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2023 Sparganium (Typhaceae) Is an Aquatic Genus of ± 14 Species

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2023 Sparganium (Typhaceae) Is an Aquatic Genus of ± 14 Species American Journal of Botany 100(10): 2023–2039. 2013. S YSTEMATICS, BIOGEOGRAPHY, AND CHARACTER EVOLUTION OF SPARGANIUM (TYPHACEAE): DIVERSIFICATION OF A WIDESPREAD, AQUATIC LINEAGE 1 J OSHUA D. SULMAN 2,5 , B RYAN T . D REW 3 , C HLOE D RUMMOND 2 , E ISUKE H AYASAKA 4 , AND K ENNETH J. SYTSMA 2 2 Department of Botany, University of Wisconsin, Madison, Wisconsin 53706 USA; 3 Department of Biology, University of Florida, Gainesville, Florida 32607 USA; and 4 Fukui Botanical Garden, Echizen, 916-0146 Japan • Premise of the study: Sparganium (Typhaceae) is a genus of aquatic monocots containing ± 14 species, with fl owers aggregated in unisexual, spherical heads, and habit ranging from fl oating to emergent. Sparganium presents an opportunity to investigate diversifi cation, character evolution, and biogeographical relationships in a widespread temperate genus of aquatic monocots. We present a fossil-calibrated, molecular phylogeny of Sparganium based on analysis of two chloroplast and two nuclear mark- ers. Within this framework, we examine character evolution in both habit and stigma number and infer the ancestral area and biogeographic history of the genus. • Methods: Sequence data from two cpDNA and two nDNA markers were analyzed using maximum parsimony, maximum likelihood, and Bayesian inference. We used the program BEAST to simultaneously estimate phylogeny and divergence times, S-DIVA and Lagrange for biogeographical reconstruction, and BayesTraits to examine locule number and habit evolution. • Key results: Two major clades were recovered with strong support: one composed of S. erectum and S. eurycarpum ; and the other containing all remaining Sparganium . We realigned the subgenera to conform to these clades. Divergence time analysis suggests a Miocene crown origin but Pliocene diversifi cation. Importantly, the fl oating-leaved habit has arisen multiple times in the genus, from emergent ancestors—contrary to past hypotheses. • Conclusions: Cooling trends during the Tertiary are correlated with the isolation of temperate Eurasian and North American taxa. Vicariance, long-distance dispersal, and habitat specialization are proposed as mechanisms for Sparganium diversifi cation. Key words: aquatic habit; biogeography; BEAST; Beringia; bur-reed; monocot; Pliocene; Poales; Sparganium ; Typhaceae. Sparganium (Typhaceae) is an aquatic genus of ± 14 species. relationships of extant species, and test the current classifi ca- Species of Sparganium are ecologically important in aquatic tion of the genus; use a fossil-calibrated chronogram to uncover communities, providing cover and food for a variety of waterfowl patterns of biogeographic spread across the Northern Hemi- and mammals ( Arber, 1920 ; Fassett, 1940 ). Bur-reeds provide sphere under vicariance and dispersal models; and estimate the forage for cattle, especially during dry periods ( Aston, 1987 ), transitions and evolutionary implications of two key morpho- but may become a nuisance, choking waterways ( Cook and logical features of this aquatic genus—growth form and ovary/ Nicholls, 1987 ). Traditionally, bur-reeds have been used as a stigma number. medicinal herb to improve blood circulation ( Tulin et al., 1999 ) Sparganium occupy aquatic habitats primarily in temperate and as a food source ( Moerman, 1998 ). Though of minor eco- and cool regions, and several species show wide-ranging, cir- nomic importance, Sparganium are of biogeographical, phyloge- cumboreal distributions. The latter include S. angustifolium , netic, and evolutionary interest. We examine here with nuclear S. emersum , S. glomeratum , S. natans , and S. hyperboreum. These (nDNA) and chloroplast (cpDNA) regions the phylogenetic species have limited range extensions southward at high ele- vations in Eurasia and North America. The remaining species 1 are limited to either Eastern or Western Hemisphere distribu- Manuscript received 4 February 2013; revision accepted 25 June 2013. tions. The centers of diversity in the genus are eastern North The authors thank the many people who contributed to this research, especially Mami Yamazaki who collected in northern Japan, Richard Ree America (9–10 spp.), East Asia (10–13 spp.), and Europe (7 spp.; who contributed material from China, Rachel Jabaily who provided ITS Cook and Nicholls, 1986 ; Kaul, 1997 ; Sun and Simpson, 2010 ). sequences of Puya , S. Galen Smith who provided guidance and shared his Sparganium fallax and S. subglobosum are primarily East expertise in aquatic plants, and Greg Virnig, Sarah Paust, Susan Knight, Asian, but also appear in the mountains of New Guinea ( Cook Eric Rossborough, and Erin McGrath who assisted in fi eld work. Special and Nicholls, 1986 ). Only two species ( S. subglobosum and thanks to Tom Givnish, Ken Cameron, Ted Cochrane, Mark Wetter, and S. erectum ) reach the Southern Hemisphere in Australia and Takanori Toriyama for technical advice, to Sarah Friedrich for assistance New Zealand, where S. erectum was probably introduced ( Cook with the fi gures, and to two anonymous reviewers whose comments and and Nicholls, 1987 ). Distributional patterns and morphological insights made this a much better paper. They are grateful to staff at MO, similarities have suggested close relationships between North ALA, HAST, MIN and WIS for sharing material used in this study. The fi eldwork was funded in part by a Davis Research Award from the American and Eurasian species pairs, such as S. fl uctuans–S. UW-Madison Dept. of Botany. gramineum and S. americanum–S. japonicum ( Cook and Nicholls, 5 Author for correspondence (e-mail: [email protected]) 1987 ), but these relationships have not been evaluated in a molecular context. Though Sparganium was until recently un- doi:10.3732/ajb.1300048 known from Central and South America ( Cook and Nicholls, American Journal of Botany 100(10): 2023–2039, 2013 ; http://www.amjbot.org/ © 2013 Botanical Society of America 2023 2024 AMERICAN JOURNAL OF BOTANY [Vol. 100 1986 ), its occurrence has been documented in west-central ( Sculthorpe, 1967 ; Cook, 1996 ; Barrett and Graham, 1997 ). Mexico ( Kaul, 1997 ; Socorro González Elizondo et al., 2007 ) Recently, increased attention has been focused on examples of and Colombia, and vouchers from both locales were reviewed for species radiation and character evolution in aquatic groups of this study (see Appendix 1). Without DNA evidence, it is diffi cult angiosperms using phylogenetic methods. Several recent stud- to say whether these represent disjunct populations of S. ameri- ies have applied character state reconstruction to assess diver- canum (as identifi ed), S. emersum , or undescribed species. sifi cation in aquatic growth form, revealing complex patterns Though Sparganium has traditionally been placed in Spargani- of transition between emergent, fl oating, and submerged habits aceae, Sparganium and Typha are now both placed in Typhaceae ( Barrett and Graham, 1997 ; Chen et al., 2004 , 2012 ; Moody and ( APG III, 2009 ), as was earlier advocated by Müller-Doblies Les, 2007 ) and between rosulate (rosette) and vittate (caules- (1970) based on the lack of signifi cant differences in fl ower and cent) habits ( Les et al., 2008 ). The genus Sparganium pres- infl orescence morphology. Support for the monophyly of Typha + ents an opportunity to assess the evolution of divergent growth Sparganium is well established based on intensive phylogenetic forms and locule numbers in a widespread, primarily Northern study of monocots in recent years ( Bremer, 2000 ; Chase et al., Hemisphere genus of aquatic monocots. 2006 ; Givnish et al., 2007 , 2010 , 2011 ; Soltis et al., 2011 ). Spar- Rooted aquatic plants can be divided into three groups based ganium and Typha constitute an early-diverging lineage within on growth form: emergent, fl oating, or submerged ( Sculthorpe, the Poales ( Bremer, 2000 ; Chase et al., 2006 ; Givnish et al., 2010 , 1967 ; Schuyler, 1984 ). Sparganium species exhibit a striking 2011 ), with phylogenetic analysis of whole plastome sequences dichotomy in growth form between emergent and fl oating hab- across monocots placing the family as the second-diverging lin- its ( Fig. 1 ), an uncommon occurrence within a single genus of eage after Bromeliaceae ( Givnish et al., 2010 ). However, the po- aquatic vascular plants. Whether the ancestral habit in Sparga- sition of Typhaceae has the lowest support within the Poales nium was emergent or fl oating has been the subject of contro- (87–97% bootstrap). The placement of Sparganium as an early- versy. Cook and Nicholls (1986 , p. 227) suggested that the diverging lineage in Poales, complemented with a rich fossil fl oating growth form was the ancestral state and that the “evolu- record dating to the Paleocene, make this group an intriguing tionary trend from small aquatic species to large terrestrial spe- subject for molecular dating of key events. cies is clear.” Kaul (1972) , in comparing leaf anatomy in fl oating Despite the distinctiveness of Sparganium as a genus and its and emergent Sparganium , identifi ed features such as stomata apparent monophyly based on the inclusion of fi ve Sparganium on the underside of fl oating leaves as evidence that the fl oating species in a recent phylogenetic study of Typha ( Kim and Choi, form was derived. No rigorous phylogenetic analysis of growth 2011 ), the phylogenetic relationships within Sparganium have form evolution in Sparganium has been done, or evidence of not previously received intensive study. Its species and their multiple growth form transitions presented. relationships
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