El Ghazali sium Desf. (Claxton et al., 2005; Schneider, 2007*); Suriana L. et al., 1997; Caccavari, 2002; Lewis et al., 2005*; Lima et al., (Claxton et al., 2005; Schneider, 2007*). 2008); Mora Benth. (Lewis et al., 2005*; Banks & Lewis, 2009; Fagales/Betulaceae/Alnus Mill. (Chen, 1991; Weis & Banks et al., 2010); Mucuna Adans. (Ferguson, 1990; Hopkins Hermanutz, 1993*; Wang et al., 1995; Blackmore et al., & Hopkins, 1993*; Basso-Alves et al., 2011; Kobayashi et al., 2003; Puc & Kasprzyk, 2013*; Zhu et al., 2014*); Betula

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L. (Kubitzki, 1993a; Weis & Hermanutz, 1993*; Wang et al., Humulus L. (Punt & Malotaux, 1984; Kubitzki, 1993b*; Wang 1995; Blackmore et al., 2003; Jasenka, 2013*); Carpinus et al., 1995; Culley et al., 2002*); Trema Lour. (Nair & Sharma, L. (Pehlivan, 1987; Chen, 1991; Manos & Steele, 1997*; 1965; Zavada, 1983; Wang et al., 1995; Culley et al., 2002*); Blackmore et al., 2003; Akhondnezhad et al., 2011; Zhu Dirachmaceae/Dirachma Schweinf. ex Balf. f. (Erdtman & et al., 2014*); Corylus L. (Chen, 1991; Friis, 1993a*; Black- Sorsa, 1971; Bayer, 2004; Ronse De Craene & Miller, 2004*); more et al., 2003; Puc & Kasprzyk, 2013*); Ostrya Scop. Elaeagnaceae/Elaeagnus L. (Wang et al., 1995; Bartish & (Chen, 1991; Blackmore et al., 2003; Zhu et al., 2014*); Swenson, 2004*; Ma & Han, 2010); Hippophae L. (Sorsa, 1971; Ostryopsis Decne. (Chen, 1991; Friis, 1993a*; Zhu et al., 2014*); Bartish & Swenson, 2004*; Zhang et al., 2009; Mangla & Casuarinaceae/Allocasuarina L. A. S. Johnson (this study; Tandon, 2014*); Shepherdia Nutt. (Erdtman & Sorsa, 1971; Johnson & Wilson, 1993*; Culley et al., 2002*); Casuarina Bartish & Swenson, 2004*; Lin et al., 2015*); Moraceae/ L. (Kershaw, 1970; Coetzee & Praglowski, 1984; Johnson & Batocarpus H. Karst. (Punt & Eetgerink, 1982; Barth, 1984; Wilson, 1993*; Agashe et al., 1994; Culley et al., 2002*); Rohwer & Berg, 1993*; Culley et al., 2002*); Brosimum Sw. Gymnostoma L. A. S. Johnson (Kershaw, 1970; Coetzee & (Barth, 1976, 1984; Hoen & Punt, 1989; Rohwer & Berg, Praglowski, 1984; Johnson & Wilson, 1993*; Culley et al., 1993*; Culley et al., 2002*); Dorstenia L. (Barth, 1976, 1984, 2002*); Fagaceae/Castanea Mill. (Praglowski et al., 1984; 1986; Hoen & Punt, 1989; Rohwer & Berg, 1993*); Ficus L. Van Benthem et al., 1984; Kubitzki, 1993c*; Wang et al., (Galil & Eisikowitch, 1968*; Barth, 1976, 1984; Ejh, 1985*; 1995; Culley et al., 2002; Denk & Tekleva, 2014; Chen, Kerdelhue et al., 1997; Burn & Mayle, 2008; Rønsted et al., 2015*); Castanopsis (D. Don) Spach (Miyoshi, 1983; Praglowski 2008*); Helicostylis Trécul (Barth, 1984; Hoen & Punt, 1989; et al., 1984; Wang et al., 1995; Jia-Sheng, 2002*; Denk & Rohwer & Berg, 1993*; Burn & Mayle, 2008); Maclura Nutt. Tekleva, 2014; Wang et al., 2014*); Chrysolepis Hjelmq. (Punt & Eetgerink, 1982; Rohwer & Berg, 1993*; Burn & (Erdtman & Sorsa, 1971; Denk & Tekleva, 2014; Chen, Mayle, 2008); Morus L. (Nair & Sharma, 1965; Punt & 2015*); Colombobalanus Nixon & Crepet (Wang et al., Malotaux, 1984; Rohwer & Berg, 1993*; Wang et al., 1998; Denk & Tekleva, 2014; Chen, 2015*); Fagus L. (Nielsen 1995); Rhamnaceae/Adolphia Meisn. (Zietsman, 1990*; & Muckadeli, 1954*; Hashizume, 1975*; Van Benthem et al., Schirarend & Koehler, 1993; Culley et al., 2002*; Medan & 1984; Nilsson & Wästljung, 1987*; Wang et al., 1995; Denk & Schirarend, 2004*); Alphitonia Reissek ex Endl. (Zhang & Tekleva, 2014); Formanodendron Nixon & Crepet (Wang et al., Chen, 1992; Williams & Adam, 2001*); Berchemia Neck. ex 1998; Denk & Tekleva, 2014; Chen, 2015*); Lithocarpus DC. (Zhang & Chen, 1986; Culley et al., 2002*; Medan & Blume (Praglowski et al., 1984; Wang & Chang, 1989; Wang Schirarend, 2004*; Perveen & Qaiser, 2005); Ceanothus L. et al., 1995; Denk & Tekleva, 2014; Chen, 2015*); Quercus L. (Schirarend & Koehler, 1993; Hardig et al., 2000*); Colletia (Erdtman & Sorsa, 1971; Hashizume, 1975*; Van Benthem Comm. ex Juss. (Schirarend & Koehler, 1993; Basilio & et al., 1984; Wang et al., 1995; Yacine & Bouras, 1997*; Cao & Medan, 2001*; Medan & Schirarend, 2004; Gotelli et al., Zhou, 2002; Denk & Tekleva, 2014); Trigonobalanus Forman 2012*); Colubrina Rich. ex Brongn. (Zhang & Chen, 1992; (Wang et al., 1998; Culley et al., 2002*; Chen et al., 2008*; Medan & Schirarend, 2004*); Crumenaria Mart. (Schirarend & Denk & Tekleva, 2014); Juglandaceae/Alfaroa Standl. (Stone Koehler, 1993; Culley et al., 2002*; Medan & Schirarend, & Broome, 1975; Stone, 1993*; Wang et al., 1995; Culley 2004*); Gouania Jacq. (Schirarend & Koehler, 1993; Medan & et al., 2002*); Annamocarya A. Chev. (Stone, 1993*; Wang Schirarend, 2004*); Hovenia Thunb. (Zhang & Chen, 1992; et al., 1995; Culley et al., 2002*); Carya Nutt. (Stone & Medan & Schirarend, 2004*); Karwinskia Zucc. (Schirarend & Broome, 1975; McCarthy & Quinn, 1990*; Wang et al., Koehler, 1993; Medan & Schirarend, 2004*); Lasiodiscus 1995; Yang et al., 2014*; Q.-Z. Zhang et al., 2017*); Cyclo- Hook. f. (Schirarend & Koehler, 1993; Figueiredo, 1996*); carya Iljinsk. (Wang et al., 1995; Feng et al., 2010*); Engel- Maesopsis Engl. (Schirarend & Koehler, 1993; Medan & hardia Lesch. ex Blume (Stone & Broome, 1971; Stone & Schirarend, 2004*); Noltea Rchb. (Schirarend & Koehler, Broome, 1975; Stone, 1993*; Culley et al., 2002*); Juglans L. 1993; Medan & Schirarend, 2004*); Phylica L. (Schirarend (Stone & Broome, 1975; Prihar & Bajpai, 1985; Wang et al., & Koehler, 1993; Medan & Schirarend, 2004*); Pomaderris 1995, 1999*; Bai et al., 2006*; Mert, 2010); Platycarya Labill. (Schirarend & Koehler, 1993; Medan & Schirarend, Siebold & Zucc. (Stone & Broome, 1975; Wang et al., 2004*); Reissekia Endl. (Schirarend & Koehler, 1993; Medan 1995; Fukuhara & Tokumaru, 2014*); Pterocarya Kunth & Schirarend, 2004*; Braga et al., 2012); Retanilla (DC.) (Stone & Broome, 1975; Stone, 1993*; Wang et al., 1995; Brongn. (Schirarend & Koehler, 1993; Medan & Arce, Culley et al., 2002*); Rhoipteleaceae/Rhoiptelea Diels & 1999*); Reynosia Griseb. (Schirarend & Koehler, 1993; Medan Hand.-Mazz. (Erdtman & Sorsa, 1971; Liu, 1987; Wu & & Schirarend, 2004*); Rhamnidium Reissek (Schirarend & Kubitzki, 1993*; Sun et al., 2006*; Skarby et al., 2009); Koehler, 1993; Medan & Schirarend, 2004*); Rhamnus L. Myricaceae/Canacomyrica Guillaumin (Sundberg, 1985; (Zhang & Chen, 1992; Premathilake & Nilsson, 2001; Punt Kubitzki, 1993d; Culley et al., 2002*); Comptonia L’Hér. ex et al., 2003; Traveset et al., 2003*; Perveen & Qaiser, 2005); Aiton (Sundberg, 1985; Kubitzki, 1993d; Culley et al., 2002*); Sageretia Brongn. (Zhang & Chen, 1992; Medan & Schirarend, Myrica L. (Sundberg, 1985; Punt et al., 2002; Chai et al., 2004*; Perveen & Qaiser, 2005); Schistocarpaea F. Muell. 2011*, 2012*); Nothofagaceae/Nothofagus Blume (Cookson (Schirarend & Koehler, 1993; Medan & Schirarend, 2004*); & Pike, 1955; Praglowski, 1982; Kubitzki, 1993c; Wang et al., Scutia (Comm. ex DC.) Brongn. (Schirarend & Koehler, 1993; 2000; Culley et al., 2002*); Ticodendraceae/Ticodendron Medan & Schirarend, 2004*); Ziziphus Mill. (Devi et al., Gómez-Laur. & L. D. Gómez (Feuer, 1991; Gomez-Laurito & 1989*; Zhang & Chen, 1992*; Perveen & Qaiser, 2005; Nadia Gomez, 1991; Kubitzki, 1993e*; Culley et al., 2002*). et al., 2007); Rosaceae/Acaena Mutis ex L. (Kalkman, 1993; Rosales/Barbeyaceae/Barbeya Schweinf. (Zavada & Kalkman, 2004*; Pérez de Paz, 2004; Chung et al., 2010); Dilcher, 1986; Tobe & Takahashi, 1990; Friis, 1993a*); Alchemilla L. (Reitsma, 1966; Kalkman, 2004*; Perveen & Cannabaceae/Aphananthe Planch. (Zavada, 1983; Lu & Qaiser, 2014; Faghir et al., 2015); Armeniaca Scop. (Tong Kang, 1991; Kubitzki, 1993b*; Mason, 1999; Culley et al., et al., 1995; Kalkman, 2004*; Arzani et al., 2005); Bencomia 2002*); Celtis L. (Erdtman & Sorsa, 1971; Wang et al., 1995*; Webb & Berthel. (Hebda & Chinnappa, 1994; Kalkman, Williams & Adam, 1999*; Sattarian et al., 2006); Chaetachme 2004*; Pérez de Paz, 2004); Chaenomeles Lindl. (Hebda & Planch. (Zavada, 1983; Kubitzki, 1993b*); Gironniera Gau- Chinnappa, 1994; Zhou et al., 2000b; Kaufmane & Rumpunen, dich. (Zavada, 1983; Lu & Kang, 1991; Kubitzki, 1993b*); 2002*; Zang & Ma, 2014); Cotoneaster Medik. (Wang et al.,

1995; Zhou et al., 2000b; Kalkman, 2004*; Perveen & Qaiser, Chinnappa, 1990; Naruhashi et al., 2001*; Perveen & Qaiser, 2014); Dichotomanthes Kurz (Zhou et al., 2000a; Kalkman, 2014); Sarcopoterium Spach (Kalkman, 2004*; Pérez de Paz, 2004*); Dryas L. (Reitsma, 1966; Zhou et al., 1999c; Kalkman, 2004); Sorbaria (Ser.) A. Braun (Hebda & Chinnappa, 1990; 2004*; Chung et al., 2010); Duchesnea Sm. (Naruhashi & Zhou et al., 1999a; Kalkman, 2004*; Perveen & Qaiser, 2014); Sugimoto, 1996*; Han et al., 2012; Perveen & Qaiser, 2014); Sorbus L. (Reitsma, 1966; Zhou et al., 2000b; Bednorz et al., Exochorda Lindl. (Zhou et al., 1999b; Kalkman, 2004*); 2003; Perveen & Qaiser, 2014; Hamston et al., 2017*); Filipendula Mill. (Reitsma, 1966; Hebda & Chinnappa, Stranvaesia Lindl. (Wang et al., 1995; Zhou et al., 2000b; 1994; Zhou et al., 1999c*; Weidema et al., 2000*); Fragaria Kalkman, 2004*); Ulmaceae/Ampelocera Klotzsch (Zavada, L. (Reitsma, 1966; Naruhashi & Toyoshima, 1979; Svensson, 1983; Todzia, 1993*); Hemiptelea Planch. (Zavada, 1983; 1991*; Wang et al., 1995; Zebrowska,˙ 1998*; Chung et al., Todzia, 1993*); Zelkova Spach (Suo & Hashizume, 1995*; 2010*; Perveen & Qaiser, 2014); Geum L. (Reitsma, 1966; Wang et al., 1995; Nakagawa et al., 1998; Pattemore, Hebda & Chinnappa, 1990; Wang et al., 1995; Zhou et al., 2013*); Urticaceae/Boehmeria Jacq. (Nair & Sharma, 1965; 1999c; Kalkman, 2004*; Chung et al., 2010; Perveen & Tarnavschi et al., 1967; Sorsa & Huttunen, 1975; Friis, 1993b*; Qaiser, 2014); Hagenia J. F. Gmel. (Kalkman, 2004*; Pérez Culley et al., 2002*; Laaidi & Thibaudon, 2002*); Cecropia de Paz, 2004; Chung et al., 2010); Holodiscus (K. Koch) Maxim. Loefl. (Barth, 1976, 1989; Kubitzki & Berg, 1993*; Roubik, (Hebda et al., 1988; Kalkman, 2004*); Kerria DC. (Wang et al., 2005*; Cox-Foster, 2008*); Coussapoa Aubl. (Barth, 1976; 1995; Zhou et al., 1999c; Kalkman, 2004*); Leucosidea Eckl. Friis, 1993b*; Culley et al., 2002*; Laaidi & Thibaudon, & Zeyh. (Kalkman, 2004*; Pérez de Paz, 2004; Chung et al., 2002*); Cypholophus Wedd. (Sorsa & Huttunen, 1975; Friis, 2010); Malus Mill. (Palmer-Jones & Clinch, 1968; Wang et al., 1993b*; Culley et al., 2002*; Laaidi & Thibaudon, 2002*); 1995; Kemp, 1996*; Zhou et al., 2000b; Joneghani, 2008; Liu Droguetia Gaudich. (Sorsa & Huttunen, 1975; Friis, 1993b*; et al., 2008*; Perveen & Qaiser, 2014); Margyricarpus Ruiz & Culley et al., 2002*; Laaidi & Thibaudon, 2002*); Elatostema Pav. (Kalkman, 2004*; Chung et al., 2010); Neillia D. Don J. R. Forst. & G. Forst. (Sorsa & Huttunen, 1975; Recio (Wang et al., 1995; Zhou et al., 1999a; Kalkman, 2004*); et al., 2009*); Laportea Gaudich. (Tarnavschi et al., 1967; Oemleria Rchb. (Hebda & Chinnappa, 1990; Hebda et al., Sorsa & Huttunen, 1975; Menges, 1990*); Lecanthus Wedd. 1991; Hesse & Pannell, 2011*); Photinia Lindl. (Wang et al., (Sorsa & Huttunen, 1975; Friis, 1993b*; Culley et al., 2002*; 1995; Zhou et al., 2000b; Kalkman, 2004*); Physocarpus Laaidi & Thibaudon, 2002*); Maoutia Wedd. (Sorsa & Maxim. (Reitsma, 1966; Hebda & Chinnappa, 1990; Hebda Huttunen, 1975; Friis, 1993b*; Culley et al., 2002*; Laaidi et al., 1991; Zhou et al., 1999a; Kalkman, 2004*); Potentilla L. & Thibaudon, 2002*); Parietaria L. (Tarnavschi et al., 1967; (Naruhashi & Toyoshima, 1979; Wang et al., 1995; Zhou et al., Sorsa & Huttunen, 1975; Punt & Malotaux, 1984; Kovacevi´ˇ c 1999c; Chung et al., 2010; McIver & Erickson, 2012; Perveen et al., 2014*; Ariano et al., 2017*); Pellionia Gaudich. (Sorsa & Qaiser, 2014); Prunus L. (Reitsma, 1966; Hebda & Chinnappa, & Huttunen, 1975; Friis, 1993b*; Culley et al., 2002*; Laaidi 1990; Hebda et al., 1991; Wang et al., 1995; Calzoni & & Thibaudon, 2002*); Pilea Lindl. (Nair & Sharma, 1965; Speranza, 1998*; Fang & Siqing, 2007*; Cali´´ c et al., 2013; Tarnavschi et al., 1967; Sorsa & Huttunen, 1975; Friis, Perveen & Qaiser, 2014); Pygeum Gaertn. (Zhou et al., 1999b; 1993b*; Culley et al., 2002*; Laaidi & Thibaudon, 2002*); Kalkman, 2004*; Shi et al., 2013); Pyrus L. (Xu & Yao, 1991; Pipturus Wedd. (Sorsa & Huttunen, 1975; Friis, 1993b*; Zhou et al., 2000b; Maccagnani et al., 2003*; Del Duca et al., Culley et al., 2002*; Laaidi & Thibaudon, 2002*); Urera 2010*; Perveen & Qaiser, 2014; Gemeda et al., 2017*); Rosa Gaudich. (Burn & Mayle, 2008; Holz et al., 2009*); Urtica L. (Reitsma, 1966; Jicinska, 1975*; Naruhashi & Toyoshima, L. (Nair & Sharma, 1965; Tarnavschi et al., 1967; Sorsa & 1979; Hebda & Chinnappa, 1990; Ueda et al., 1996*; Jesse Huttunen, 1975; Faegri & van der Pijl, 1979*; Goyder, et al., 2006; Perveen & Qaiser, 2014); Sanguisorba L. 1983*; Punt & Malotaux, 1984; Wang et al., 1995; Shannon (Reitsma, 1966; Naruhashi & Toyoshima, 1979; Hebda & & Holsinger, 2007*).

Appendix 4. Comprehensively coded matrix of pollen, continued. Morphological data for nitrogen-fixing clade (characters as in Table 1).

Taxon Democratic coding Abobra 021113200140111601310 Acacia 2????2{2,3}?1{1,0}4?010{1,3,7}10131{1,3,2} Acaena 0211122010301113??310 Acanthocladus 02111{2,1}3010300042??31{3,1} Actinostemma 021112201000004501312 Adenanthera 2????1{2,3}?0141104{1,3}??313 Adolphia 021101201020004{2,1}??311 Albizia 2????23?0140004{3,1,2}??31{3,1} Alchemilla 021{1,2}1{1,2}{2,3}01000011{3,0}??310 Aldina 02111{1,2}2010201041013{1,0}{3,1} Alfaroa 02100{1,2}{2,1,3}011000110101113 Allocasuarina 02110220014101110110{3,1} Alnus 021{1,0}02{3,2}01{1,0}20011{3,1}0111{3,1} Alphitonia 021{1,0}0{2,1}201020004{3,2,1}??31{1,3}

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Appendix 4. Continued.

Taxon Democratic coding Alsomitra 021111201000004{1,3}01312 Alysicarpus 021{1,0}1{2,1}201020004{3,1,7}01310 Amorpha 021111201030104401311 Ampelocera 02111{2,1}300140011111113 Ampelosycios 021113{2,3}01120004401312 Anadenanthera 2????{1,0}{2,3}?01410047113{1,0}3 Anisophyllea 021211{2,1}01000004{1,5}0132{3,1} Annamocarya 021002201100011011113 Anthyllis 021{1,2}{1,0}{2,3}{2,3}01030004{1,2}1131{1,0} Aphananthe 021112{2,3}0110001011111{3,1} Armeniaca 021{2,3}{1,0}{2,1}2010000045??313 Astragalus 021{1,2,3}{1,0}{2,1}2010{3,2}0004{4,1,2}??311 Augouardia 021{1,2}12201000004401313 Badiera 02111{2,1}3010{1,3}000400131{1,3,0} Baijiania 021212201000004401312 Baphia 021{1,2}{1,0}{2,1}{2,3}01020004{1,4,3}1131{3,1,2} Barbeya 021111201030011311103 Barnhartia 02101{2,3}3010{1,3}00040??31{3,1} Batocarpus 02{1,0}111{2,1}01100011{3,1}??113 Bauhinia {0,1}211{1,0}{3,4}{2,3}011{2,3}001{3,1}{1,4}1131 {3,1,2} Bayabusua 021222301000013101312 Begonia 021{3,2,1}2{1,2}{2,3}0102001{4,1}{5,1}0103{1,2}0 Bencomia 0211122010000113??311 Benincasa 021113201000004401312 Berchemia 021101201020004{2,1}??31{1,2,3} Betula 0211{1,0}2{2,3}01100011{3,1}0111{3,1} Bocoa 021{1,2}1{1,2}2010{3,0}0004{2,1,3}01313 Boehmeria 02{1,0}111{2,1,3}001401111??11{1,0,3} Borneosicyos 121113201000010101312 Brenierea 02111?201030004{1,3}?131{1,0} Brosimum 020111101100111{3,1}??113 Browneopsis 02111{2,3}{2,3}011{4,0}00{1,0}4{1,5}01313 Bryonia 021{1,2}132010{2,3}0004401312 Burkea 02111{1,2}2010?0004{1,3}01313 Cadellia 02111{1,2}201020004501113 Caesalpinia 0211{1,2}{2,3}20103000440131{3,1,2} Cajanus 02111{2,3}2010{0,2,3}00044??31{1,2} Calopogonium 0211{1,0}{1,2}201030004{3,1,4}10131{2,0} Camptosema 02111{1,2}20102000440131{2,1} Campylotropis 021{1,2}1{1,2}201020004401311 Canacomyrica 02100220110001100111{3,1} Canavalia 01110{2,3}20102{1,0}004101310 Caragana 021{2,1}1{1,2}2010{3,0}0104{1,4}??3{1,0}1 Carpinus 021112{2,3}01100111{3,1}01113 Carpolobia 0211123010{1,3}{1,0}004{1,2}??31{1,3} Carya 02100{2,3}201100011011113 Castanea 021{2,1}{2,1}1201020004{3,5}11313 Castanopsis 021{2,1,3}{2,1}{1,2}201030004301313 Casuarina 021102200140010{1,3}0111{3,1} Ceanothus 02110{1,2}2010{2,0,3}0004{3,2,1}??311 Cecropia 020{1,2}11100140011001{1,3}13 Celtis 02111{1,2}201100010101113 Ceratonia 0211{1,0}{2,1}{3,2}01020004{1,3}01313 Ceratosanthes 021113{3,2}01000004401312 Cercis 021{1,3}1120100000410131{1,3}

Appendix 4. Continued.

Taxon Democratic coding Chaenomeles 021{1,2,3}122010200045??31{1,3} Chaetachme 02111220110001010111{1,3} Chamaecrista 021{1,2}1{2,3}2010{2,0,3}0004{1,3}??3{1,0}{1,3} Chrysolepis 021{2,0,1}21201020004301313 Cicer 021{1,2}122010300044??312 Clathrotropis 0211122010300041??313 Cogniauxia 021{1,2}13201001004401312 Collaea 021112201020004401311 Colletia 0211022010200042??311 Colombobalanus 021202200040010101113 Colophospermum 00111231014000441131{3,1} Colubrina 02110{2,1}2010{2,0}0012{2,3,1}??313 Combretocarpus 021211201000004101323 Comesperma 02111{2,3}3010{1,3}0004{1,0,2}0131{1,2,0} Comptonia 02110220110001100111{1,3} Cordyla 021{1,2}1{2,1}2010{3,0}000410131{3,1} Coriaria 021112{1,2}01{1,0}00010{1,7}01111 Coronilla 021{1,2}1{1,2}201020004{3,5}01311 Corylus 021102{2,3}01100011{3,1}0111{1,3} Corynocarpus 0100321010300043013{1,0}3 Cotoneaster 021112201020004{5,1}??311 Coussapoa 0201111001400110??11{1,3} Cranocarpus 00111231014?1043010311 Crossosoma 02110?2010?00044??301 Crotalaria 021{2,1}1{1,2}{2,1}010{2,3,0}00044??311 Crudia 021{1,2}1220103000450131{3,1} Crumenaria 0211022010{2,0}0004{5,3,2}01310 Cucumeropsis 021{1,0}132010{2,0}?004401312 Cucumis 021{1,0}13201{1,0}30004{4,1}01312 Cucurbita 001114310140104601312 Cucurbitella 021{1,0}1320102{1,0}004{4,1}01312 Cyathostegia 0212122010{3,0}000410131{3,1} Cyclanthera 021113301020004{1,3}01312 Cyclantheropsis 021{1,2}12201000004501312 Cyclocarya 021012{3,2}01100011011113 Cyclolobium 02111{1,2}2010300041??3{1,0}3 Cypholophus 021111{2,3}001401110??11{1,3} Dalbergia 02111{1,2}20103000410131{3,1,2} Dalea 021{2,1}1{2,3,4}200040104401311 Datisca 0212212010?0004{3,1}01110 Daviesia 0211112000401044??31{1,3} Delonix 0211132010{4,?}0004401313 Dendrosicyos 021113201020004401313 Desmanthus 0211022010000045??31{3,1,0} Desmodium 02111{1,2}201020004{4,1,3,7}11031{1,0} Dichotomanthes 0211122010300045??31{1,3} Dinizia 1211122010000100??313 Dioclea 0{2,1}101{3,2}201021004{1,0}01311 Diplocyclos 021114200130111401312 Diptychandra 12111220100?0044013{1,0}{3,1} Dirachma 0211132010000044??3{1,0}{3,1} Dolichos 021102200140004{1,4}1131{2,0,1} Dorstenia 0011{1,3}1311100111{3,1}??311 Droguetia 02{1,0}111{2,1}001401110??120 Dryas 021112201030004{5,1}??311 Duchesnea 021{1,3}12201000004{5,1}??310

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Appendix 4. Continued.

Taxon Democratic coding Dumasia 021102{2,3}00100004{3,4}0131{2,0,1} Duparquetia 02003{1,2}10100000410131{1,3} Ecballium 021213201000004401310 Echinocystis 021113301020004101312 Elaeagnus 0211122010300100??31{3,1} Elatostema 0{2,1}01111001400110??120 Engelhardia 021001{2,1,3}011300110101113 Eperua 02110{2,3,4}20{1,0}13001{4,0,2}{1,4,3}01313 Erythrina 02111{2,1}{2,3}00140004{4,3}0141{3,1} Erythrophleum 02111{1,2}2010?0004101313 Exochorda 02111{1,2}2010300045??311 Exostyles 02111{2,1}20103001110131{3,1} Fagus 02111220102{1,0}01000111{3,1} Fevillea 021{1,2}12201000004501312 Ficus 0200{1,3}1101100011{3,1}??3{1,2}{3,1} Filipendula 0211112010200110??310 Formanodendron 021102201020010001113 Fragaria 021{1,2}1{1,2}2010001045??310 Galega 0211112010300044??310 Genista 021{1,2}1{1,2}20{1,0}0{3,4}0004{1,2}??311 Gerrardanthus 0211132010{2,0}0004401312 Geum 02111{2,1}2010300045??310 Gigasiphon 02121?2010?001{4,0}1013{1,2}{3,1} Gironniera 021112{2,3}011000101011{1,2}{3,1} Glycine 0211{1,0}1201000004311{0,3}10 Glycyrrhiza 0211{1,0,2}{2,1}201030004{1,3,2}??310 Gouania 02110{1,2}2010{2,0,3}0004{1,2,5,3}??312 Guaiacum 02110220004?0044??30{1,3} Guilfoylia 02101{1,2}201020010001113 Gurania 12111{3,4}200100004401412 Gymnopetalum 021113201000004401312 Gymnostoma 021102200140010{1,3}0111{3,1} Gynostemma 021{1,2}12201000004501312 Hagenia 0211122010301103??313 Hedysarum 021{2,3}1{1,2}2011{4,3}0104{4,1}013{1,0}1 Helicostylis 021111{1,2}01100011{3,1}??313 Helmontia 021113201100104{4,1}01312 Hemiptelea 0211123001400113??11{3,1} Hemsleya 021{1,2}12201000004{5,4}01312 Herpetospermum 021114200140104601312 Heterosamara 01003{2,3}3110100044??31{3,1} Hillebrandia 021221201000004501320 Hippophae 021112{2,3}010{2,0,3}00110??31{1,3} Hodgsonia 02111430100{1,0}004401312 Holocalyx 02121{1,2}201030004201313 Holodiscus 021111201020004501311 Hovenia 0211022010{2,0}0004{5,3}0131{3,1} Humulus 021{1,0}12{2,1,3}011000101??110 Indigofera 021{1,0}{1,0}22010{3,2}0004{3,1}1131{1,3} Inga 2????23?01400042??3{2,1}3 Jacqueshuberia 021113201030004411313 Juglans 0010123111000110101113 Karwinskia 02110{2,1}201020012{2,1}??31{1,3} Kedrostis 021113201020004{1,4,5}01312 Kerria 0211112010?0004{5,2}??311 Lagenaria 0211132010{2,0}0004201312

Appendix 4. Continued.

Taxon Democratic coding Laportea 0211112001400100??110 Lasiodiscus 02110{1,2}2010{2,0,3}0004{3,2,1}??312 Lecanthus 0201111001400110??120 Lecointea 02111{1,2}201030010101313 Leucaena 221113{2,3}1{1,0}12001010131{1,0} Leucosidea 0211122010301045??31{1,3} Lithocarpus 021{2,1,3}{2,1}1201030004301313 Lotus 021{1,2}1{1,2}{2,3}010{3,0,2}0004{3,1,2}11310 Luffa 02111{3,4}20100{1,0}004{1,4}01312 Maclura 021111{1,2,3}01100011{3,1}??11{3,1} Macrotyloma 021{1,0}1{2,3}201{1,0}{4,0}001131031{2,0} Maesopsis 0211012010000100??313 Malus 021{2,1,3}1{2,3}2010?0004{5,1}??31{3,1} Maoutia 021111{1,2}00140{1,0}100??12{1,3} Marah 021{2,1}{2,1}3301020004{4,1}01312 Margyricarpus 02110?3010301043??311 Medicago 021{1,2}{1,0}{2,1}20{1,0}03{1,0}004{4,2}??310 Melancium 021113201020004101312 Melianthus 02121?2010200044??311 Microlobius 2????23?014000471131{1,3} Mildbraediodendron 02111{1,2}2010{3,0}0004{1,2}01313 Millettia 02111{1,2}201030004{2,1,4,3}0131{2,3,1} Mimosa {1,2}????{1,2}2?0101004{3,7}1031{1,3} Momordica 0211132010{2,0}0004401312 Monnina 02111{2,3}3010{1,3}10041??31{1,2,3} Mora 021112201000004101313 Morus 0{2,0}1{1,0}{1,3}{1,2}{1,2,3}11100111{3,1}??11 {3,1} Moutabea 02111{2,1}3010{1,0}001{4,0}0??31{3,2,1} Mucuna 021{1,2}1{2,3,4}20103001{4,0}{1,4,3}10141{2,0} Myrica 021{1,0}0{2,1}20110001170111{3,1} Neillia 02111{1,2}2010?00042??311 Neptunia 0211132010000045??3{1,3,2}0 Noltea 02110{1,2}201020004{3,1}??31{1,3} Nothoalsomitra 0211132010?0004401312 Nothofagus 02111{2,1,3}300040011001113 Octomeles 0211112010000044??113 Oemleria 02111{2,1}20100000450131{1,3} Ormosia 0211122010200041??313 Ornithopus 021{1,2}1{1,2}201020004{3,1}00310 Ostrya 021112{2,3}01100111{3,1}01113 Ostryopsis 021112{2,3}01100111{3,1}01111 Oxalis 0211{1,0}22000400044??{0,3}10 Oxystigma 02111{2,1}20103{1,0}004{1,3}013{2,1}3 Pachyelasma 0211122010200041??313 Papuasicyos 021112201020004401312 Parapiptadenia 2????13?014?004{7,3}1131{3,1} Parietaria 02{1,0}111{2,3,1}001400110??120 Pellionia 02{1,0}111{2,1,3}001400110??1{1,2}0 Peltophorum 0211132010?000440?313 Pentaclethra 02111320{1,0}131004{1,0}0?313 Peponium 02111{3,4}201000004501312 Phanera 021{1,2,0}{1,0}{2,3,4}20112001{4,0}{4,1,3}0031 {1,3} Photinia 0211122010200042??31{3,1} Phylica 02110{1,2}201020012{2,4}01311

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Appendix 4. Continued.

Taxon Democratic coding Phyllodium 021{1,2}1{2,1}201030004401311 Physocarpus 02111{1,2}201000004501311 Pilea 021111{1,2}001401110??120 Piliostigma 0211122001401111013{1,0}{3,1} Piptadeniopsis 2????33?014?00431131{1,3} Pipturus 0211112001400110??11{1,3} Platycarya 0{2,1}100{1,2}{2,3}011300110101113 Poeppigia 0211122010??0044??31{1,3} Polygala 0{2,1}1{1,2,0}{1,0,3}{2,3}3010{1,3,2}{1,0}01{4,0} {1,2}0131{3,1} Pomaderris 02110{1,2}20102001000131{1,3} Potentilla 02111{2,1}2010201045??3{1,2,0}0 Prioria 02111220103{1,0}004{3,1}01313 Prunus 02111{2,1,3}201030004{5,3,1}0131{3,1} Psiguria 121{1,0}24{2,3}00140010101412 Psoralea 021112201000004{4,3}11311 Pterocarya 00101{2,1}311130011011113 Pueraria 021{1,2}12201020004{1,4}0131{2,0} Pygeum 0211122010?0004{5,3}??31{3,1} Pyrus 021{2,1,3}122010?000450131{3,1} Quercus 0211{2,1}{1,2}2010?{1,0}010{3,1,7}0111{3,1} Quillaja 021{2,1}12201020004501313 Ranunculus 021112200040011101{3,2}{1,3}0 Recchia 02111{1,2}201020004{1,3}0111{3,1} Reissekia 0211022010200045??311 Retanilla 021101201000004501311 Reynosia 02110{1,2}2010{2,0}0012{2,3}0131{1,3} Rhamnidium 02110{1,2}201020012{1,2}??31{1,3} Rhamnus 02110{1,2}2010{2,0}001221131{1,3} Rhoiptelea 021{1,0}02201020111001113 Robinia 02121{1,2}201030004{1,3}??31{3,1} Rosa 02111{2,1}201020104{5,4}0131{1,2} Ruptiliocarpon 02111?2010?00043??313 Sageretia 021101201020004{3,1}??31{1,3} Sanguisorba 021112{2,3}010?01101??310 Sarcopoterium 0211122010000103??311 Schistocarpaea 02110{1,2}201000004{3,1}??313 Schizocarpum 001114310140104601312 Schizopepon 0211122010?0004401312 Scutia 0211012010{2,0}00122??31{1,3} Senna 0{2,1}1{1,2}1{1,2,3}{2,3}010{2,0}0004{1,3}??31 {3,1,0} Shepherdia 021222201000000{1,3}003{1,0}3 Sicydium 021{1,2}12201020004501312 Sicyos 021{1,2,0}13300040011401312 Siolmatra 021112201020004501312 Siraitia 021113201000004401312 Solena 021{1,2}13201020010001312 Sophora 021{1,2}1{1,2}2010010041??31{3,1,0} Sorbaria 021111201020004{5,1}??311 Sorbus 021{1,2}12201020004{5,3,1}??31{3,1} Spatholobus 0211122010{2,0,3}0004{1,2,3}11312 Stranvaesia 0211122010200042??31{3,1} Stylobasium 02110{2,3}{2,3}01020004{3,1}010101 Suriana 021102201020004{3,1}??11{1,3} Swartzia 021{1,2}1{1,2}201020004{1,3,5}1131{1,3}

Appendix 4. Continued.

Taxon Democratic coding Tecunumania 021114210140104601312 Tetrameles 021{1,2}{1,2}0201000004{3,2}01113 Ticodendron 021112{2,3}001400111110113 Trema 02011110110001010111{3,1} Trichosanthes 021113201130004{1,3,4}11312 Trifolium 021{1,2}12201030004{1,4}??310 Trigonobalanus 02111220100?012101313 Tylosema 02121?201000004{1,3}01312 Ulex 02111{2,1}2010?0004{1,4}11311 Umtiza 0212122010??004301311 Urera 021111{2,3}101400110??11{1,2,3} Urtica 02{1,0}111{2,3}101401110??110 Vaughania 021122201020004311311 Vicia 021{2,1,3}{1,0}22010{2,3}0004{1,4,3}11{3,0}1{2,0} Vigna 0211122001{2,3}0104411031{2,0} Wisteria 021{1,2}122010??0041??312 Xanthophyllum 02111{2,1}3010{1,2}000410131{1,3} Xerosicyos 021{1,2}122010?0004501312 Xylia 2???01{2,3}?01401043??313 Zapoteca 2???023?014?0040??311 Zehneria 021113201020004401312 Zelkova 02101{2,3}3001400113??113 Ziziphus 02110{1,2}2010{2,0}0012{2,3,1}??312 Zollernia 02111{1,2}201030004{1,4}0131{3,1}

Appendix 5. Democratically coded matrix of pollen, continued. Morphological data for nitrogen-fixing clade (characters Appendix 5. Continued. as in Table 1). Taxon Democratic coding Taxon Democratic coding Armeniaca 0212122010000045??313 Abobra 021113200140111601310 Astragalus 0211122010000044??310 Acacia 2????22?014?000110311 Augouardia 021112201000004401313 Acaena 0211122010301113??310 Badiera 021112301010004001311 Acanthocladus 0211123010300042??313 Baijiania 021212201000004401312 Actinostemma 021112201000004501312 Baphia 021112200000004100313 Adenanthera 2????12?01411041??313 Barbeya 021111201030011301103 Adolphia 0211012010200042??311 Barnhartia 0210123010100040??313 Albizia 2????23?01400043??313 Batocarpus 0211112011000113??113 Alchemilla 0211112010000113??310 Bauhinia 021013200000000100313 Aldina 021111201020004101313 Bayabusua 021222301000013101312 Alfaroa 021001201100011011113 Begonia 021321201020004501310 Allocasuarina 021102200140011101103 Bencomia 0211122010000113??311 Alnus 021102301100011301113 Benincasa 021113201000004401312 Alphitonia 0211022010200043??311 Berchemia 0211012010200042??311 Alsomitra 021111201000004101312 Betula 021112201100011301113 Alysicarpus 021112201000004301310 Bocoa 021111201030004201313 Amorpha 021111201030104401311 Boehmeria 0211112001400111??111 Ampelocera 021112300140011111113 Borneosicyos 121113201000010101312 Ampelosycios 021113201020004401312 Brenierea 02111?2010000041?1311 Anadenanthera 2????12?0141004701313 Brosimum 0201111011001113??113 Anisophyllea 021211201000004101323 Browneopsis 021112200040010100313 Annamocarya 021002201100011011113 Bryonia 021113201000004401312 Anthyllis 021112201030004100311 Burkea 0211112010?0004101313 Aphananthe 021112201100010111113 Cadellia 021111201020004501113

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Appendix 5. Continued. Appendix 5. Continued.

Taxon Democratic coding Taxon Democratic coding Caesalpinia 021112201030004401313 Cypholophus 0211112001401110??111 Cajanus 0211122010000044??311 Dalbergia 021111201000004101313 Calopogonium 021111201000004311312 Dalea 021212200040104401310 Camptosema 021111201020004401312 Datisca 0212212010?0004301110 Campylotropis 021111201020004401311 Daviesia 0211112000401044??311 Canacomyrica 021002201100011001113 Delonix 021113200040004401313 Canavalia 011002201021004101310 Dendrosicyos 021113201020004401313 Caragana 0212112010301041??311 Desmanthus 0211022010000045??313 Carpinus 021112201100111301113 Desmodium 021111201020004401311 Carpolobia 0211123010110041??311 Dichotomanthes 0211122010300045??311 Carya 021002201100011011113 Dinizia 1211122010000100??313 Castanea 021221201020004301313 Dioclea 021013201020004101311 Castanopsis 021221201030004301313 Diplocyclos 021114200000111401312 Casuarina 021102200140010101113 Diptychandra 12111220100?004401313 Ceanothus 0211012010200043??311 Dirachma 0211132010000044??313 Cecropia 020111100140011001113 Dolichos 021102200140004110312 Celtis 021111201100010101113 Dorstenia 0011113111001113??310 Ceratonia 021112301000004101313 Droguetia 0211112001401110??120 Ceratosanthes 021113301000004401312 Dryas 0211122010300045??311 Cercis 021111201000004101311 Duchesnea 0211122010000045??310 Chaenomeles 0211122010200045??311 Dumasia 021102200100004301312 Chaetachme 021112201100010101111 Duparquetia 020031101000004101311 Chamaecrista 0211122010200041??310 Ecballium 021213201000004401310 Chrysolepis 021221201020004301313 Echinocystis 021113301020004101312 Cicer 0211122010300044??310 Elaeagnus 0211122010300100??313 Clathrotropis 0211122010300041??313 Elatostema 0201110001400110??120 Cogniauxia 021113201001004401312 Engelhardia 021001201100011011113 Collaea 021112201020004401311 Eperua 021002201000004101313 Colletia 0211022010200042??311 Erythrina 021102200140004401413 Colombobalanus 021202200040010101113 Erythrophleum 0211112010?0004101313 Colophospermum 001112310140004411313 Exochorda 0211112010300045??311 Colubrina 0211022010200022??313 Exostyles 021112201030001101313 Combretocarpus 021211201000004101323 Fagus 021112201001010001113 Comesperma 021112301010004101311 Fevillea 021112201000004501312 Comptonia 021102201100011001111 Ficus 0200111011000013??313 Cordyla 021112201030004101313 Filipendula 0211112010200110??310 Coriaria 021112101100010101111 Formanodendron 021102201000010001113 Coronilla 021111201020004300310 Fragaria 0211012010001045??310 Corylus 021102201100011301111 Galega 0211112010300044??310 Corynocarpus 010032101030004301313 Genista 0211112010300041??311 Cotoneaster 0211122010200045??311 Gerrardanthus 021113201020004401312 Coussapoa 0201111001400110??111 Geum 0211122010300045??310 Cranocarpus 00111231014?104301311 Gigasiphon 02121?2010?0004101313 Crossosoma 02110?2010?00044??301 Gironniera 021112201100010101113 Crotalaria 0212112010200044??310 Glycine 021111201000004301010 Crudia 021112201030004501313 Glycyrrhiza 0211122010300041??310 Crumenaria 021102201020004501310 Gouania 0211012010200041??312 Cucumeropsis 02111320102?004401312 Guaiacum 02110220004?0044??301 Cucumis 021113200100004401312 Guilfoylia 021011201020010001113 Cucurbita 001114310140104601312 Gurania 121113200100004401412 Cucurbitella 021113201021004401312 Gymnopetalum 021113201000004401312 Cyathostegia 021212201030004101313 Gymnostoma 021102200140010101113 Cyclanthera 021113301020004101312 Gynostemma 021112201000004501312 Cyclantheropsis 021112201000004501312 Hagenia 0211122010301103??313 Cyclocarya 021002301100011011113 Hedysarum 021211200040104401310 Cyclolobium 0211112010300041??313 Helicostylis 0201111011000113??313

Appendix 5. Continued. Appendix 5. Continued.

Taxon Democratic coding Taxon Democratic coding Helmontia 021113200100104401312 Oemleria 021112201000004501311 Hemiptelea 0211123001400113??113 Ormosia 0211122010200041??313 Hemsleya 021112201000004501312 Ornithopus 021111201020004300310 Herpetospermum 021014200140104601312 Ostrya 021112201100111301113 Heterosamara 0100323110100044??310 Ostryopsis 021112201100111301111 Hillebrandia 021221201000004501320 Oxalis 0211122000400044??010 Hippophae 0211122010200100??311 Oxystigma 021112201031004101323 Hodgsonia 021114301001004401312 Pachyelasma 0211122010200041??313 Holocalyx 021211201030004201313 Papuasicyos 021112201020004401312 Holodiscus 021111201020004501311 Parapiptadenia 2????13?014?004701313 Hovenia 021102201020004501313 Parietaria 0211112001400110??120 Humulus 0211122011000101??110 Pellionia 0211112001400110??110 Indigofera 021112201030004301310 Peltophorum 0211132010?000440?313 Inga 2????23?01400040??323 Pentaclethra 02111320103100410?313 Jacqueshuberia 021113201030004411313 Peponium 021113201000004501312 Juglans 001002311100011011113 Phanera 021112201000004400311 Karwinskia 0211022010200022??311 Photinia 0211122010200042??313 Kedrostis 021113201020004101312 Phylica 021101201020002201311 Kerria 0211112010?00045??311 Phyllodium 021112201030004401311 Lagenaria 021113201020004201312 Physocarpus 021111201000004501311 Laportea 0211112001400100??110 Pilea 0201111001401110??120 Lasiodiscus 0211012010200043??312 Piliostigma 021112200140111101313 Lecanthus 0201111001400110??120 Piptadeniopsis 2????33?014?004301311 Lecointea 021111201030010101313 Pipturus 0211112001400110??111 Leucaena 021113201000000001311 Platycarya 021001201100011011113 Leucosidea 0211122010301045??311 Poeppigia 0211122010??0044??311 Lithocarpus 021221201030004301313 Polygala 021112301011004001310 Lotus 021101201030004300310 Pomaderris 021101201020010001311 Luffa 021113201001004101312 Potentilla 0211122010201045??310 Maclura 0201111011000113??113 Prioria 021112201031004301313 Macrotyloma 021102200140011300312 Prunus 021112201030004501313 Maesopsis 0211012010000100??313 Psiguria 121124200140000101412 Malus 0212122010?00045??313 Psoralea 021112201000004411310 Maoutia 0201111001401100??121 Pterocarya 001002311100011011113 Marah 021223301020004401312 Pueraria 021112201020004101312 Margyricarpus 02110?3010301043??311 Pygeum 0211122010?00045??313 Medicago 0211122010310044??310 Pyrus 0212122010?0004501313 Melancium 021113201020004101312 Quercus 0211212000?1010301113 Melianthus 02121?2010200044??311 Quillaja 021212201020004501313 Microlobius 2????23?0140004711311 Ranunculus 021112200040011101310 Mildbraediodendron 021111201030004101313 Recchia 021111201020004101113 Millettia 021111201030004201312 Reissekia 0211022010200045??311 Mimosa 1????12?0101004310310 Retanilla 021101201000004501311 Momordica 021113201020004401312 Reynosia 021101201020002201311 Monnina 0211123010110040??311 Rhamnidium 0211012010200021??311 Mora 021112201000004001313 Rhamnus 021101201020002211311 Morus 0201111011001113??113 Rhoiptelea 021102201020111001113 Moutabea 0211123010100040??313 Robinia 0212112010300041??313 Mucuna 021112201000004111412 Rosa 021112201020104501311 Myrica 021102201100011001113 Ruptiliocarpon 02111?2010?00043??313 Neillia 0211112010?00042??311 Sageretia 0211012010200043??311 Neptunia 0211132010000045??310 Sanguisorba 0211122010?01101??310 Noltea 0211012010200043??311 Sarcopoterium 0211122010000103??311 Nothoalsomitra 0211132010?0004401312 Schistocarpaea 0211012010000043??313 Nothofagus 021002300040011001113 Schizocarpum 001114310140104601312 Octomeles 0211112010000044??113 Schizopepon 0211122010?0004401312

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Appendix 5. Continued. Appendix 5. Continued.

Taxon Democratic coding Taxon Democratic coding Scutia 0211012010200022??311 Trichosanthes 021113200000004001312 Senna 0211112010200041??313 Trifolium 0211122010300041??310 Shepherdia 021222201000000100313 Trigonobalanus 02111220100?010101313 Sicydium 021112201020004501312 Tylosema 02121?201000004101312 Sicyos 021113300040011401312 Ulex 0211122010?0004101311 Siolmatra 021112201020004501312 Umtiza 0212122010??004301310 Siraitia 021113201000004401312 Urera 0211112001400110??111 Solena 021113201020010001312 Urtica 0211112001400110??110 Sophora 0211112010010041??313 Vaughania 021122201020004300310 Sorbaria 0211112010200045??311 Vicia 021212201000004110312 Sorbus 0211122010200045??313 Vigna 021112200100104411312 Spatholobus 021112201020004101312 Wisteria 0211122010??0041??312 Stranvaesia 0211122010200042??313 Xanthophyllum 021112301010004001311 Stylobasium 021102201020004301101 Xerosicyos 0211122010?0004501312 Suriana 0211022010200043??111 Xylia 2???012?01401043??313 Swartzia 021111201020004101311 Zapoteca 2???023?014?0040??311 Tecunumania 021114210140104601312 Zehneria 021113201020004401312 Tetrameles 021110201000004301113 Zelkova 0210123001400113??113 Ticodendron 021112200140011101113 Ziziphus 0211012010200022??312 Trema 020111101100010101113 Zollernia 021111201030004101313

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