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A Phylogeny and Biogeographic Analysis for the Cape-Pondweed Family Aponogetonaceae (Alismatales) ⇑ Ling-Yun Chen A, Guido W

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A Phylogeny and Biogeographic Analysis for the Cape-Pondweed Family Aponogetonaceae (Alismatales) ⇑ Ling-Yun Chen A, Guido W Molecular Phylogenetics and Evolution 82 (2015) 111–117 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev A phylogeny and biogeographic analysis for the Cape-Pondweed family Aponogetonaceae (Alismatales) ⇑ Ling-Yun Chen a, Guido W. Grimm b, Qing-Feng Wang a, Susanne S. Renner c, a Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, Hubei, PR China b Swedish Museum of Natural History, Department of Palaeobiology, Svante Arrhenius Väg 7, 10405 Stockholm, Sweden c Systematic Botany and Mycology, University of Munich (LMU), Menzinger Strasse 67, 80638 Munich, Germany article info abstract Article history: The monocot family Aponogetonaceae (Alismatales) consists only of Aponogeton, with 57 species occur- Received 2 August 2014 ring in Africa, Madagascar, India and Sri Lanka, Southeast Asia and Australia. Earlier studies inferred a Revised 21 September 2014 Madagascan or Australian origin for the genus. Aponogeton-like pollen is documented from the Late Cre- Accepted 9 October 2014 taceous of Wyoming, the early mid-Eocene of Canada, and the late mid-Eocene of Greenland. We Available online 22 October 2014 obtained nuclear and plastid DNA sequences for 42 species and generated a time-calibrated phylogeny, rooted on appropriate outgroups. Statistical biogeographic analyses were carried out with or without Keywords: the fossils incorporated in the phylogeny. The recent-most common ancestor of living Aponogetonaceae Alismatales appears to date to the mid-Eocene and to have lived in Madagascar or Africa (but not Australia). Three Aquatic plants Biogeography transoceanic dispersal events from Africa/Madagascar to Asia sometime during the Miocene could Integrating fossil geographic ranges explain the observed species relationships. As inferred in earlier studies, an ancient Australian species Molecular clock is sister to all other Aponogetonaceae, while the remaining Australian species stem from an Asian ances- tor that arrived about 5 million years ago. The family’s ancient Northern Hemisphere fossil record and deepest extant divergence between a single Australian species and an Africa/Madagascar clade are statis- tically well-supported and rank among the most unusual patters in the biogeography of flowering plants. Ó 2014 Elsevier Inc. All rights reserved. 1. Introduction of these families, all species-poor with together just 180 species (Les and Tippery, 2013; Iles et al., 2013). Aponogeton is a monocot genus of about 57 species, many of The disjunct geographic range of the Aponogetonaceae has been which are cultivated as aquarium plants. The genus occurs in Africa explained in mainly two ways. Thanikaimoni (1985) thought that (18 species), Madagascar (15 species), Sri Lanka, India, China, the family originated on Madagascar in the mid-Cretaceous and Southeast Asia, and the Malaysian region (together 11 species), dispersed from there to India, while the Indian plate was still close and Australia (13 species; van Bruggen, 1985; Hellquist and to Madagascar. He also followed Raven and Axelrod (1974: 600) in Jacobs, 1998; Jacobs et al., 2006; our Fig. 1). Aponogeton has long suggesting that the temperate Australian species A. hexatepalus been placed in its own family, the Aponogetonaceae, which might decent from a mid-Cretaceous dispersal event to Australia; together with 13 other families make up the Alismatales this is the only species of Aponogeton with two trimerous (Stevens, 2001 onwards), an order of mostly aquatic plants, includ- perianth whorls, while the remaining species retain only the inner ing sea grasses (Cymodoceaceae, Posidoniaceae, Ruppiaceae, whorl. Raven and Axelrod’s suggestion was based on a report of Zosteraceae), freshwater aquatics (Alismataceae, Aponogetona- Upper Cretaceous flowering and fruiting structures from ceae, Butomaceae, Hydrocharitaceae and Potamogetonaceae which Patagonia (Selling, 1947). Study of Selling’s material, however, also include a few sea grasses), plants of marshy habitats shows that it does not represent Aponogeton remains (Grímsson (Juncaginaceae, Maundiaceae, Scheuchzeriaceae, Tofieldiaceae), et al., 2014). and free-floating aquatics (most strikingly Lemnoideae and Pistia A different interpretation of the history of Aponogetonaceae in the Araceae). The Aponogetonaceae are the sister clade to eight was proposed by Les et al. (2005), who concluded that Aponogeton originated in Australia and expanded to its remaining distribution area from there. This was based on the position of A. hexatepalus as sister to the rest of the genus in DNA trees from nuclear and plastid ⇑ Corresponding author. sequences of ten species from Australia, six from Asia, three from E-mail address: [email protected] (S.S. Renner). http://dx.doi.org/10.1016/j.ympev.2014.10.007 1055-7903/Ó 2014 Elsevier Inc. All rights reserved. 112 L.-Y. Chen et al. / Molecular Phylogenetics and Evolution 82 (2015) 111–117 Madagascar, and one from Africa. Les et al. (2003) earlier inferred Australia. Lacking sufficient molecular data, Grímsson et al., of divergence times in Aponogeton, with 23.3 Ma for the split between course, were unable to study the modern family’s biogeography. the African A. distachyos and the Australian A. euryspermus, 15.3 Ma Here we provide a phylogeny and biogeographic analysis for the for that between A. distachyos and the Madagascan A. madagascar- Aponogetonaceae, based on sampling of African, Madagascan, iensis, 13.5 Ma for that of A. euryspermus and the Indian A. crispus, Indian and Chinese species (42 of the 57 species are included) and 15.8 Ma for that of the Indian A. rigidifolius and the Madaga- and formal statistical ancestral area reconstruction on a dated scan A. longiplumosa. These ages came from a strict clock model phylogeny, taking into account the pollen fossils. Ancestral area calibrated with a rate of 0.24% change per million years for trnK reconstructions (AAR) with fossil ranges included directly in the intron and 0.27% for the ITS region (such patristic distances need statistical runs may shed light on a clade’s earliest history, yet to be halved to calculate nucleotide change per site per million few such analyses have been carried out (but see Clayton et al., years). Les and Tippery (2013), after adding eight more species to 2009; Mao et al., 2012; Nauheimer et al., 2012). In such studies, the dataset of Les et al. (2005), upheld the earlier conclusion of fossils ranges are added into a Newick-format phylogenetic tree an Australian origin of the family. as sister to the clade to which the respective fossil has been Newly discovered fossil pollen from North America, Canada, assigned, using artificial branch lengths (since there is no DNA and Greenland, and rejection of Selling’s report of Upper Creta- sequence) that could reflect the fossil age. For the present study, ceous fossils from Argentina/Chile (Patagonia) caused Grímsson we explored this approach to test the hypothesis of Les et al. et al. (2014) to undertake a re-investigation of the family’s biogeo- (2005; Les and Tippery, 2013) of an Australian origin of graphic history using morphological data, compiled mainly from Aponogeton. literature, and molecular data available in GenBank. The three fos- sils are Aponogeton harryi from the Late Cretaceous (82–81 Ma) of Wyoming, USA, A. longispinosum from the early middle Eocene (ca 2. Materials and methods 46 Ma) of British Columbia, Canada, and A. hareoensis from the late middle Eocene (44–40 Ma) of West Greenland. Aponogeton and 2.1. Taxon sampling Butomus (Butomaceae) are the only Alismatales producing mono- sulcate pollen, and these two differ greatly in their exine sculptur- All sequences used in this study, with herbarium vouchers, geo- ing (Grímsson et al., 2014); Aponogeton pollen can therefore graphic origin, and GenBank accession numbers are listed in reliably be assigned as to family. These pollen finds imply that, Appendix S1 (see Supporting Information). The sequences come while the family today is confined to the tropics and subtropics from 45 individuals representing 11 of the 18 African species, 9 of the Old World, during the late Cretaceous and early Cenozoic, of the 11 Asian species, 10 of the 13 Australian species and 12 of it was widespread in the Northern Hemisphere from where it must the 15 Madagascan species. Based on Les and Tippery (2013) and have expanded its range into India, Africa, Madagascar, and Iles et al. (2013), Aponogetonaceae are the sister clade to the (a) 44–40 Ma 46 Ma 82– 81 Ma (b) Fig. 1. Geographical distribution and photographs of Aponogetonaceae. Distribution was mainly compiled from literature: Lye (1989), Hellquist and Jacobs (1998), Jacobs et al. (2006), Zhou and Zhou (1992), and Sundararaghavan et al. (1982). (a) Aponogeton lakhonsis and its habitat (China; 28°380.00.2800N, 119°16016.5700E; 324 m alt.); (b) A. abyssinicus and its habitat (Kenya; 01°07041.8100S, 35°47.22.0800E; 1924 m alt.). Red stars indicate the location of Aponogetonaceae fossils (Grímsson et al., 2014). The straight line indicates the equator. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) L.-Y. Chen et al. / Molecular Phylogenetics and Evolution 82 (2015) 111–117 113 Cymodoceaceae, Juncaginaceae, Maundiaceae, Posidoniaceae, Pot- the major clades of Aponogeton. We used the BEAST package v. amogetonaceae, Ruppiaceae, Scheuchzeriaceae and Zosteraceae,
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