PHYLOGENETIC RELATIONSHIPS OF MONOCOTS BASED ON THE HIGHLY INFORMATIVE PLASTID GENE ndhF: EVIDENCE FOR WIDESPREAD CONCERTED CONVERGENCE

Thomas Givnish; J. Chris  Pires; Kenneth Sytsma; Tom Givnish; Heath O&#39;Brien

We used ndhF sequence variation to reconstruct relationships across 282 taxa representing 78 mono-cot families and all 12 orders. The resulting tree is highly resolved and places commelinids sister to Asparagales, with both sister to Liliales–Pandanales in the strict consensus; Pandanales are sister to Dioscoreales in the bootstrap majority-rule tree, just above Petrosaviales. Acorales are sister to all other monocots, with Alismatales sister to all but Acorales. Relationships among the four major clades of commelinids remain unresolved. Relationships within orders are consistent with those based on rbcL, alone or in combination with atpB and 18S nrDNA, and generally better supported: ndhF contributes more than twice as many informative characters as rbcL, and nearly as many as rbcL, atpB, and 18S nrDNA combined. Based on functional arguments, we hypothesized that net venation and fleshy fruits should both evolve—and thus undergo concerted convergence—in shaded habitats, and revert to parallel venation and dry, passively dispersed fruits in open, sunny habitats. Our data show that net venation arose at least 26 times and disappeared 9 times, whereas fleshy fruits arose 22 times and disappeared 11 times. Both traits arose together at least 15 times and disappeared together 5 times. They thus show a highly significant pattern of concerted convergence (P 10 9) and are each even more strongly associated with shaded habitats (P 10 10 to 10 23); net venation is also associated, as predicted, with broad-leaved aquatic plants. Exceptions to this pattern illustrate the importance of other selective constraints and phylogenetic inertia.

Aliso 22, pp. 28–51 䉷 2006, Rancho Santa Ana Botanic Garden PHYLOGENETIC RELATIONSHIPS OF MONOCOTS BASED ON THE HIGHLY INFORMATIVE PLASTID GENE ndhF: EVIDENCE FOR WIDESPREAD CONCERTED CONVERGENCE THOMAS J. GIVNISH,1,14 J. CHRIS PIRES,2,15 SEAN W. GRAHAM,3 MARC A. MCPHERSON,4,16 LINDA M. PRINCE,5 THOMAS B. PATTERSON,1 HARDEEP S. RAI,3 ERIC H. ROALSON,6 TIMOTHY M. EVANS,7 WILLIAM J. HAHN,8 KENDRA C. MILLAM,1 ALAN W. MEEROW,9 MIA MOLVRAY,10 PAUL J. KORES,10 HEATH E. O’BRIEN,11,17 JOCELYN C. HALL,12 W. JOHN KRESS,13 AND KENNETH J. SYTSMA1 Department of Botany, University of Wisconsin, Madison, Wisconsin 53706-1381, USA; 2Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706-1597, USA; 3UBC Botanical Garden and Centre for Plant Research, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada; 4Department of Agricultural, Food, and Nutritional Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada; 5Rancho Santa Ana Botanic Garden, Claremont, California 91711-3157, USA; 6School of Biological Sciences, Washington State University, Pullman, Wash. 99164-4236, USA; 7Department of Biology, Hope College, Holland, Michigan 49422-9000, USA; 8Department of Biology, Georgetown University, Washington, D.C. 20057-1003, USA; 9USDA-ARS-SHRS, National Germplasm Repository, and Fairchild Tropical Garden, Miami, Florida 33156, USA; 10Department of Biological Sciences, Moorpark College, Moorpark, California 93021-1695, USA; 11Department of Biology, Duke University, Durham, North Carolina 27708, USA; 12Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massassachusetts 02138, USA; 13National Museum of Natural History, Department of Botany, Smithsonian Institution, Washington, D.C. 20013-7012, USA 14Corresponding author (givnish@facstaff.wisc.edu) 1 ABSTRACT We used ndhF sequence variation to reconstruct relationships across 282 taxa representing 78 monocot families and all 12 orders. The resulting tree is highly resolved and places commelinids sister to Asparagales, with both sister to Liliales–Pandanales in the strict consensus; Pandanales are sister to Dioscoreales in the bootstrap majority-rule tree, just above Petrosaviales. Acorales are sister to all other monocots, with Alismatales sister to all but Acorales. Relationships among the four major clades of commelinids remain unresolved. Relationships within orders are consistent with those based on rbcL, alone or in combination with atpB and 18S nrDNA, and generally better supported: ndhF contributes more than twice as many informative characters as rbcL, and nearly as many as rbcL, atpB, and 18S nrDNA combined. Based on functional arguments, we hypothesized that net venation and fleshy fruits should both evolve—and thus undergo concerted convergence—in shaded habitats, and revert to parallel venation and dry, passively dispersed fruits in open, sunny habitats. Our data show that net venation arose at least 26 times and disappeared 9 times, whereas fleshy fruits arose 22 times and disappeared 11 times. Both traits arose together at least 15 times and disappeared together 5 times. They thus show a highly significant pattern of concerted convergence (P ⬍ 10⫺9) and are each even more strongly associated with shaded habitats (P ⬍ 10⫺10 to 10⫺23); net venation is also associated, as predicted, with broad-leaved aquatic plants. Exceptions to this pattern illustrate the importance of other selective constraints and phylogenetic inertia. Key words: adaptation, biomechanics, correlated evolution, DISCRETE, seed dispersal, submersed plants, tropical forests. INTRODUCTION Monocotyledons—with roughly 60,000 species, 92 families, and 12 orders—are the most diverse, morphologically varied, and ecologically successful of the early-divergent angiosperms. Over the past ten years, molecular systematics has revolutionized our understanding of higher-level relationships within the monocots and made them among the best understood in the angiosperms (Chase et al. 1993, 1995a, b, 2000, 2006; Givnish et al. 1999; Bremer 2000, Present addresses: 15 Division of Biological Sciences, 371 Life Sciences Center, University of Missouri, Columbia, Missouri 652117310, USA; 16 Department of Biology, Duke University, Box 90338, Durham, North Carolina 27708, USA; 17 Department of Agriculture, Food and Nutritional Science, University of Alberta, Edmonton, Alberta T6G 2P5, Canada. 2002; Kress et al. 2001; Caddick et al. 2002a, b; Hahn 2002; Patterson and Givnish 2002; Pires and Sytsma 2002; Michelangeli et al. 2003; Zanis et al. 2003; Graham et al. 2006; McPherson et al. submitted). Such studies have laid the groundwork for rigorous studies of adaptive radiation, geographic diversification, and the evolution of development, independent of phenotypic convergence among distantly related groups or divergence among close relatives. Based on a cladistic analysis of more than 500 rbcL sequences, Chase et al. (1995a, b) identified six major clades of monocotyledons: commelinids (including Poales, Commelinales, Zingiberales, Dasypogonales, and Arecales), Asparagales, Liliales, Pandanales, Dioscoreales, and Alismatales, with Acorus L. sister to all other monocots. However, even when Chase et al. (2000) complemented these data with sequences of atpB plastid DNA and 18S nrDNA for a subset VOLUME 22 Monocots: Concerted Convergence of 140 species—more than tripling the number of nucleotides scored per taxon—relationships among many major clades remained unresolved or weakly supported, and evolutionary ties among several groups of commelinids and asparagoids remained unclear. To contribute to efforts to resolve these higher-level relationships and investigate the possibility of widespread concerted convergence and plesiomorphy in ecologically significant traits across the monocots, we decided to produce a well-resolved, highly inclusive monocot phylogenetic analysis based on sequences of the plastid gene ndhF. This gene provides abundant data for phylogenetic reconstruction: it is more than 50% larger than rbcL (ca. 2200 base pairs [bp] vs. ca. 1428 bp) and has substantially more variable positions (Gaut et al. 1997; Patterson and Givnish 2002). Our ndhF tree is also ideally suited for analyzing patterns of repeated convergence and divergence among the monocots: it entails many more characters, better resolution, and higher levels of support for individual clades than phylogenetic trees based on rbcL alone (albeit for fewer taxa), while incorporating many more taxa than the existing three-gene tree (Chase et al. 2000) based on rbcL, atpB, and 18S nuclear ribosomal DNA (nrDNA), or the 7- and 17-gene trees now in preparation (Chase et al. 2006; Graham et al. 2006). Concerted convergence (Givnish and Sytsma 1997a, b; Givnish and Patterson 2000; Patterson and Givnish 2002) is the independent rise in different lineages under similar ecological conditions of two or more traits that are genetically, developmentally, and functionally unrelated; concerted plesiomorphy involves the retention of the same suite of traits in different lineages under similar conditions (Patterson and Givnish 2002). These phenomena might result from adaptations of unrelated traits to the same environmental conditions, or (possibly more likely) to different components of the shared set of conditions. They should be challenging to detect and study using analyses based on phenotypic data, given that multiple (and seemingly independent) characters would carry the same, misleading ‘‘signal’’ regarding evolutionary relationships. Patterson and Givnish (2002) demonstrated that concerted convergence and plesiomorphy occur among the monocots in the order Liliales. Phylogenetic reconstruction demonstrated that (1) visually showy flowers, capsular fruits, winddispersed seeds, narrow leaves, parallel venation, and bulbs arose upon invasion of open seasonal habitats, and (2) visually inconspicuous flowers, fleshy fruits, animal-dispersed seeds, broad thin leaves, net venation, and rhizomes persisted in lineages inhabiting ancestral forest understories. For each trait, the observed variation in phenotype with environment across lineages appeared to be functionally adaptive (Givnish and Patterson 2000; Patterson and Givnish 2002). Two of these patterns of concerted convergence and plesiomorphy may hold throughout the monocots. Specifically, we predict that net venation and vertebrate-dispersed fleshy fruits should frequently evolve and be retained with each other under shady conditions in forest understories, and that parallel venation and nonfleshy fruits (dispersed by wind, water, or gravity) should frequently evolve and be retained with each other in open habitats. These predictions are based on the biomechanical economy of branched vs. unbranched support networks in thin leaves adapted to shady conditions, 29 and on the efficiency of dispersal via vertebrates vs. more passive means in less windy forest understories. Shady conditions favor thin, broad leaf laminas, which cannot support themselves mechanically (especially after small losses of turgor pressure), and therefore require longitudinal and lateral reinforcement from primary and secondary veins (Givnish 1979, 1987). The cost per unit length of such veins scales like their diameter squared, whereas their strength scales like diameter cubed, favoring the coalescence of nearby, subparallel veins into one or few branching ribs of lower cost (Givnish 1979, 1995). Thus, the broader and thinner a lamina or its divisions, the greater should be the advantage of net venation and the greater the advantage of a single midrib. Givnish et al. (submitted) argue that soft, thin, broad leaves are also favored in fast-growing, emergent aquatic plants with access to abundant moisture and nutrients (e.g., Sagittaria L.), and in filmy-leaved submersed species adapted for photosynthesis underwater (e.g., Aponogeton L. f.). Net venation should thus also be selectively favored in such plants. In addition, whereas wind dispersal of seeds is likely to be effective in open, windy habitats, animal dispersal of fleshy fruits should be more effective below closed habitats (Croat 1978; Givnish 1998). In Neotropical rain forests, up to 95% of the woody understory species (mostly dicots) bear fleshy fruits dispersed by birds, bats, or nonvolant mammals (Gentry1982). In this paper, we evaluate these hypotheses by deriving a well-resolved monocot phylogenetic tree based on ndhF sequence variation. We compare the resulting clades with those previously resolved based on rbcL, atpB and 18S nrDNA sequence variation. Finally, we use the ndhF tree to test whether fleshy fruits, net venation, and occurrence in shady forest understories show significant patterns of concerted convergence under shady conditions. MATERIALS AND METHODS Phylogenetic Analyses We included 282 monocot species in our analysis, representing as broad and representative a group of taxa as possible, including members of 78 of 92 families and all 12 orders (Table 1). Families and orders follow APG II (2003), except that we recognize Dasypogonales as equaling Dasypogonaceae (see Givnish et al. 1999; Doweld 2001; Reveal and Pires 2002), and Petrosaviales (Cameron et al. 2003). Most of the families unsampled are small, and several are nonphotosynthetic (e.g., Corsiaceae) or occur in wet or submerged habitats (e.g., Anarthriaceae, Posidoniaceae). The families not represented comprise only 1.2% of all monocot species. Only four (Burmanniaceae, Cyclanthaceae, Hydrocharitaceae, Potamogetonaceae) involve substantial numbers of taxa (100–225 species per family). We used Ceratophyllum L. as the outgroup, given its position sister to the monocots in several recent analyses (Soltis et al. 1997, 2000; Graham and Olmstead 2000; Zanis et al. 2002; Borsch et al. 2003). Total DNAs were extracted from fresh, deep-frozen, or silica gel-dried leaf material. We amplified and sequenced ndhF for most taxa ourselves following standard techniques (see Patterson and Givnish 2002), obtaining both forward and reverse strands in most cases. New sequences were uploaded to GenBank and accession numbers obtained; se- 30 Givnish et al. ALISO Table 1. Classification, GenBank accession numbers, vouchers, and authors for the 283 ndhF sequences included in this study. Nomenclature follows Bremer et al. (2002) for orders and families (including ‘‘bracketed’’ taxa), and the International Plant Name Index (2004) for generic names, specific epithets, and taxonomic authorities. Specimens sampled include herbarium vouchers, accessions of living plants provided by various botanical gardens, and, in a few instances, initial citations. Material from curated living collections is designated by institution, followed by accession number. Abbreviations are as follows: ADBG (Adelaide Botanical Garden), ADU (University of Adelaide), NYBG (New York Botanical Garden), SEL (Marie Selby Botanical Garden), SIRG (Smithsonian Institution Research Greenhouses), and UCBG (University of California—Berkeley Botanical Garden). Order and family GenBank Voucher, accession, or citation Acorus calamus L. AY007647.2 H. O’Brien A. gramineus Aiton AF546992 Denver Botanic Garden, no voucher (RGO 97-149 DNA) Rothwell & McPherson/Williams s. n., ALTA Aponogetonaceae Araceae Alisma plantago-aquatica L. Sagittaria latifolia Willd. Aponogeton elongatus Benth. Arisaema fraternum Schott Gymnostachys anceps R. Br. Spathiphyllum wallisii Hort. AF546993 AY007657.2 AY191195 AF546995 AY191196 AY007658.2 Buzgo 1013, ALTA Barrett s. n., TRT Hahn s. n., WIS Buzgo 953, ALTA Chase 3841, K Chase 210, NCU Butomaceae Cymodoceaceae Juncaginaceae Limnocharitaceae Butomus umbellatus L. Halodule wrightii Asch. Triglochin maritimum L. Hydrocleys Rich. sp. AF546997 AY191197 AF546998 AY191198 Scheuchzeriaceae Scheuchzeria palustris L. AF547007 Tofieldiaceae Tofieldia glutinosa (Michx.) Pers. AF547023 Chase 6414, K Kolterman s. n., WIS Buzgo 1011, ALTA U Wisconsin—Madison Botanical Garden Waterway & Graham 97-60, ALTA Morton & Venn 9282, ALTA L. Rollins H. O’Brien J. C. Pires L. Rollins J. C. Pires H. O’Brien & S. Graham L. Rollins J. C. Pires L. Rollins J. C. Pires Zosteraceae Zostera angustifolia (Hornem.) Rchb. AF547022 Chase 2795-W2, K M. A. McPherson & H. O’Brien H. Rai & L. Rollins Japonolirion osense Nakai AY191199 Chase 3000, K J. C. Pires Dioscorea bulbifera L. AY007652.2 H. O’Brien Tacca chantieri André Trichopus sempervirens (H. Perrier) Caddick & Wilkin Aletris farinosa L. Narthecium ossifragum Huds. AY191200 AF546996 EPO Biology, U Colorado—Boulder, no voucher (RGO 97-151 DNA) Hahn 6977, WIS Caddick 304, K J. C. Pires L. Rollins AY191201 AY191202 Smith et al. 2263, WIS Chase 610, K J. C. Pires J. C. Pires Pandanus utilis Bory Croomia japonica Miq. Stemona tuberosa Lour. Stichoneuron caudatum Ridl. Vellozia Vand. sp. Talbotia elegans Balf. AY191203 AF547002 AF547009 AF547010 AF546999 AF547011 Hahn 6898, WIS Rothwell & Stockey Rothwell & Stockey Rothwell & Stockey Kubitzki & Feuerer Rothwell & Stockey J. C. Pires M. A. McPherson M. A. McPherson M. A. McPherson L. Rollins M. A. McPherson Alstroemeria L. sp. Calochortus albus Dougl. ex Benth. C. apiculatus Baker C. weedii Wood Prosartes maculata A. Gray Scoliopus bigelovii Torr. Streptopus amplexifolius DC. S. lanceolatus (Aiton) J. L. Reveal Tricyrtis affinis Makino T. latifolia Maxim. Campynema lineare Labill. Androcymbium ciliolatum Schltr. & K. Krause Disporum flavens Kitagawa Uvularia sessilifolia J. F. Gmel. Wurmbea pygmaea (Endl.) Benth. AF276011 AF275994 Anderson 13653, MICH Patterson 13, WIS T. B. Patterson T. B. Patterson AF275995 AF275998 AF276015 AF276017 AF276019 AF276020 Patterson 1060, WIS Patterson 18, WIS Foster s. n., Messiah Coll. Kalt 9278, WIS Foster s. n., Messiah Coll. Foster s. n., Messiah Coll. T. T. T. T. T. T. B. B. B. B. B. B. Patterson Patterson Patterson Patterson Patterson Patterson AF276021 AF276022 AF276013 AF276012 Chase 2777, K Patterson 1070, WIS Walsh 3488, MEL Chase 272, NCU T. T. T. T. B. B. B. B. Patterson Patterson Patterson Patterson AY438618 AF276023 AF547012 Millam 1307, WIS Patterson 10, WIS Case 77, PERTH K. C. Millam T. B. Patterson M. A. McPherson Acorales Acoraceae Alismatales Alismataceae Petrosaviales Petrosaviaceae Dioscoreales Dioscoreaceae Nartheciaceae Pandanales Pandanaceae Stemonaceae Velloziaceae Liliales Alstroemeriaceae Calochortaceae Campynemataceae Colchicaceae Species 43, ALTA 46, ALTA 45, ALTA 97-3, HBG 48, ALTA Author H. O’Brien M. A. McPherson VOLUME 22 Table 1. Monocots: Concerted Convergence 31 Continued. Order and family Liliaceae Melianthiaceae Philesiaceae Ripogonaceae Smilacaceae Asparagales Agapanthaceae Agavaceae Species Cardiocrinum giganteum Makino var. yunnanense Makino Clintonia borealis Raf. Erythronium albidum Nutt. Fritillaria meleagris L. Gagea wilczekii Braun-Blanquet & Maire Lilium kelleyanum Lemmon L. superbum L. Lloydia serotina Sweet Medeola virginiana L. Nomocharis pardanthina Franch. Notholirion bulbuliferum (Lingelsh.) Stearn Tulipa pulchella Fenzl Trillium flexipes Raf. Veratrum viride Aiton Xerophyllum tenax (Pursh) Nutt. Philesia buxifolia Lam. ex Poir. Ripogonum elseyanum F. Muell. Smilax hispida Muhl. Agapanthus africanus Beauverd Agave celsii Hook. A. parviflora Torr. Anemarrhena asphodeloides Bunge Anthericum liliago Linn. Behnia reticulata Didr. Camassia quamash (Pursh) Greene Chlorophytum alismaefolium Baker Herreria salsaparilha Mart. Hosta ventricosa (Salisb.) Stearn Yucca glauca Nutt. Alliaceae Amaryllidaceae Aphyllanthaceae Asparagaceae Asteliaceae Allium haematochiton S. Watson A. textile A. Nels. & J. F. Macbr. Ipheion dialystemon Guaglianone Leucocoryne coquimbensis F. Phil. Amaryllis paradisicola D. A. Snijman Boophone disticha (L. f.) Herb. Cyrtanthus herrei (Leighton) R. A. Dyer Eustephia darwinii Vargas Griffinia parviflora Ker Gawl. Hippeastrum reticulatum Herb. Hymenocallis tubiflora Salisb. Leucojum aestivum L. Narcissus elegans (Haw.) Spach Paramongaia weberbaueri Velarde Proiphys cunninghamiana (Lindl.) Habb. Scadoxus membranaceus (Baker) Friis & Nordal Sternbergia lutea Spreng. Ungernia flava Boiss. & Haussk. ex Boiss. Aphyllanthes monspeliensis L. Asparagus falcatus L. Astelia banksii A. Cunn. A. fragrans Colenso Collospermum hastatum (Colenso) Skottsb. GenBank Voucher, accession, or citation Author AF275999 AF276000 AF276001 AF276002 AF276003 AF276004 Chase 3689, K Chase 935, K Patterson s. n., WIS Patterson 1069, WIS Patterson 1068, WIS Chase 748, K T. T. T. T. T. T. B. B. B. B. B. B. AF276005 AY007655.2 AF276006 AF276007 AF276008 AF276009 Felson 13, WIS Chase 112, NCU Jones s. n., K Patterson 1065, WIS Chase 934, K Patterson s. n., WIS T. B. Patterson H. O’Brien T. B. Patterson T. B. Patterson T. B. Patterson T. B. Patterson AF276010 AY191205 AF276024 AY191204 AF276014 AF276016 AF276018 Patterson 1066, WIS Givnish, no voucher Chase 551, K Pires 99-072, WIS Chase 545, K Chase 187, NCU Givnish s. n., WIS T. B. Patterson J. C. Pires T. B. Patterson J. C. Pires T. B. Patterson T. B. Patterson T. B. Patterson AF508405 AF508398 AF508399 AY191162 UCBG 45.0288, UC UCBG 65.1883, UC UCBG 67.0582, UC Chase 1022, K J. J. J. J. AF508402 AY191168 AF547001 UCBG 93.0946, UC Goldblatt 9273, MO Coxson & Kuijt 5060, ALTA J. C. Pires J. C. Pires M. A. McPherson AF508400 AY191163 UCBG 86.949, UC ADBG G951045, ADU J. C. Pires J. C. Pires AY191178 AF508401 AF547014 J. C. Pires J. C. Pires M. A. McPherson AY191160 AF547000 AF508406 AF508407 AY191161 Chase 2154, K UCBG 87.0576, UC Addicott, McPherson, & Hurlburt, no voucher (SWG 00121DNA) UCBG 90.0117, UC McPherson 990704-79, ALTA UCBG 93.0448, UC UCBG 94.1335, UC van Jaarsveld 13263, NBG AY434486 AY434484 Malan 121, NBG van Zyl 104, NBG A. W. Meerow A. W. Meerow AY434479 AY434478 AY434481 AY434482 AF547024 U79216 AY434480 Meerow 2436, FTG Meerow 2389, FTG Meerow 2407, FTG Meerow 2240, FTG Graham 00-4-2, ALTA Barrett 1434, TRT Meerow 2303, FTG A. W. Meerow A. W. Meerow A. W. Meerow A. W. Meerow M. A. McPherson S. W. Graham A. W. Meerow AY434487 Meerow 1188, FTG A. W. Meerow AY434485 Meerow 2240, FTG A. W. Meerow U79224 AY434483 Barrett 1434, TRT Meerow 2436, FTG M. A. McPherson A. W. Meerow AY191167 AF508403 AY191164 AY191165 AY191166 Chase 614, K Hahn 6881, WIS Chase 1072, K ADBG G900014, ADU ADBG G87567, ADU J. J. J. J. J. C. C. C. C. Patterson Patterson Patterson Patterson Patterson Patterson Pires Pires Pires Pires J. C. Pires M. A. McPherson J. C. Pires J. C. Pires J. C. Pires C. C. C. C. C. Pires Pires Pires Pires Pires 32 Givnish et al. Table 1. ALISO Continued. Order and family Asphodelaceae Blandfordiaceae Boryaceae Hemerocallidaceae Hyacinthaceae Hypoxidaceae Iridaceae Ixioliriaceae Lanariaceae Laxmanniaceae Orchidaceae Ruscaceae Tecophilaeaceae Themidaceae Xanthorrhoeaceae Xeronemataceae Species Asphodelus L. sp. Blandfordia punicea (Labill.) Sweet Alania endlicheri Kunth Borya septentrionalis F. Muell. Arnocrinum preissii Lehm. Caesia calliantha R. J. F. Henderson Dianella ensifolia (L.) DC. Geitonoplesium cymosum R. Br. Hensmania turbinata (Endl.) W. Fitzg. Johnsonia pubescens Lindl. Phormium cookianum Le Jolis Tricoryne elatior R. Br. Albuca pendula B. Mathew A. setosa Jacq. Hyacinthus orientalis Linn. Muscari comosum (L.) P. Miller Ornithogalum caudatum Aiton O. juncifolium Jacq. O. longebractatum Jacq. Scilla natalensis Planch. Hypoxis juncea Sm. Gladiolus L. spp. Iris missouriensis Nutt. I. tenax Dougl. Sisyrinchium montanum Greene Ixiolirion tataricum (Pall.) Herb. & Traub Lanaria lanata Druce Arthropodium cirratum R. Br. Cordyline fruticosa (L.) A. Chev. Eustrephus latifolius R. Br. Lomandra longifolia Labill. Diuris laxiflora Lindl. GenBank Voucher, accession, or citation Author AF508409 AY191169 Pires 99-132, WIS Chase 519, K AY191170 AY225959 AY191172 AY191173 Conran 707, Chase 2205, Conran 953, Conran 826, DQ058413 AY191174 AY191175 Hahn 6869, WIS ADBG G880709, ADU Conran 946, ADU J. C. Hall J. C. Pires J. C. Pires AY191176 AY191177 AY191206 AF508390 AF508391 AF508393 AF547006 AF508394 AF508395 AF508396 AF508397 AJ535775 AY191180 AF547003 AY191181 AF547008 AY191182 Chase 2213, K ADBG G881651, ADU Conran 827, ADU Hannon 94565, RSA UCBG 53.0370, UC Hahn 6861, WIS Harder 000419-1, ALTA Hort. UW Botany UCBG 96.0458, UC UCBG 47.0533, UC UCBG 77.0338, UC Chase DNA 5946, K Hahn 6970, WIS McPherson 000707-5a-7, ALTA Pires 99-077, WIS McPherson 990704-71, ALTA Chase 489, K J. C. Pires J. C. Pires J. C. Pires J. C. Pires J. C. Pires J. C. Pires M. A. McPherson J. C. Pires J. C. Pires J. C. Pires J. C. Pires J. C. Pires J. C. Pires M. A. McPherson J. C. Pires M. A. McPherson J. C. Pires AY191183 AY191184 AY225023 AY191185 AF547004 AJ535765 Goldblatt 9410, MO Chase 651, NCU Hahn 6932, WIS Chase 193, NCU Vitt 27411, ALTA Kores & Molvray 209, K Epipactis helleborine (L.) Crantz AJ535763 Chase 199, K Neuwiedia veratifolia Blume Ridleyella paniculata (Ridl.) Schltr. Spiranthes cernua (L.) L. C. Rich. Tropidia effusa Rchb. f. Convallaria majalis L. Dracaena aubryana Brongn. ex E. Morr. Maianthemum racemosum (L.) Link Nolina interrata Gentry Ophiopogon wallichianus (Kunth) Hook. f. Polygonatum hookeri Baker P. pubescens Pursh Cyanastrum cordifolium Oliv. Cyanella hyacinthoides L. Tecophilaea violiflora Bertero ex Colla Bessera elegans Schult. f. Brodiaea elegans Hoover Dichelostemma congestum Kunth Milla biflora Cav. Muilla maritima S. Watson Triteleia grandiflora Lindl. Xanthorrhoea semiplana F. Muell Xeronema callistemon W. R. B. Oliv. U20633 AJ535768-70 Kew DNA O-460 Hort. Botanicus Leiden 31692 AJ535761 Chase 81941 402, K AJ535766-7 AF508404 AY191186 Kores & Molvray 301, K Hahn 6867, WIS Chase 1102, K J. C. Pires J. C. Pires J. C. Pires J. C. Pires M. A. McPherson P. Kores & M. Molvray P. Kores & M. Molvray R. Neyland P. Kores & M. Molvray P. Kores & M. Molvray R. Neyland J. C. Pires J. C. Pires AF547005 McPherson 990704-97, ALTA M. A. McPherson AY191188 AY191189 ADBG W920633, ADU Chase 2865, K J. C. Pires J. C. Pires AY191190 AY191191 U79228 AY191192 AY191193 Chase 492, K Chase 481, K Graham & Barrett 2, TRT ADBG G870862, ADU Chase 1498, K J. C. Pires J. C. Pires M. A. McPherson J. C. Pires J. C. Pires AF508351 AF508357 AF508366 AF508371 AF508375 AF508380 AY191207 AY191194 Pires 99-153, WIS Pires 96-045, WIS Pires 96-030, WIS Rodriguez 2634, IBUG Pires 98-028, WIS Hufford 2776, WIS ADBG W922097, ADU ADBG G850899, ADU J. J. J. J. J. J. J. J. ADU K ADU ADU J. C. Pires J. C. Pires J. J. J. J. C. C. C. C. C. C. C. C. C. C. C. C. Pires Pires Pires Pires Pires Pires Pires Pires Pires Pires Pires Pires VOLUME 22 Table 1. Monocots: Concerted Convergence Continued. Order and family Arecales Arecaceae Dasypogonales Dasypogonaceae Commelinales Commelinaceae Haemodoraceae Species W. Hahn W. Hahn AY044558 AY044563 Hahn 7384, WIS Hahn 7077, WIS W. Hahn W. Hahn AY044523 AY044531 AY044540 AY044537 Hahn Hahn Hahn Hahn 6390, 6627, 6897, 6370, WIS WIS WIS WIS W. W. W. W. Hahn Hahn Hahn Hahn AY044562 AY044547 AY044548 AY044525 AY044529 AY044544 Hahn Hahn Hahn Hahn Hahn Hahn 7085, 7642, 7641, 7106, 6899, 6392, WIS WIS WIS WIS WIS WIS W. W. W. W. W. W. Hahn Hahn Hahn Hahn Hahn Hahn AY044551 Hahn 7811, WIS W. Hahn AY191210 Hahn 7057, WIS J. C. Pires Calectasia intermedia Sond. Dasypogon bromeliifolius R. Br. AY191208 AY191209 Chase 456, K Rudall 29, K J. C. Pires J. C. Pires Amischotolype monosperma (C. B. Clarke) I. M. Turner Aneilema calceolus Brenan Cartonema philydroides F. Muell. Spatholirion longifolium Dunn Anigozanthos flavidus DC. Lachnanthes Ell. sp. Xiphidium caeruleum Aubl. AY198178 Bogner 1811 T. M. Evans AY198180 AY198181 AY198179 AF546994 AY191211 AF547013 T. M. Evans T. M. Evans T. M. Evans H. O’Brien J. C. Pires M. A. McPherson AY125006 AY007654 AY191212 U41622 U41599 Faden & Faden 77/565, US Hort. Munich Bot. Gard. s. n. Chase 593, K Neyland 1884, MCN Hahn 6973, WIS SDSU greenhouse (coll. M. Simpson) SWG 5.7.94 DNA Kress 99-6325, US Sirirugsa s. n., SONG Sirirugsa s. n., SONG Graham & Barrett 1, TRT Barrett 814, TRT U41608 Barrett 1054, TRT M. A. McPherson U41606 U41615 Barrett 1414, TRT Barrett 1415, TRT M. A. McPherson M. A. McPherson AY191214 Hahn 6912, WIS J. C. Pires AY191215 AY124997 Sytsma s. n., WIS Kress 94-3601, US J. C. Pires L. M. Prince AY124996 AY191216 AY191217 AY125003 Kress 90-2984, US Hahn 6921, WIS Kress & Beach 87-2159, US Duke 287935 L. M. Prince J. C. Pires J. C. Pires L. M. Prince AY191218 AY125004 Kress 94-3724, US Kress 78-0894, US J. C. Pires L. M. Prince AY125005 Kress 98-6288, US L. M. Prince AY124993 Kress 94-5321, US L. M. Prince AY191219 AY124992 Sytsma 7203, WIS Kress 94-3709, US J. C. Pires L. M. Prince Philydrum lanuginosum Gaertn. Eichhornia crassipes (Mart.) Solms Heteranthera limosa (Swartz) Willd. Hydrothrix gardneri Hook. f. Monochoria korsakovii Reg. & Maack Heliconiaceae Lowiaceae Marantaceae Author Hahn 6363, WIS Hahn 7047, WIS Philydraceae Pontederiaceae Costaceae Voucher, accession, or citation AY044535 AY044564 Hanguana Blume sp. H. malayana (Jack) Merr. Zingiberales Cannaceae GenBank Areca vestiaria Giseke Allagoptera arenaria (Gomes) Kuntze Bactris humilis (Wall.) Burret Beccariophoenix madagascariensis Jum. & H. Perrier Calamus caesius Blume Caryota mitis Lour. Chamaedorea seifrizii Burret Drymophloeus litigiosus (Becc.) H. E. Moore Elaeis oleifera (Kunth) Cortés Leopoldinia pulchra Mart. Manicaria saccifera J. Gaertn. Nypa fruticans Wurmb. Phoenix dactylifera L. Ravenea hildebrandtii C. D. Bouché Reinhardtia simplex (Wendl.) Drude ex Dammer Serenoa repens (W. Bartram) Small Hanguanaceae Musaceae 33 Canna polymorpha Lodd. ex Loud. Costus pulverulentus Presl Dimerocostus strobilaceus Kuntze Tapeinochilos Miq. sp. Heliconia latispatha Benth. Orchidantha fimbriata Holttum Calathea foliosa Rowlee ex Woodson & Schery Maranta leuconeura E. Morr. Marantochloa purpurea (Ridley) Milne-Redhead Thaumatococcus daniellii (Benn.) Benth. & Hook. f. Ensete ventricosum (Welw.) E. E. Cheesm. Musa L. sp. Musella lasiocarpa (Fr.) Wu ex H. W. Li L. M. Prince S. W. Graham J. C. Pires S. W. Graham S. W. Graham 34 Givnish et al. Table 1. ALISO Continued. Order and family Strelitziaceae Zingiberaceae Poales Bromeliaceae Cyperaceae Ecdeiocoleaceae Eriocaulaceae Flagellariaceae Joinvilleaceae Juncaceae Species Phenakospermum guyanense Endl. Ravenala madagascariensis J. F. Gmel. Strelitzia Aiton sp. Alpinia galanga (L.) Willd. Globba curtisii Holttum Hedychium flavescens Carey ex Rosc. Riedelia Trin. ex Kunth sp. Siphonochilus kirkii (Hook.) B. L. Burtt Zingiber officinale Roscoe Aechmea haltonii H. Luther Ananas ananassoides (Baker) L. B. Sm. Brewcaria reflexa (L. B. Sm.) B. K. Holst Brocchinia acuminata L. B. Sm. B. paniculata Schult. F. Bromelia Adans. sp. Canistrum giganteum (Baker) L. B. Sm. Catopsis wangerini Mez & Werckle Cryptanthus beuckeri E. Morren Deuterocohnia longipetala Mez Dyckia Schult. f. sp. Encholirium Mart. ex Schult. sp. Fosterella penduliflora (C. H. Wright) L. B. Sm. Glomeropitcairnia penduliflora Mez Guzmania monostachya Rusby Hechtia lundelliorum L. B. Sm. Hohenbergia disjuncta L. B. Sm. Mezobromelia pleiosticha J. F. Utley & H. Luther Navia saxicola L. B. Sm. Nidularium selloanum (Baker) E. Pereira & Leme Pitcairnia carinata Mez Puya aequatorialis André Tillandsia complanata Benth. Vriesea viridiflora (Regel) J. R. Grant Carex dioica L. Cladium californicum (S. Watson) O’Neill Dulichium arundinaceum (L.) Britt. Eleocharis elegans (Kunth) Roem. & Schult. Gahnia deusta (R. Br.) Benth. Mapania paradoxa Raynal Rhynchospora corniculata (Lam.) A. Gray Scirpus nevadensis S. Watson Ecdeiocolea monostachya F. Muell. Eriocaulon compressum Lam. Tonina fluviatilis Aubl. Flagellaria indica L. Joinvillea ascendens Gaudich. Juncus effusus L. GenBank Voucher, accession, or citation Author AY124995 Kress 86-2099D, US L. M. Prince AY124994 Kress 92-3504, US L. M. Prince AY191220 AY125002 AY125001 AY124998 Sytsma 7204, WIS SIRG 94-753 Kress 99-6347, US Kress 99-6590, US J. C. Pires L. M. Prince L. M. Prince L. M. Prince AY125000 AY124999 SIRG 98-025 Kress 94-3692, US L. M. Prince L. M. Prince AY191221 Sytsma 7205, WIS J. C. Pires L75844 L75845 SEL 85-1447 Brown 3129, RM R. G. Terry et al. R. G. Terry et al. AY208982 Givnish et al. 1997 K. C. Millam L75859 AY208981 L75860 L75861 SEL 81-1937 Fernandez 8236, PORT Brown 3128, RM Brown 3183, RM R. K. R. R. L75855 Palacı́ 1235, RM R. G. Terry et al. L75856 AY208984 L75857 L75862 L75863 SEL 89-499 Hort. Marnier-Lapostelle s. n. Brown 3131, RM SEL 1984-0364 SEL 69-1976-12 R. K. R. R. R. L75864 Givnish s. n., WIS R. G. Terry et al. L75865 AY208985 L75906 L75891 SEL SEL SEL SEL R. K. R. R. AY208983 L75894 Givnish et al. 1997 Leme 1830, HB K. C. Millam R. G. Terry et al. L75902 L75903 L75899 L75910 Brown 3173, RM SEL 93-211 SEL 79-0519 SEL 78-757 R. R. R. R. AF191808 A. C. Yen AY129249 Royal Botanic Garden, Edinburgh 19851401 Swearingen 1596, RSA E. H. Roalson AY129250 Williams 1441, RSA E. H. Roalson AY129258 Roalson 1458, WS E. H. Roalson AY129253 AY129256 AY129252 Overton 2708, RSA Granville 13232, US Roalson 1276, WS E. H. Roalson E. H. Roalson E. H. Roalson AY129254 AY438617 Helmkamp s. n., RSA Hopper 8531, K E. H. Roalson M. A. McPherson AF547017 AY198182 U22008 U21973 AF547015 Unwin 241, MU Givnish 3109, WIS Clark & Zhang 1305, ISC NYBG 800379 Rai 1004, ALTA H. Rai T. M. Evans J. F. Wendel J. F. Wendel H. Rai 82-225 85-1005 83-393 81-1986 G. C. G. G. G. C. G. G. G. G. C. G. G. G. G. G. G. Terry et al. Millam Terry et al. Terry et al. Terry et Millam Terry et Terry et Terry et al. al. al. al. Terry et al. Millam Terry et al. Terry et al. Terry Terry Terry Terry et et et et al. al. al. al. VOLUME 22 Table 1. Monocots: Concerted Convergence 35 Continued. Order and family Mayacaceae Poaceae Species Mayaca fluviatilis Aubl. Anomochloa marantoidea Brongn. Arundo donax L. Avena sativa L. Bambusa stenostachya Hack. Brachyelytrum erectum (Schreb.) P. Beauv. Chusquea circinata Soderstr. & C. E. Calderón Coix lacryma-jobi L. Restionaceae Thurniaceae Typhaceae Xyridaceae Voucher, accession, or citation Author DQ058414 U21992 Berry 3004, WIS Clark 1299, ISC J. C. Hall J. F. Wendel U21998 U22000 U21967 U22005 Clark s. n., ISC Zhang 8400174, ISC Zhang 8400174, ISC Clark 1330, ISC J. J. J. J. U21990 Quail Botanical Garden J. F. Wendel AF117403 R. Spangler et al. AF164777 U22003 U21978 USDA Plant Identification Number (MIN) Kobayashi et al. 1539, ISC Wise, no voucher, ISU Clark 1298, ISC U21971 NC㛮001320 Londoño & Clark 911, ISC Hiratsuka et al. 1989 Panicum virgatum L. Phaenosperma globosa Munro Pharus lappulaceus Aubl. Phyllostachys edulis Mazel ex J. Houz. Poa pratensis L. Schizachyrium scoparium Nash Sorghastrum nutans Nash Sporobolus indicus (L.) R. Br. Tripsacum dactyloides Schltr. Zea mays L. U21986 U22006 U21994 U21970 Clark Clark Clark Clark U21980 AF117420 AF117421 U21983 AF117433 NC㛮001666 Clark 1156, ISC Kellogg V48, GH Clark 1641, ISC Clark 1293, ISC Kellogg V49, GH Maier et al. 1995 Zoysia matrella Druce Amphiphyllum rigidum Gleason U21975 AF207638 Cephalostemon flavus (Link) Steyerm. Epidryos guayanensis Maguire Guacamaya superba Maguire AF207624 Kunhardtia rhodantha Maguire AF207635 Marahuacaea schomburgkii (Maguire) Maguire Maschalocephalus dinklagei Gilg & K. Schum. Monotrema bracteatum Maguire AF207633 Clark 1174, ISC Fernández, Stergios, Givnish, & Funk 8061, PORT Smith, Sytsma, & Givnish 303, WIS Berry & Brako 5539, WIS Smith, Sytsma, & Givnish 301, WIS Smith, Sytsma, & Givnish 300, WIS Fernández, Stergios, Givnish, & Funk 8205, PORT Assı́ s. n., Côte d’Ivoire 5/95 Potarophytum riparium Sandwith Rapatea paludosa Aubl. AF207627 AF207623 Saxofridericia regalis Schomb. AF207637 Schoenocephalium cucullatum Maguire Spathanthus bicolor Ducke S. unilateralis Desv. AF207634 Guaduella marantifolium Franch. Hordeum vulgare L. Lithachne pauciflora (Sw.) P. Beauv. Olyra latifolia L. Oryza sativa L. Rapateaceae GenBank Stegolepis hitchcockii subsp. morichensis Maguire Elegia fenestrata Pillans Prionium serratum E. Mey. Thurnia sphaerocephala Hook. f. Sparganium L. sp. Typha angustifolia L. Orectanthe sceptrum (Steyerm.) Maguire Xyris jupicai Rich. AF207632 AF207636 AF207628 AF207625 AY438615 AY438613 AF207629 AF547016 AF547019 AY208986 AY191213 U79230 AY438616 AF547017 1164, 1292, 1329, 1289, ISC ISC ISC ISC Smith, Sytsma, & Givnish s. n., WIS Givnish 94-3100, WIS Sytsma, Smith, & Givnish 5157, WIS Hahn 4675, WIS Sytsma, Smith, & Givnish 5116, WIS Givnish 89-125, WIS Berry & Bachhuber 10 July 2000, WIS Smith, Sytsma, & Givnish 297, WIS NYBG 1697/95, NY Hahn 3999, US Givnish s. n., WIS Graham 1040, TRT Goldman 1766, BH F. F. F. F. Wendel Wendel Wendel Wendel L. G. Clark et al. J. F. Wendel J. F. Wendel J. F. Wendel H. Shimada & M. Sugiura J. F. Wendel J. F. Wendel J. F. Wendel J. F. Wendel J. F. Wendel R. Spangler et al. R. Spangler et al. J. F. Wendel R. Spangler et al. G. Strittmatter & H. Kossel J. F. Wendel T. M. Evans & M. L. Zjhra T. M. Evans T. B. Patterson T. M. Evans T. M. Evans T. B. Patterson & M. L. Zjhra T. M. Evans T. M. Evans T. M. Evans T. M. Evans T. M. Evans & M. L. Zjhra T. M. Evans & M. L. Zjhra K. C. Millam J. C. Hall T. M. Evans H. Rai H. Rai H. Rai J. C. Pires S. W. Graham K. C. Millam & T. M. Evans H. Rai 36 Givnish et al. quences from previous studies were downloaded from GenBank to complete the data matrix (Table 1). Sequences were visually aligned using MacClade vers. 4 (Maddison and Maddison 2002). Almost all of the 54 indels detected were in-frame and straightforward (albeit laborious) to align, given their general restriction to single species or small sets of close relatives. The aligned data matrix (including 2518 aligned bases) is available upon request from the three senior authors. Phylogenetic analyses based on maximum parsimony (MP) were conducted using PAUP* vers. 4.0b8 (Swofford 2002). One hundred replicate searches were conducted using tree-bisection-reconnection (TBR) and random stepwise-addition to maximize the chances of detecting multiple islands of trees if they exist. Bootstrap percentages were obtained via TBR searches on 500 random resamplings of the nucleotide data, saving up to 50 trees per replicate. For comparative purposes, an additional MP search was conducted including both nucleotide and indel data; individual indels were treated as equally weighted characters and scored to minimize the number of additional evolutionary events following Baum et al. (1994). We merged our nucleotide data with those analyzed by Chase et al. (2000) to conduct an MP search involving 88 monocot genera for which sequence data are available for 18S nrDNA, rbcL, atpB, and ndhF, using Acorus as an outgroup. Based on this analysis, the numbers of informative and variable characters contributed by each of these sequences were calculated. Calibration of Molecular Phylogenetic Trees Against Time As previously shown for rbcL (Gaut et al. 1992, 1997), ndhF displays substantial variation in rates of nucleotide evolution across different groups of monocots, precluding the use of simple molecular clocks to place phylogenetic events and character-state changes on a time line. We therefore used the computer program r8s to transform one of the most-parsimonious ndhF trees into ultrametric form—with equal branch lengths from the root after discarding the outgroup Ceratophyllum—using cross-verified penalized likelihood (Sanderson 2002). We calibrated this tree against absolute time by fixing the age of the divergence of Acorales from other monocots at 134 million years ago (Mya) (Bremer 2000), while setting the minimum ages of the stem groups of six clades (Poaceae–Joinvilleaceae–Flagellariaceae–Restionaceae, Typhaceae–Sparganiaceae, Zingiberales, Arecales, Araceae, and Tofieldiaceae) equal to 69.5 Mya, 69.5 Mya, 83 Mya, 89.5 Mya, 69.5, and 83 Mya, respectively, based on the estimated ages of the oldest known Cretaceous fossils for these groups (Bremer 2000). Tests of Concerted Convergence We used selected ndhF trees to test whether fleshy fruits, net venation, and occurrence in shaded understories show correlated evolution employing DISCRETE (Pagel 1994, 1999). DISCRETE uses a continuous Markov model to analyze the evolution of binary characters, incorporating branch lengths and weighting gains and losses equally. We executed separate tests of correlated evolution between (1) fleshy fruits and life in shady habitats; (2) net venation and shady habitats; (3) fleshy fruits and net venation; (4) net ALISO venation and shady habitats, emergent broad-leaved aquatics, or submersed broad-leaved aquatics; and (5) fleshy fruits and net venation, excluding emergent and submersed broadleaved aquatics. DISCRETE produces a likelihood ratio for which the distribution converges on that of ␹2 with 4 degrees of freedom. We tested for correlated evolution—and hence, concerted convergence—by comparing the observed likelihood ratio against critical values of ␹2, a conservative approach (Pagel 1999). We conducted each test on four fully resolved trees, chosen randomly from among the maximumparsimony trees to represent each of the four resolutions of the major polytomy at the base of the commelinids. The other unresolved nodes are unlikely to have any substantial effect on inferences regarding the correlated evolution of fleshy fruits, net venation, or life in shaded understories. We ran each test using branch lengths (inferred number of substitutions) as measures of the amount of molecular evolution down each branch, reflective of time discounted by the rate of molecular evolution inherent to different lineages. Rates of phenotypic transitions were fitted to a gamma distribution, based on median rates in quartiles across monocots. We conducted each test five times independently because DISCRETE can fit slightly different likelihood models to the data from each random starting point, as a result of nearly flat response surfaces and/or large numbers of species. In a few instances, the first step of a DISCRETE run—which evaluates a model assuming no correlated evolution between the given pair of traits—returned a log-likelihood substantially below that of other runs. We discarded such cases a priori because they represent a much worse fit of the independent model than is possible and would bias the dependent test toward higher significance of correlated evolution. This procedure would, if anything, create a bias against acceptance of a significant pattern of correlated evolution. We considered ‘‘net venation’’ to include branching support structures within leaves, including cases of reticulate venation, simple leaves in which the veins diverge from a massive central rib regardless of whether they branch anatomically (e.g., Musa), and compound leaves with a branching rachis (palms). ‘‘Fleshy fruits’’ include berries, drupes, and seeds with showy, massive, nutritional arils dispersed by vertebrates. Proiphys Herb. (Amaryllidaceae) has brightly colored capsules that seem to mimic fleshy fruits (Meerow and Snijman 1998) and were scored as such. Seeds dispersed by ants, bearing small arils (elaiosomes), occur in forest and nonforest habitats and can serve as adaptations for purposes not directly related to dispersal (e.g., placement in nutrientrich ant nests, shelter from frequent fire) (Beattie and Culver 1983; Beattie 1985; Hughes and Westoby 1992; Boyd 2001). The fruits of Acorus are anatomically berries, but are minute, have a relatively thick, dry coat, and lack the sweet or oily composition usually associated with adaptation for ingestion and dispersal by vertebrates. Other features of its morphology and (especially) its geographic pattern of genetic variation suggest that Acorus is water-dispersed (Liao and Hsiao 1998). Thus, we did not score either ant-dispersed seeds or the dry berries of Acorus as fleshy fruits. Species were classified as occurring primarily in open, sunny habitats (e.g., tundra, chaparral, desert) or closed, shady habitats (forest understories). For species growing in seasonally deciduous forests, the timing of leaf activity and fruit production rela- VOLUME 22 Monocots: Concerted Convergence tive to canopy closure was used to categorize the habitats occupied as sunny or shady (see Patterson and Givnish 2002). Assigning species to these two classes was occasionally problematic: light regimes occupied by different species can vary continuously (e.g., see Leach and Givnish 1999; Givnish et al. 2004b) and most published accounts of ecological distributions are qualitative. However, no matter how one slices the light availability gradient, taxa like Schizachyrium Nees and Strelitzia Aiton occur in brightly lit sites, while Trillium L. and Cyanastrum Cass. occur in shaded understories. For illustrative purposes, we overlaid net venation, fleshy fruits, and life in shady habitats on an ultrametric tree using MacClade. Accelerated transformation was employed to minimize the number of apparently independent origins of each trait. A complete matrix of venation, fruit, and ecological character states is available upon request from the first author. RESULTS Phylogenetic Relationships Maximum parsimony produced one island of 880 trees, each 16,489 steps in length based on 1727 variable characters, of which 1408 are potentially phylogenetically informative (Fig. 1A–D). Across monocots, ndhF strongly supports (85–100% bootstrap) the monophyly of nine of the twelve orders identified by previous molecular studies (Chase et al. 1995a, b, 2000); support is only modest for Commelinales (52%) and Asparagales (65%), and Petrosaviales are represented by only a single taxon (Japonolirion Nakai). Several nodes previously unresolved or weakly supported are resolved in the ndhF phylogenetic tree. Our analysis demonstrates that (1) Asparagales are sister to the commelinids; (2) both of these groups are sister to Liliales plus Pandanales; (3) Japonolirion (Petrosaviales) and/or Dioscoreales are sister to all preceding groups; (4) Alismatales are strongly supported (99% bootstrap) as sister to the preceding orders; and (5) Acorus (Acorales) is sister to all other monocots. Bootstrap support for individual clades is often substantially higher than that based on rbcL, considered alone or in combination with atpB and 18S nrDNA (see Chase et al. 1995a, b, 2000). Even so, support values are still only modest at several points along the backbones of the asparagoid portion of the tree and the monocot tree as a whole (Fig. 1A–D). In a four-gene analysis, ndhF contributes 2.2 times as many informative characters as rbcL, and 87% as many as rbcL, atpB, and 18S nrDNA combined. Only nine nodes are unresolved in the ndhF strict consensus tree. Of these, only two—involving a four-way polytomy at the base of the commelinids, and a trichotomy involving four families of Zingiberales—involve substantial numbers of taxa. The commelinid polytomy involves unresolved relationships among Poales (P), Zingiberales plus Commelinales (ZC), Dasypogonales (D), and Arecales (A). Each of these clades is strongly supported individually (79–100%), as are the commelinids as a whole (85%). Among the most-parsimonious trees based on ndhF sequence variation, we found four different patterns of relationship among the major comme- 37 linid clades: ((P,A),(ZC,D)); (P,(ZC,A,D)); ((P,(ZC,D)),A); and ((P,D),A),ZC). Within Poales, ndhF places Bromeliaceae sister to Typhaceae–Sparganiaceae at the base of the order, with this overall group sister to an unresolved trichotomy involving (1) Rapateaceae, (2) the sedge alliance—Cyperaceae–Juncaceae– Thurniaceae, Eriocaulaceae–Xyridaceae, and Mayacaceae, and (3) the grass alliance—Poaceae, Joinvilleaceae, Ecdeiocoleaceae, Flagellariaceae, and Restionaceae (Fig. 1A–B). Rapateaceae are sister to the grass and sedge alliances in the bootstrap consensus (54% support), and are sister to these groups in the strict consensus tree as well if Ecdeiocolea F. Muell. is excluded or if nucleotide characters are sequentially reweighted based on their consistency index. Poaceae and Poaceae–Joinvilleaceae–Ecdeiocoleaceae have 100% bootstrap support, with Elegia L. (Restionaceae) and/or Flagellariaceae sister to these other elements of the grass alliance. Thurniaceae are sister to Cyperaceae–Juncaceae (93% bootstrap) at the core of the sedge alliance. Eriocaulaceae and Xyridaceae are monophyletic (100% and 84% bootstrap support, respectively) and each other’s closest relatives at the base of the sedge alliance minus Mayacaceae (Fig. 1A). The four major subclades of Poales—the grass alliance, sedge alliance, Rapateaceae, and Bromeliaceae—show as much sequence divergence from each other as that seen among the remaining orders of monocots. Members of the grass and sedge alliances show the highest rates of ndhF evolution among monocots; bromeliads display unusually low rates, and rapateads are intermediate in this respect (Fig. 1A–D). Resolution of relationships within the latter two families by highly informative ndhF indicates that both require new internal classifications, including five new subfamilies and recircumscription of an additional two (Givnish et al. 2004a, in press). Commelinales and Zingiberales are both resolved as sister clades (79% bootstrap support). In Zingiberales, ndhF resolves three pairs of sister families—Zingiberaceae–Costaceae (61%), Marantaceae–Cannaceae (80%), and Strelitziaceae–Lowiaceae (89%). Within Commelinales, Pontederiaceae and Haemodoraceae both have 100% bootstrap support as sister taxa. Philydraceae are sister to the rest of Commelinales, but this position is weakly supported (Fig. 1B). One indel supports their placement with Pontederiaceae and Haemodoraceae, and a combined analysis of ndhF indels and nucleotides (not shown) places Philydrum Banks ex Gaertn. in an unresolved trichotomy with Pontederiaceae– Haemodoraceae and Commelinaceae–Hanguanaceae. Hanguana is strongly supported (90%) as being sister to Commelinaceae; Cartonema R. Br. is sister to all other members of the latter. Our analysis places the climbing rattan Calamus Auct. ex L. sister to the rest of Arecales (98% bootstrap), with the mangrove palm Nypa Steck next-divergent. Dasypogon R. Br. and Calectasia R. Br. are resolved as forming the monophyletic order Dasypogonales (100% bootstrap). An important finding of this study is that ndhF places Asparagales sister to the commelinids rather than Liliales in the strict consensus tree (Fig. 1C). Asparagales are composed of a ladder of eight clades, with Orchidaceae sister to the rest (Fig. 1C). The sequence of families is broadly similar to that seen in recent studies (see Discussion). Hyacinthaceae are sister to Agavaceae rather than Themidaceae, 38 Givnish et al. ALISO Fig. 1A–D.—Phylogram of one of 874 most parsimonious trees produced by cladistic analysis of ndhF sequence variation. CI ⫽ consistency index including all variable characters; CI⬘ ⫽ consistency index for informative characters only; RI ⫽ retention index. Arrowheads indicate nodes that collapse in the strict consensus tree. Bootstrap values are indicated above each node.—A. Poales I.—B. Poales II, Zingiberales, Commelinales, Dasypogonales, and Arecales.—C. Asparagales.—D. Liliales, Pandanales, Dioscoreales, Petrosaviales, Alismatales, and Acorales. with which they share bulbs and a similar habit. Agapanthaceae are sister to Amaryllidaceae–Alliaceae. Orchidaceae are strongly supported as monophyletic (100% bootstrap), and are placed sister to all other Asparagales with moderate support (Fig. 1C). In Liliales, ndhF identifies Campynema Labill. as earliest divergent, followed successively by Melanthiaceae, Colchicaceae–Alstroemeriaceae, Philesiaceae–Ripogonaceae, Smilacaceae, and Liliaceae (Fig. 1D). The last consists of Calochortaceae and Liliaceae sensu Tamura (1998a, b), with Calochortus Pursh itself embedded in a lineage containing Prosartes D. Don, Scoliopus Torr., Streptopus Michx., and Tricyrtis Wall. Disporum Salisb. is sister to Uvularia L. in Colchicaceae. Clintonia Dougl. ex Lindl. and Medeola L., with fleshy fruits and broad, net-veined leaves, are strongly supported as each other’s closest relatives, forming subfamily Medeoloideae of Liliaceae (Tamura 1998b); this group is sister, in turn, to subfamily Lilioideae, characterized by capsular fruits and narrow, parallel-veined leaves excepting forest-dwelling, net-veined Cardiocrinum Lindl. Pandanales are sister to Liliales in the ndhF strict consen- sus tree (Fig. 1D), and to Dioscoreales in the bootstrap majority-rule tree. Among the families sampled, Velloziaceae are sister to Pandanaceae–Stemonaceae in Pandanales, and Nartheciaceae are sister to Dioscoreaceae of Dioscoreales. Japonolirion of Petrosaviales is part of an unresolved trichotomy involving itself, Dioscoreales, and commelinids– Asparagales–Liliales–Pandanales; together, these groups form a strongly supported clade (100% bootstrap) consisting of all monocots except Alismatales and Acorales (Fig. 1D). Araceae (100% bootstrap) are sister to Tofieldiaceae and the remaining Alismatales. The latter form a clade with 100% bootstrap support and two well-marked subclades, including Alismataceae–Limnocharitaceae–Butomaceae (95%), and Aponogetonaceae–Juncaginaceae–Scheuchzeriaceae–Cymodoceaceae–Zosteraceae. Juncaginaceae and Scheuchzeriaceae are resolved as sister groups based on ndhF sequence variation. Tofieldiaceae are weakly supported (69%) as sister to the families of the former Najadales (Dahlgren et al. 1985). Finally, ndhF provides 100% bootstrap support for the position of Acorus sister to all other monocots (Fig. 1D). VOLUME 22 Monocots: Concerted Convergence 39 Fig. 1A–D.—Continued. Concerted Convergence Based on our ndhF data, fleshy fruits appear to have arisen at least 21 times and been lost 11 times, whereas net venation has arisen at least 26 times and been lost 9 times (Table 2; Fig. 2). As predicted, these traits have undergone concerted convergence. They have done so in highly significant fashion (P ⬍ 10⫺9, log-likelihood test), with both traits arising together (at the same or adjacent nodes) 15 times and disappearing together 5 times (Table 2; Fig. 2). Fleshy fruits 40 Givnish et al. ALISO Fig. 1A–D.—Continued. and net venation arose together in Joinvilleaceae, Flagellariaceae, Hanguanaceae, Arecales, Zingiberales, Behnia Didr., two groups of Amaryllidaceae, Geitonoplesium A. Cunn., Curculigo Gaertn., the core Liliales, Trillium, and Araceae, and are associated with each other in Ruscaceae–Laxman- niaceae, Disporum, and Tacca Forst., with the evolution of fleshy fruits slightly lagging that of net venation among close relatives and inferred ancestors in the last two lines (Fig. 2). Fleshy fruits and net venation were lost together in Arthropodium R. Br., Hypoxis L.–Lanaria Aiton., Lilioideae, and Monocots: Concerted Convergence 41 Fig. 1A–D.—Continued. VOLUME 22 42 Givnish et al. Table 2. Inferred evolutionary origins of net venation, fleshy fruits, and life in shady habitats, and of parallel venation, passively dispersed fruits and/or seeds, and life in sunny habitats. Most instances of the evolution of the former character states represent initial transitions from the latter, while most instances of the origin of the latter represent reversals from the former. Transitions on the same line occurred at the same node or (in a few cases) adjacent nodes. Instances where all three character states underwent transition at the same or adjacent nodes—involving concerted convergence— are underlined. All calls are based on overlaying characters on a single most-parsimonious tree using accelerated transformation in MacClade (Maddison and Maddison 2002). Net venation Bambusoideae Joinvillea ⫹ earlydivergent Poaceae Flagellaria Hanguanaceae Zingiberales ⫹ Philydraceaea Arecaceae Hosta Behnia Ruscaceae ⫹ Laxmanniaceae Griffinia Hymenocallis Proiphys–Scadoxus Geitonoplesium Cyanastrum Curculigo Fleshy fruits Joinvillea Flagellaria Bromelioideae Hanguanaceae Amischotolype Zingiberales Arecaceae Behnia Ruscaceae ⫹ Laxmanniaceae Hippeastrum Proiphys–Scadoxus Geitonoplesium Curculigo Asteliaceae ⫹ Blandfordiaceae Neuwiedia Cardiocrinum Liliales above Alstroemeria [Cardiocrinum]b Liliales above Ripogonum Disporum–Uvularia Trillium Stemonaceae Disporum Trillium Dioscoreaceae Alismataceaea Zosteraa Aponogetona Araceae Pandanaceae Tacca Araceae Shade Bambusoideae Joinvillea ⫹ early divergent Poaceae Flagellaria Monotremeae Bromelioideae (Hanguanaceae ⫹ Commelinaceae) Zingiberales Arecaceae Hosta Behnia Chlorophytum Ruscaceae ⫹ Laxmanniaceae Griffinia ⫹ Hippeastrum Hymenocallis Proiphys–Scadoxus Geitonoplesium Cyanastrum Curculigo Asteliaceae ⫹ Blandfordiaceae Neuwiedia Epipactis Tropidia Cardiocrinum Liliales above Ripogonum Calochortus albus Disporum–Uvularia Trillium Stemonaceae Dioscoreaceae Alismataceaea Araceae Nolina Michx., with the loss of fleshy fruits in the last lagging that of net venation by one node. Both fleshy fruits and (especially) net venation show even stronger patterns of correlated evolution with shady conditions than with each other. In almost every case, the evolution of net venation and fleshy fruits is associated with life Table 2. ALISO Continued. Parallel venation Higher Poaceae Passively dispersed fruits Poaceae Costaceae Cannaceaea Lowiaceae Nypa Dracaena ⫹ Nolina Ophiopogon Asparagus Arthropodium Hypoxis–Lanaria Lilioideae Calochortus Nolina Arthropodium Hypoxis–Lanaria Lilioideae Calochortus ⫹ Tricyrtisb Scoliopus Sun Higher Poaceae Cartonema Cannaceae Strelitziaceae Nypa Phoenix Dracaena ⫹ Nolina Asparagus Arthropodium Hypoxis–Lanaria Lilioideae Calochortus Androcymbium– Wurmbea a Associated with broad-leaved emergent or submersed aquatic habit. b Associated with retention or origin of passively dispersed fruits adapted to dispersal in autumn under an open canopy in temperate deciduous forests, while leaves have net venation adapted for activity in summer under a closed canopy. in forest understories, whereas their loss is associated with open habitats. Specifically, 19 of 21 gains of fleshy fruits are associated with invasion of—or life in—shady sites, whereas 7 of 11 losses are associated with the invasion of sunny conditions. For net venation, 22 of 26 gains are associated with shady conditions, whereas 8 of 9 losses are associated with sunny conditions. These patterns of origin and maintenance are highly significant (P ⬍ 10⫺10 to 10⫺30) when tested in DISCRETE, using branch lengths that are equal to the inferred total amounts of molecular evolution down each lineage, a function of time plus plant characteristics such as generation time; Table 3). These results support our hypotheses about adaptation and establish the existence of a highly significant pattern of concerted convergence across the monocots. Net venation shows an even more marked association with shade if we factor out the four lineages (Alismataceae, Aponogetonaceae, Philydraceae, Zosteraceae) in which it arose in broad-leaved aquatic plants, mostly near the base of the monocots in Alismatales (Tables 2, 3). All origins of net venation are associated with either shady conditions (85%) or broad leaves in aquatic emergents or submersed species (15%). Fleshy fruits also show a stronger association with net venation if we exclude aquatic plants with broad leaves and net venation, in which we have no a priori reason to expect the evolution of fleshy fruits. The numerous origins of fleshy fruits and net venation are distributed rather evenly across lineages and time (Fig. 2). Both traits arose nearly 90 Mya ago in Araceae and Arecaceae. The former family is dominated by herbs, vines, and epiphytes of tropical rain-forest understories, together with some temperate forest herbs (e.g., Arisaema Mart., Arum L.) VOLUME 22 Monocots: Concerted Convergence 43 Fig. 2.—Concerted convergence of net venation (green), fleshy fruits (red), shaded habitats (sand boxes), and broad-leaved aquatic habit (blue boxes). Note that almost all transitions to net venation and fleshy fruits occur upon invasion of shaded habitats, and that almost all reversals to parallel venation and dry, passively dispersed seeds or fruits occur upon re-invasion of open, sunny habitats. The tree shown is ultrametric and has been calibrated against the age of six Cretaceous fossils using penalized likelihood, so that the tempo and taxonomic distribution of phenotypic transitions can be visualized. Both net venation and fleshy fruits show somewhat constant rates of ecological evolution over the past 90 million years, with an increase in the absolute number of origins toward the present and a decrease in the number of origins per clade present. 44 Givnish et al. ALISO Table 3. Log likelihood ratios (LR) and significance levels (P) resulting from five different tests for correlated evolution across monocots in net venation, fleshy fruits, and life under shaded conditions, conducted on four representative trees using DISCRETE (Pagel 1994, 1999). Mean (⫾SE) LR represents the average value from five independent analyses per tree per test (see text). Tree A Tree B Tree C Tree D Mean SE of mean Significance 1. Fleshy fruits and net venation Mean LR 50.6 Standard error 0.8 Minimum 48.0 53.1 1.4 50.7 59.4 2.6 50.7 48.1 0.3 47.5 52.8 1.3 49.2 2.4 1.2 P ⬍ 10⫺9 2. Fleshy fruits and shade Mean LR Standard error Minimum 74.0 3.9 63.9 73.4 2.5 65.7 72.4 1.4 66.8 66.3 1.7 59.7 71.5 1.3 64.0 1.8 2.2 P ⬍ 10⫺11 3. Net venation and shade Mean LR Standard error Minimum 129.8 3.2 117.0 132.7 1.3 127.5 120.9 1.7 116.1 132.1 0.9 128.6 128.9 1.8 122.3 2.7 1.2 P ⬍ 10⫺23 4. Net venation and shade ⫹ broad-leaved aquatics Mean LR 154.3 154.7 Standard error 2.4 1.7 Minimum 144.8 148.2 154.2 2.0 148.1 159.3 3.9 146.5 155.7 2.5 146.9 1.2 1.2 P ⬍ 10⫺30 5. Fleshy fruits and net venation, excluding broad-leaved aquatics Mean LR 63.8 61.2 58.4 Standard error 1.4 1.3 0.9 Minimum 61.1 56.1 55.0 60.6 1.4 55.4 61.0 1.2 56.9 1.1 2.0 P ⬍ 10⫺10 and broad-leaved submersed aquatics (e.g., Anubias Schott, Cryptocoryne Fisch. ex Wydler). The palms contain many rain-forest lineages, but have also invaded open subtropical savannas and scrub. The most recent instances of concerted convergence in fleshy fruits (or mimics thereof) and net venation occurred within the last 5 to 10 Mya, in Griffinia Ker Gawl. and Proiphys–Scadoxus Raf. of Amaryllidaceae and Curculigo of Hypoxidaceae. Fleshy fruits arose at least three times in Poales, twice in Commelinales, once in Zingiberales, once in Arecales, eight times in Asparagales, three times in Liliales, once in Pandanales, once in Dioscoreales, and once in Alismatales. Net venation arose at least three times in Poales, once in Commelinales, once in Zingiberales, once in Arecales, eleven times in Asparagales, four times in Liliales, once in Pandanales, once in Dioscoreales, and four times in Alismatales. During 10-Mya intervals, an average of 2.9 ⫾ 0.5 lineages evolved net venation, whereas an average of 2.4 ⫾ 0.4 lineages evolved fleshy fruits, implying a rather clocklike rate of adaptive evolution in both these traits across the monocots. It is important to note that many of the inferred reversals to parallel venation or passively dispersed, dry fruits appear to have occurred quite recently, with the exception of the reversal at the base of subfamily Lilioideae of Liliaceae (Fig. 2). As might be expected given the relative numbers of origins of net venation and fleshy fruits, there are a number of groups of understory plants in which only net venation, not fleshy fruits, evolved. The net-venation-only syndrome characterizes the bambusoids, early-divergent grasses, Costaceae, Hosta Tratt., Cyanastrum Oliv., and Stemonaceae. Cardiocrinum and Tricyrtis of temperate deciduous forests both have net veins only, but are photosynthetically active under shady conditions in summer while releasing seeds af- ter the canopy re-opens in autumn. Net veins also occur in the absence of fleshy fruits in four lineages of broad-leaved aquatics, including Alismataceae, Aponogetonaceae, and Zosteraceae of Alismatales and Philydraceae of Commelinales. Fleshy fruits arose without net venation under shady conditions in bromelioid bromeliads, Amischotolype Hassk., Asteliaceae and relatives, and the apostasioid orchid Neuwiedia Blume. DISCUSSION Phylogenetic Relationships Cladistic analysis of ndhF sequence variation yields a highly resolved, well-supported phylogenetic tree for the monocots (Fig. 1). Relationships among orders are unclear in only two cases, involving the commelinids and the position of Dioscoreales and Pandanales close to the base of the monocots. The lack of resolution among the four major commelinid clades—Poales, Zingiberales plus Commelinales, Dasypogonales, and Arecales—may simply reflect a rapid initial diversification among the commelinids. Analyses based on seven genes (but many fewer taxa) resolve this polytomy by placing Dasypogonales sister to Poales, and Arecales sister to Zingiberales–Commelinales, but the bootstrap support for both relationships is weak (ⱕ51%) (Chase et al. 2006). Analyses based on 17 genes flip these relationships, placing Arecales as sister to Poales and Dasypogonales sister to Zingiberales–Commelinales, and bootstrap support for these relationships is also weak (⬍50%) (Graham et al. 2006). Here Pandanales are sister to Liliales in the ndhF strict consensus, but to Dioscoreales in the bootstrap consensus. The latter position is consistent with that obtained from an analysis based on 7 and 17 genes (Chase et al. 2006; VOLUME 22 Monocots: Concerted Convergence Graham et al. 2006). Alismatales are sister to a strongly supported clade (100% bootstrap) consisting of all other monocots except Acorales (Fig. 1). Petrosaviales or Dioscoreales are, in turn, sister to all other elements of this large clade; 7- and 17-gene analyses place Petrosaviales sister to all monocots except Alismatales and Acorales, and Dioscoreales sister to Pandanales (Chase et al. 2006; Graham et al. 2006). Within commelinids, ndhF supports many relationships identified previously based on other sequence data (Givnish et al. 1999; Chase et al. 2000; Graham et al. 2003; Michelangeli et al. 2003), and resolves others for the first time. Bromeliaceae and Typhaceae–Sparganiaceae are sister to each other and earliest divergent within Poales, with Rapateaceae being next divergent in the bootstrap consensus and sequentially weighted analyses (see Fig. 1 and Results). Our findings for Poales differ somewhat from those of Michelangeli et al. (2003) based on morphology and sequence variation in rbcL and atpA. Those authors placed Rapateaceae sister to paraphyletic family Xyridaceae, including Eriocaulaceae and Mayacaceae, at the base of Poales; identified Bromeliaceae, then Typhaceae–Sparganiaceae as sister lineages to the remaining members of the order; and positioned Flagellaria L. as sister to two terminal clades, consisting of (1) Anarthria R. Br., Aphelia R. Br., and Restionaceae, and (2) Joinvillea Gaudich., Ecdeiocolea, and Poaceae. The nodes at which our results and those of Michelangeli et al. (2003) differ, however, are weakly supported (⬍50% bootstrap) in their analysis. These include (1) the positions of Bromeliaceae, Rapateaceae, and Typhaceae–Sparganiaceae relative to each other and to Eriocaulaceae, Mayacaceae, and Xyridaceae; (2) the supposed paraphyly of Xyridaceae; and (3) the position of Flagellaria, not Restionaceae, as sister to the remainder of the grass alliance. Our ndhF analysis resolves both Xyridaceae (including Orectanthe) and Eriocaulaceae as being monophyletic with 84–100% bootstrap, and identifies these two families as each other’s closest relative (75% bootstrap). We resolve Bromeliaceae as sister to Typhaceae– Sparganiaceae with 64% bootstrap support, and place Rapateaceae as the next-divergent element with 79% support in the bootstrap majority-rule tree, consistent with its strongly supported position in the 7-gene tree (Chase et al. 2006). These relationships are similar to those derived by Bremer (2000) based on rbcL, but differ in the placement of the three earliest-divergent clades consisting of Bromeliaceae, Rapateaceae, and Typhaceae–Sparganiaceae. The placement of the last just inside Bromeliaceae–Rapateaceae by Bremer (2000) involves a very short branch, however. We were unable to amplify and sequence ndhF for DNAs of Aphelia (Centrolepidaceae) and Trithuria Hook. f. (Hydatellaceae) kindly provided by J. Davis and D. Stevenson, and so were unable to confirm their strongly supported finding that Aphelia is sister to Restionaceae or the more weakly supported association of Trithuria with Xyridaceae. The strongly supported placement of Thurnia Hook. f.– Prionium E. Mey. sister to Cyperaceae–Juncaceae by ndhF is consistent with that of several recent molecular studies (Givnish et al. 1999; Bremer 2000; Chase et al. 2000; Michelangeli et al. 2003). The position of Mayaca Aubl. sister to all other elements of the sedge alliance, however, is more weakly supported and problematic. An earlier ndhF se- 45 quence of this taxon had placed it sister to Bromeliaceae (Givnish et al. 1999), but a new, higher quality sequence from Venezuelan material places it sister to the remainder of the sedge alliance, near Xyridaceae and Eriocaulaceae, which seems more plausible based on morphology and atpA and rbcL sequence data (Michelangeli et al. 2003); rbcL places Mayaca immediately sister to Xyridaceae and Eriocaulaceae (Bremer 2000). The possibility that Mayaca could act as a ‘‘wild card’’ much like Ecdeiocolea (see above) or Aphyllanthes Tourn. ex L. in Asparagales (see Fay et al. 2000), should not be overlooked. The extensive divergence of the grass alliance, sedge alliance, rapateads, and bromeliads from each other is comparable to that among other groups of monocots already recognized at the ordinal level (Fig. 1). The remarkable isolation of both Bromeliaceae and Rapateaceae from other monocots in both morphology and sequence variation appears to reflect 15 to 40 million years between the origins of each group and when present-day lineages began to diverge from each other (Givnish et al. 2004a, in press). If support for the four major clades of Poales grows in future multigene analyses, and the position of Eriocaulaceae, Xyridaceae, and (especially) Mayacaceae becomes solidified, it would be prudent to revisit the issue of recognizing the four major clades in Poales—representing 31% of all monocot species—as orders in their own right. The resolution of Commelinales and Zingiberales as sister taxa is consistent with previous molecular analyses (Givnish et al. 1999; Chase et al. 2000; Evans et al. 2003; Graham et al. 2003). Relationships among families within Zingiberales are largely consistent with a detailed analysis based on morphology and several rapidly evolving stretches of DNA (Kress et al. 2001). Our analysis, however, places Musaceae, Heliconiaceae, and Strelitziaceae–Lowiaceae in an unresolved trichotomy sister to the remaining ‘‘ginger’’ families, rather than in a ladder with Musaceae earliest-divergent as seen in Kress et al. (2001). Our ndhF tree identifies Haemodoraceae and Pontederiaceae as each other’s closest relatives (Fig. 1B). They fail, however, to provide positive evidence that their immediate sister is Philydraceae, as have other molecular studies (Graham and Barrett 1995; Graham et al. 1998; Chase et al. 1995a, 2000; Givnish et al. 1999). However, inclusion of indels places Philydrum in a polytomy consistent with a tie to Haemodoraceae and Pontederiaceae (see Results), and thus consistent with previous studies based on morphology (Dahlgren et al. 1985) and molecular variation. Fleshy-fruited, net-veined Hanguana is strongly supported as being sister to Commelinaceae, consistent with previous molecular analyses (Givnish et al. 1999; Chase et al. 2000) but not with morphology, which tends to place this genus of southeast Asian rain forests with Zingiberales instead (Rudall et al. 1999). The placement of Calamus as sister to the rest of Arecales, followed by Nypa, is consistent with relationships obtained using 5–7 kilobases (kb) of coding and noncoding plastid DNA (Asmussen and Chase 2001; Hahn 2002). Although bootstrap support for relationships within the rest of Arecales based on ndhF alone are low (35–95%), the fact that they are fully resolved based on a single gene is promising, given that many similar relationships are unresolved using rbcL alone (Uhl et al. 1995). Members of Arecales, Bro- 46 Givnish et al. meliaceae, and Zingiberales display unusually slow rates of plastid DNA evolution (Gaut et al. 1992; Givnish et al. 1999; Fig. 1A–D). It should thus not be surprising that relationships within these groups are much better resolved by ndhF than by rbcL, with or without atpB and 18S nrDNA (see Chase et al. 1995a, 2000). Although molecular data (ndhF; rbcL, atpB, 18S nrDNA; and 7- and 17-gene trees in development) do not resolve the relationships among the four major clades of commelinids, certain anatomical and chemical characteristics tend to link Commelinales–Zingiberales to Poales (Stevens 2003). The placement of Asparagales sister to the commelinids rather than Liliales by ndhF (Fig. 1C) runs counter to the previous view that Asparagales and Liliales are sister to each other (Dahlgren et al. 1985). The arrangement of families within Asparagales generally supports that obtained in other recent studies (Fay et al. 2000; Pires et al. 2006; McPherson et al. submitted). Relationships within and near Amaryllidaceae are largely consistent with those obtained by Meerow et al. (1999) based on rbcL and the trnL–trnF region, except that ndhF places Agapanthaceae sister to Amaryllidaceae– Alliaceae, rather than Amaryllidaceae alone. Relationships within Liliales are mostly consistent with those obtained by Vinnersten and Bremer (2001) based on rbcL, and by Patterson and Givnish (2002) based on rbcL and ndhF. Our results differ slightly from the rbcL tree, in which Alstroemeriaceae and Colchicaceae are sister to the rest of the order, and in which Liliaceae sensu Tamura (1998b), Calochortus, and Scoliopus–Streptopus–Tricyrtis form a trichotomy at the base of Liliaceae sensu Tamura (1998a). Analysis of the combined rbcL and ndhF data produces a tree identical to that based on ndhF alone (Patterson and Givnish 2002). The placement of Prosartes in Liliaceae and Disporum in Colchicaceae supports previous analyses based on rbcL (Shinwari et al. 1994a, b; Chase et al. 1995a, b), despite the striking morphological convergence in habit, net venation, and fleshy fruits in these two groups, formerly lumped in Disporum. The position of Pandanales sister to Dioscoreales in the ndhF bootstrap majority-rule tree is consistent with analyses of placeholders involving 7 and 17 genes, as is the position of Japonolirion (or Dioscoreales) sister to monocots other than Alismatales and Acorales in the strict consensus tree (Chase et al. 2006; Graham et al. 2006). Attempts to sequence ndhF for representatives of Burmanniaceae (Burmannia L., Thismia Griff.) failed despite repeated attempts, preventing us from determining where this family belongs. Tacca–Dioscorea L. is sister to Trichopus Gaertn. within the dioscorealean taxa sequences surveyed, consistent with the findings of Caddick et al. (2002a, b) based on rbcL, atpB, and 18S nrDNA. The isolated position of Japonolirion supports the decision to recognize this genus (and achlorophyllous Petrosavia Becc.) as constituting Petrosaviales, one of the 12 monocot orders (Cameron et al. 2003). Relationships among the families of Alismatales based on ndhF are broadly similar to those implied by rbcL (Les et al. 1997) but differ in detail. Mostly, the divergences between the two trees are not strongly supported in either case. The identification of Juncaginaceae and Scheuchzeriaceae as sister groups by ndhF, however, is probably significant, given that these morphologically similar families share a unique ALISO cyanogenic glucoside (triglochinin) known in no other angiosperm family (see Haynes et al. 1998). Repeated attempts to amplify and sequence ndhF from several of the smallest, aquatic families of Alismatales failed, preventing as detailed an analysis of relationships in this group as desired (D. Les and S. W. Graham pers. comm.). Our results support the important conclusion of Les et al. (1997) that the ‘‘aquatic’’ families of Alismatales fall into two clades, one including Alismataceae, Limnocharitaceae, and Butomaceae, and the other a series of three independently evolved families of seagrasses, with the Madagascar lace-plant family (Aponogetonaceae) closely related to the latter clade. As noted by Chase et al. (1995a) and Zomlefer (1999), several genera once placed in Melanthiaceae in Liliales— including Japonolirion, Narthecium Huds., and Tofieldia Huds.—are now identified as belonging to three additional orders of monocots, including Petrosaviales, Dioscoreales, and Alismatales. Their growth form, marked by narrow equitant leaves, is also strikingly similar to that of Acorus at the base of the monocots (although Japonolirion differs from Narthecium and Tofieldia in having bifacial leaves; M. W. Chase pers. comm.). Our results strongly support this position for Acorus, consistent with all recent molecular studies (e.g., Chase et al. 1993, 1995a, b, 2000, 2006; Bremer 2000; Fuse and Tamura 2000; Graham and Olmstead 2000; Soltis et al. 2000; Borsch et al. 2003; Zanis et al. 2003; Graham et al. 2006). Concerted Convergence The independent origin of net venation at least 26 times in the monocots, always in association with invasion of shady conditions (85%) or life as a broad-leaved aquatic plants—as well as the independent origin of fleshy fruits at least 21 times, 19 in association with shaded forest understories—is one of the most remarkable, widespread, and highly significant (P ⬍ 10⫺30 to 10⫺30) cases of convergent evolution ever documented. The joint evolution of fleshy fruits and net venation 15 times across the monocots, and their joint loss five times, is also—by far—the most striking case of concerted convergence and plesiomorphy thus far demonstrated. These patterns are not only highly significant, they have high explanatory value as well. Phylogenetically unstructured correlation coefficients (r) range from 0.54 for the coincidence of net venation and fleshy fruits, to 0.64 and 0.73 for the coincidence of fleshy fruits and net venation with shaded habitats, to 0.77 for the coincidence of net venation with shaded habitats or a broad-leaved aquatic habit, when all traits are scored as binary characters. In many ways, the contrast between Trillium and its closest relatives in Melanthiaceae (represented in this and all other surveys by Xerophyllum Michx.) epitomizes the pattern of concerted convergence discussed in this paper. Trillium grows in the shaded understories of temperate mesic forests, has broad, thin, soft leaves, net venation, and fleshy fruits, while Xerophyllum grows in more open habitats (meadows, fireswept pine glades) and possesses narrow, thick, hard leaves with parallel venation and tiny, wind-dispersed seeds released from dry capsules. It would be difficult, based on gross morphology, to infer that these taxa are actually very close relatives; the demonstration that they are VOLUME 22 Monocots: Concerted Convergence is one of the triumphs of plant molecular systematics. The contrast between Trillium and Xerophyllum is paralleled by several other cases, most notably involving the contrast between Hypoxis (mostly grass-leaved, capsule-fruited herbs of meadows, prairies, and glades, occasionally found in woodlands) and Curculigo (broad-leaved, net veined, fleshy-fruited herbs of tropical forest understories). A few Hypoxis occur in tropical forest understories or have broad leaves, and a few Curculigo have rather narrow leaves. Fleshy-fruited, net-veined, forest-dwelling Geitonoplesium also contrasts sharply with all of its dry-fruited, parallel-veined relatives of open habitats (see Conran 1999). Cyanastrum of shady African rain forests and woodlands has broad, cordate leaves with net venation, while confamilial Cyanella L. of open South African fynbos and Tecophilaea Bert. ex Colla of the Chilean high Andes have narrow, rather fleshy, grasslike foliage that lack cross veins. The difference between forestdwelling Hosta (with thin, broad, net-veined leaves) and Agave L., Yucca L., and other elements of Agavaceae (mostly with thick, succulent, parallel-veined leaves) to which Hosta is sister (Bogler and Simpson 1996) could hardly be more striking, although it does not entail the evolution of different fruit types. In addition to such cases of divergence among close relatives, striking convergence among distant relatives also supports our case. Asian Disporum of Colchicaceae and North American Prosartes of Liliaceae both grow in the understories of temperate mesic forests and share net venation and fleshy fruits, as well as many other features of growth form (e.g., arching stems) and floral morphology. They are so similar that both were placed in the same genus, until Shinwari et al. (1994a, b) used molecular data to demonstrate that the North American taxa were closely related to Streptopus, while the Asian taxa were closely related to Uvularia. Both of these genera, in turn, are remarkably similar in many ways to Polygonatum Miller, Disporopsis Hance, and Smilacina Desf. (also native to temperate forest understories) of Ruscaceae in order Asparagales; indeed, these genera were grouped with Disporum and Prosartes in the asparagoid tribe Polygonatae by Krause (1930), Therman (1956), Hutchinson (1959), and La Frankie (1986)! The joint evolution of fleshy fruits and net venation is not lock-step: by no means is every invasion of forest understories associated with a gain of both traits, nor is every invasion of open sites associated with a loss of both traits. Nevertheless, this pattern is highly significant and some apparent exceptions are illuminating. Bromelioid bromeliads evolved fleshy fruits, but not net venation—which may be understandable, given that they also possess CAM photosynthesis and thus have thick, succulent leaves in which net venation would not be adaptive. CAM photosynthesis seems obviously adaptive in the open, dry habitats (Winter and Smith 1996) in which bromelioids evolved (Givnish et al. in press), but is also advantageous under the constantly damp, rainforest-interior conditions where most other bromelioids grow because it allows CO2 recycling when the leaf surfaces are occluded with raindrops (Pierce et al. 2002). Vanilloid orchids (not included in our survey) evolved net venation but not fleshy fruits, except Vanilla Plum. ex Mill. itself (Cameron and Chase 1998)—which may also be understandable, given that mycotrophy in general appears to favor tiny, ex- 47 ceedingly numerous seeds that are independently dispersable, presumably to maximize the chances of contacting a suitable fungal partner. Finally, the retention of net venation in several species of palms (Arecaceae) and yams (Dioscoreaceae) that have invaded open tropical and subtropical habitats speaks for the importance of phylogeny and genetic/ developmental heritage, not ecology, in helping maintain this trait. It is true that even yams of open, hot savannas often have thin, soft-textured leaves; presumably this is related to their short leaf lifespans, the ephemeral period of abundant moisture in their savanna habitats, and the widespread trend for specific leaf mass (g m⫺2) to decline with leaf longevity across biomes and (mainly dicot) lineages (Reich et al. 1997; Ackerly and Reich 1999). However, palms of open savannas and oases often have tough, coriaceous foliage and a relatively compact, palmate form—and yet retain a branching support structure within leaves, strongly supporting a role of phylogenetic morphological conservatism. There are a few additional cases involving the concerted convergence of net venation and fleshy fruits beyond the monocot taxa we included in our survey. Examples include Palisota Rchb. ex Endl. (Commelinaceae), Vanilla and Selenipedium Rchb. f. (Orchidaceae), Eucharis Planch. & Linden (Amaryllidaceae), and Cyclanthaceae of tropical rainforest understories. Perhaps the most striking evidence that selection strongly favors both net venation and fleshy fruits under shaded conditions, however, is provided by Gnetum L. This genus of tropical vines and trees is characterized by fleshy fruits and broad, net-veined leaves that strongly resemble those of Coffea L. and other understory angiosperms—and yet Gnetum is a gymnosperm, closely related to the xeric-adapted Ephedra L. and Welwitschia Reichb. (Bowe et al. 2000; Chaw et al. 2000). The strong resemblance of Gnetum to certain angiosperms helped inspire the hypothesis that the angiosperms were derived from gymnosperms via Gnetales (Doyle and Donoghue 1986; Donoghue 1994). Molecular data do not support that hypothesis, however, indicating that the gymnosperms as a whole are sister to the angiosperms and that Gnetales arose from within the conifers (Bowe et al. 2000; Chaw et al. 2000; Soltis et al. 2002; but see Rydin et al. 2002). Won and Renner (2003) have recently discovered a horizontal transfer of a group II intron (a self-splicing RNA and putative spliceosomal ancestor) and adjacent exons of mitochondrial nadI from asterid angiosperms to a few Asian species of Gnetum. Although this might seem to open the possibility of a horizontal transfer of genes coding for net venation into Gnetum, such a scenario seems highly unlikely, given that the Asian species involved are nested well within Gnetum, all of whose species are characterized by net venation. Phylogenetic analyses indicate that fleshy fruits have evolved repeatedly in association with forest understories in Lobeliaceae (Givnish 1998), Gesneriaceae (Smith 2001), and urticoid Rosales (Sytsma et al. 2002) among the dicots. Givnish (1979) observed that net venation occurs in several monocot groups with thin, broad leaves in forest understories, including Arisaema, Smilax L., Trillium, and various tropical gingers and their relatives. Conover (1983) and Chase et al. (1995a) independently noted similar, qualitative associations of net venation with broad-leaved forest vines; Cameron and Dickison (1998) noted a similar association of 48 Givnish et al. net venation with achlorophyllous vanilloid orchids. The association of net venation with the climbing habit among monocots is well marked. We believe it arises for three reasons: (1) most vines are, perforce, growing in microsites shaded by the hosts they are climbing; (2) species growing directly on tree boles are likely to experience especially dense shade, given that the boles occlude half the sky (Givnish and Vermeij 1976); and (3) the vine habit, by its nature, entails low allocation to support tissue, resulting in more rapid rates of upward growth and self-shading of lower leaves than in self-supporting plants with the same photosynthetic rate, and favoring shorter leaf lifespans and thus thinner, softer leaves with lower specific leaf mass (Givnish 2002). Indeed, a survey of 52 European woody species grown in a common garden showed that climbers/scramblers (6 species) had the lowest specific leaf mass of the species surveyed (Castro-Diez et al. 2000). The association of net veins with the achlorophyllous vanilloid orchids most likely reflects initial adaptation of chlorophyllous ancestors to shady conditions, including the evolution of net venation (seen today in other shade-adapted orchid genera, such as Goodyera R. Br. and Isotria Raf.). Subsequently, evolution may have favored abandonment of the photosynthetic habit under such unproductive conditions and a focus on carbon input via mycotrophy, with further reduction in leaf size and thickness. Given that both fleshy fruits and net venation each arose more than 20 times in the monocots, the question immediately arises as to whether the same developmental pathways and underlying genes were involved in each case, or whether these adaptations arose in different ways in different groups (as has occurred in different populations of rock pocket mice that have independently evolved dark pelage on dark-colored soils [Nachman et al. 2003]). The fact that both fleshy fruits and net venation have arisen without the other in some cases demonstrates that they are unlikely to be the pleiotropic effects of a single gene or supergene. Furthermore, given that several groups show obvious differences in the fine details of their pattern of net venation (e.g., see Shinwari et al. 1994a, b), and that ‘‘fleshy fruits’’ involve the elaboration of different tissues in different groups (e.g., arils vs. capsule walls), it seems unlikely that all of the multiple origins of net venation and fleshy fruits have each depended on the same genes and developmental pathways for each trait. Determining whether or not this has been the case should be a goal of new studies at the interface of ecology, evolution, and development (‘‘eco-evo-devo’’; Givnish 2003). When Patterson and Givnish (2002) demonstrated that net venation, fleshy fruits, inconspicuous flowers, and rhizomes undergo concerted convergence under shady conditions in Liliales, they also showed that these patterns distorted phylogenetic inference based solely on morphology. When morphology was analyzed cladistically, two clades—characterized by the alternative suites of traits undergoing concerted convergence—emerged; when these traits were excluded from analysis, the relationships inferred were nearly identical to those deduced from DNA sequence variation. It would now be worthwhile to see if the same holds true for monocots as a whole: if both fruit and venation type are excluded, does an analysis of relationships across monocots based on morphology more closely approach that based on molecular ALISO data? Chase et al. (1995a) have already noted that several of the groups placed at the base of the monocots by morphology alone (Stevenson and Loconte 1995) share reticulate venation. It would also be interesting to evaluate whether— as in Liliales—large, visually conspicuous flowers are mainly found in open habitats with strong illumination by broadspectrum light, and if small, visually inconspicuous flowers are mainly found in shaded sites with low illumination by narrow-spectrum, greenish light. Many forest herbs in eastern North America accord with this prediction (Givnish and Patterson 2000). Across the angiosperms as a whole, this hypothesis may account for the striking increase with rainfall in the fraction of woody species with inconspicuous flowers in tropical forests documented by Gentry (1982), given that most of the tree diversity added in wetter forests are understory species (Givnish 1999a). Repeated shifts to visually inconspicuous flowers in shade to visually conspicuous flowers under bright, full-spectrum light may be analogous to the increased sexual selection for bright coloration in African rift-lake cichlids in clearer waters (Seehausen et al. 1997) and the likely role that an analogous process has played in the evolution of bright coloration in tropical coral-reef fish (Givnish 1999b). ACKNOWLEDGMENTS This study was partly supported by a University of Wisconsin–Madison Vilas research fellowship and NSF grants DEB 9623690 and IBN-9904366 to TJG, by NSERC Discovery grants to SWG, by NSF grant DEB 0129179 to AWM, and by a Smithsonian Institution grant to WJK and LMP. The authors would like to thank Mark Chase (Royal Botanic Gardens, Kew) for kindly providing access to DNA samples for a number of taxa. Several helpful comments on the manuscript were provided by Mark Chase and another anonymous reviewer. LITERATURE CITED ACKERLY, D. D., AND P. B. REICH. 1999. 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