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Eurasian origin of Alismatidae inferred from statistical dispersal–vicariance analysis
Molecular Phylogenetics and Evolution 67 (2013) 38–42
By Saravanan K at 2:36 pm, Feb 01, 2013
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Short Communication
Eurasian origin of Alismatidae inferred from statistical dispersal–vicariance analysis Ling-Yun Chen a,b, Jin-Ming Chen a,b, Robert Wahiti Gituru c, Qing-Feng Wang a,b,⇑ a
Key Laboratory of Aquatic Botany and Watershed Ecology, The Chinese Academy of Sciences, Wuhan 430074, Hubei, PR China Wuhan Botanical Garden, The Chinese Academy of Sciences, Wuhan 430074, Hubei, PR China c Botany Department, Jomo Kenyatta University of Agriculture and Technology, P.O. Box 62000-00200, Nairobi, Kenya b
a r t i c l e
i n f o
Article history: Received 7 July 2012 Revised 26 December 2012 Accepted 4 January 2013 Available online 16 January 2013 Keywords: Alismatidae Phylogeny Biogeography Dispersal
a b s t r a c t Alismatidae is a wetland or aquatic herb lineage of monocots with a cosmopolitan distribution. Although considerable progress in systematics and biogeography has been made in the past several decades, geographical origin of this group remains unresolved. In this study, we used statistical dispersal–vicariance analysis implemented in program RASP to investigate the biogeography of Alismatidae. Six areas of endemism were used to describe the distribution: North America, South America, Eurasia, Africa, Southeast Asia and Australia. 18,000 trees retained from Bayesian inference of rbcL served as a framework to reconstruct the ancestral areas. The results suggested that the most recent common ancestor of Alismatidae most probably occurred in Eurasia, followed by a split into two major clades. The clade comprising Hydrocharitaceae, Butomaceae and Alismataceae mainly diversified in Eurasia and Africa. The other clade comprising the remaining families dispersed to southern hemisphere. Australia played an important role in diversification of this clade. Several families were suggested to have occurred in Australia, such as Ruppiaceae, Cymodoceaceae, Posidoniaceae and Zosteraceae. Ó 2013 Elsevier Inc. All rights reserved.
1. Introduction Alismatidae is a monocot group with a worldwide distribution. The group is imbedded within the order Alismatales, which includes two other families, Araceae and Tofieldiaceae (Stevens, 2012). According to Les et al. (1997), the group consists of 14 families, 57 genera and about 500 species. However, as currently circumscribed, Alismatidae consists of 12 families (Stevens, 2012) and 56 genera, in which, Limnocharitaceae was merged into Alismataceae (Stevens, 2012; Chen et al., 2012a), Lilaeaceae was merged into Juncaginaceae (Stevens, 2012), Zannichelliaceae was merged into Potamogetonaceae (Stevens, 2012), Maundia was treated as a separate family Maundiaceae (von Mering and Kadereit, 2010) and Maidenia was merged into Vallisneria (Les et al., 2008). All marine angiosperms and most water-pollinated angiosperms are taxonomically confined to this group (Cook, 1990; Les et al., 1997). Members of Alismatidae are wetland or aquatic herbs. Additionally, most of the members have a completely submerged seedling phase, and flowers could either be floating or emergent. Vegetation may be totally submerged, with the leaves floating, or protruding from water (Chen et al., 2004). In the past several years, there has been a substantial improvement of our knowledge on the evolution of monocots. Presently, Alismatidae is largely considered as one of the most ancient groups ⇑ Corresponding author at: Wuhan Botanical Garden, The Chinese Academy of Sciences, Wuhan 430074, Hubei, PR China. Fax: +86 27 87510526. E-mail address: [email protected] (Q.-F. Wang). 1055-7903/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2013.01.001
of monocots (e.g. Tamura et al., 2004). The first phylogeny of Alismatidae with comprehensive samples was proposed by Les et al. (1997) based on rbcL. Les et al. (1997) divided Alismatidae into two major groups. One group consists of Alismataceae, Butomaceae and Hydrocharitaceae, while the other consists of the remaining families. Several studies based on rbcL (Chen et al., 2004; von Mering and Kadereit, 2010) and combined rbcL and morphological data (Li and Zhou, 2009) also supported the result of Les et al. (1997). The interfamilial relationships within Alismatidae inferred from mitochondrial genes (Petersen et al., 2006; Cuenca et al., 2010) were generally congruent with those based on rbcL data except for the position of Alismataceae. Therefore, the phylogeny of Alismatidae inferred from rbcL was widely accepted by researchers. Great progress has been made in the last decade in the estimation of divergence times of Alismatidae. Les et al. (2003) used molecular data to estimate the divergence times for some closely related taxa within Alismatidae. The study suggested that the genus level divergence occurred in the Eocene and Oligocene. Based on the analysis using rbcL and fossil calibration points, Janssen and Bremer (2004) proposed that Alismatidae originated around 108 Ma, which is similar to the result by Magallon and Castillo (2009). In addition, the ages of the major lineages within Alismatidae were also estimated by Janssen and Bremer (2004), although they may be affected by a comparatively limited taxon sampling. Recently, we presented the dated phylogenies of Alismataceae and Hydrocharitaceae, which suggested Late Cretaceous or Paleocene origin times of the two families (Chen et al., 2012a,
L.-Y. Chen et al. / Molecular Phylogenetics and Evolution 67 (2013) 38–42
2012b). The above-mentioned divergence times of Alismatidae provided us with a solid basis for understanding the historical biogeography of the group. However, the geographical origin of Alismatidae remains unresolved. Lindqvist et al. (2006) thought that aquatic angiosperms, in general, have a wider distribution than their terrestrial relatives. This remarkably wide distribution has in itself become a challenge in pinpointing geographic origins for aquatic angiosperms. Alismatidae is no exception, although several biogeographic studies related to this group have been reported. Bremer and Janssen (2006) had suggested a Gondwanan origin of the major monocot groups based on a dispersal–vicariance analysis with 79 of the 81 monocot families. However, the study failed to resolve the geographic origin of Alismatales and Alismatidae due to a high number of possible area combinations suggested in the analysis. This may be attributed to their use of families rather than genera or species as terminal taxa in the dispersal–vicariance analysis. The geographical origin of several genera within Alismatidae is still a subject of debate. For example, Miki (1937) and Les (1983) considered East Asia as the area of origin of Potamogeton, based on fossil records and chromosome number. However, the opinion was challenged by Lindqvist et al. (2006) who argued Potamogeton originated in North America. With respect to the transoceanic distributions of organisms, two competing processes have been proposed: vicariance and dispersal. It is interesting to investigate which process was mainly responsible for the transoceanic distribution pattern of Alismatidae. To address the geographical origin of Alismatidae, this paper aims to reconstruct the possible ancestral ranges of Alismatidae using statistical dispersal–vicariance analysis (S-DIVA). Combined with the available information of divergence times of the group (Les et al., 2003; Janssen and Bremer, 2004; Chen et al., 2012a, 2012b), we try to obtain a hypothesis explaining its biogeographical history.
39
ally, and all gaps were treated as missing. The gene after manual edit was 1191 bp in length, starting at 30 bp downstream of the start site, and ending at 226 bp upstream of the end site (Data 1, Supplementary). 2.2. Biogeograhical analysis The recently developed statistical dispersal–vicariance analysis (S-DIVA) implemented in RASP (Yu et al., 2012) was used to reconstruct the possible ancestral ranges of Alismatidae on phylogenetic trees. In S-DIVA, the frequencies of an ancestral range at a node in ancestral reconstructions are averaged over all trees. To account for phylogenetic uncertainty, we inferred the distributions by integrating 18,000 trees from Bayesian MCMC analysis. The Bayesian trees were generated using MrBayes v3.1.2 (Ronquist and Huelsenbeck, 2003) with rbcL, run for 10,000,000 generations, sampled every 1000 generations. GTR + I + G was selected as the best-fit model of DNA substitution with the Akaike Information Criterion (AIC) in MrModeltest v2.3 (Nylander, 2004). The first 10% generations were discarded. The remaining 18,000 trees (9000 2) (Data 2, Supplementary) were used for computing Condense Tree and SDIVA in RASP. We defined the geological criterion according to Bremer and Janssen (2006), and palaeogeographical history (i.e. plate tectonics). In all, six geographical areas were used to describe the distribution of Alismatidae and outgroup taxa: A, North America; B, South America; C, Eurasia; D, Africa; E, Southeast Asia; F, Australia (Fig. 1a). We used genera as terminal taxa. Each genus was coded based on its current distribution, which was mainly compiled from literatures (e.g. Cook, 1990; von Mering and Kadereit, 2010; Azuma and Tobe, 2011). The distribution data was presented (Data 3, Supplementary). The number of maximum areas at each node was setted as 4. Divergence times of Alismatidae was cited from Chen et al. (2012a, 2012b) and Janssen and Bremer (2004).
2. Materials and methods 2.1. Taxa sampling and sequence alignment Fifty-two terminals representing 52 genera in 12 families of Alismatidae were selected. Eighteen genera were chosen as outgroup taxa. Tofieldiaceae (Alismatales) and Araceae (Alismatales) are the closest relatives of Alismatidae (Tamura et al., 2004). All genera of Tofieldiaceae (viz. Tofieldia, Pleea, Harperocallis, Isidrogalvia, Triantha) were selected as outgroup taxa. Based on molecular phylogenetic analyses, Araceae, which includes 117 genera (Nauheimer et al., 2012), was separated into ten major groups (Cabrera et al., 2008). Therefore, one genus for each group was selected as outgroup taxa. Petrosaviales (Petrosaviaceae), which includes two genera (viz. Japonolirion and Petrosavia), is a sister to Alismatales (Tamura et al., 2004). The two genera were chosen as outgroups. In addition, Acorus, the lone genus in Acoraceae (Acorales), was also selected as an outgroup following the methodology in Les et al. (1997). Prior to present study, large numbers of rbcL sequences for Alismatid plants except three genera (viz. Appertiella, Althenia and Pseudalthenia) have been reported. Therefore, all the rbcL sequences used in our analyses, except Butomopsis latifolia, were obtained from GenBank (Table A1, Supplementary). In order to improve the credibility of sequences, the sequences generated by Les et al. (1993, 1997) and our lab were preferentially selected. The rbcL of B. latifolia was amplified according to methodology in Chen et al. (2012a). Purified PCR product was ligated to pMD18-T vector (Takara Biotech Co., Dalian, China), and six positive clones were sequenced. The newly generated sequence was submitted to GenBank (Table A1, Supplementary). Sequences were aligned using Clustal X v2.0 (Thompson et al., 1997) with default parameters. The output was inspected manu-
3. Results The Condense Tree retained from computing the Bayesian MCMC trees divided Alismatidae into two major clades (Fig. 1b). (1) Clade A consists of Alismataceae, Butomaceae and Hydrocharitaceae. Alismataceae was divided into two major suclades. Limnocharis, Hydrocleys and Butomopsis were nested within Alismataceae, and Butomaceae clustered together with it. (2) Clade B consists of the remaining nine families of Alismatidae. From the S-DIVA, it could be inferred that the most recent common ancestor (MRCA) of Alismatidae occurred in Eurasia with a relative probability of 84% (Fig. 1b, Table 1). The result shows that a Eurasian origin for the two major clades (Clade A (probability 90%) and B (probability 69%)), Hydrocharitaceae (probability 86%), subclade Alismataceae + Butomaceae (probability 86%) is most likely. In addition, the clade formed by Alismatidae, Araceae and Tofieldiaceae (excluding Isidrogalvia) share a common ancestor whose ancestral distribution area is Eurasia (probability 100%). Clade B suggested a widespread occurrence in Australia (Fig. 1b), pointing to an Australian origin for some families of this clade, e.g. Zosteraceae, Cymodoceaceae. The possible ancestral ranges of Juncaginaceae were suggested to be South America (a probability of 33%), South America and Australia (probability 33%), Americas and Australia (probability 33%).
4. Discussion Alismatidae was divided into two major clades in our analysis. The interfamilial relationships of the group were generally similar
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(c)
(b)
5
4 1
Tertiary
2
3
D
Limnophyton sp. (DEF) Wiesneria triandra (DE) Sagittaria latifolia (ABCDE) BD ABD 23 Echinodorus grandiflorus (AB) Caldesia parnassifolia (CDEF) 5 D D Burnatia enneandra (D) Alisma plantago-aquatica (ACD) C C 8 Baldellia ranunculoides (C) Alismataceae C Damasonium alisma (ACDEF) CD Luronium natans (C) Hydrocleys nymphoides (BCDE) 7C C Butomopsis latifolia (DEF) BC Limnocharis flava (BCDE) B Ranalisma rostratum (CDE) Butomus umbellatus (CDE) Butomaceae Vallisneria natans (ABCDEF) C E Nechamandra alternifolia (E) C Hydrilla verticillata (CE) CE E E Enhalus acoroides (CDEF) 6 E CE Thalassia hemprichii (BCDEF) C Halophila engelmannii (ABCDEF) CE CE C C E C Najas marina (ABCDEF) Hydrocharitaceae C AB Stratiotes aloides (C) CD Egeria densa (B) B Elodea nuttallii (A) CDE C Apalanthe granatensis (B) D C Ottelia alismoides (BCDEF) 9 BC Blyxa aubertii (CDEF) BCD C Lagarosiphon muscoides (D) Hydrocharis morsus-ranae (CDEF) Limnobium spongia (AB) Ruppia megacarpa (ABCDEF) Ruppiaceae 20 F Syringodium filiforme (BCEF) F Cymodocea serrulata (CEF) 21 Cymodoceaceae F 19 Amphibolis antarctica (F) F F Thalassodendron pachyrhizum (DEF) Posidonia oceanica (CEF) Posidoniaceae 22 F Halodule beaudettei (ABCDEF) Cymodoceaceae 15 Phyllospadix torreyi (ABCEF) F 17 F Heterozostera tasmanica (F) Zosteraceae F Zostera marina (ABCDEF) 16 F Potamogeton crispus (ABCDEF) 14 F Coleogeton pectinatus (ABCDEF) F F Lepilaena australis (F) 18 F Zannichellia palustris (ABCDEF) Potamogetonaceae BF CF EF DF Groenlandia densa (CDE) 12 F Maundia triglochinoides (F) Maundiaceae Lilaea scilloides (AB) B 11 Triglochin maritimum (ABCDF) AF F Juncaginaceae 13 Cycnogeton procerum (F) BF BF ACF 10 ABF Tetroncium magellanicum (B) Scheuchzeria palustris (AC) Scheuchzeriaceae C Aponogeton elongatus (CDEF) Aponogetonaceae C Tofieldia glutinosa (AC) C Triantha japonica (AC) Tofieldiaceae C Harperocallis flava (C) (Alismatales) Pleea tenuifolia (C) Lysichiton americanus (AC) CF ACF Gymnostachys anceps (F) Callopsis volkensii (D) DE Podolasia stipitata (E) Stenospermation ulei (B) Araceae BDF Pothoidium lobbianum (CE) (Alismatales) E C Stylochaeton bogneri (D) CD CDE Calla palustris (AC) CE Pseudodracontium lacourii (E) BC Spirodela polyrrhiza (ABCDEF) BC C BC Isidrogalvia schomburgkiana (B) Tofieldiaceae (Alismatales) Petrosavia sakuraii (CE) BCE Japonolirion osense (C) Petrosaviaceae (Petrosaviales) C Acorus tatarinowii (ACE) Acoraceae (Acorales) AD
D
Clade A
Ancestral area of Alismatidae Major dispersal routes
(a)
C
5
4C
3C
1 ACE
C
BC
ABCE
Outgroup
2
Clade B
Undefined A North America B South America C Eurasia D Africa E Southeast Asia F Australia
Fig. 1. Biogeography of Alismatidae. (a) Area delimitation in biogeographic analysis; distribution of each genus is indicated along with species name. (b) Reconstruction of ancestral distributions of Alismatidae using statistical dispersal–vicariance analysis in RASP. The pie charts represent the relative probability of ancestral areas reconstructed for each node. The area(s) with highest probability are also marked with letters. (c) Ancestral area of Alismatidae and the five main possible dispersal routes.
to those based on rbcL in previous studies (Les et al., 1997; Chen et al., 2004; von Mering and Kadereit, 2010). Our biogeographical analysis suggested that the MRCA of Alismatidae most probably originated in Eurasia. Previous studies proposed that Alismatidae originated around 108 Ma (Janssen and Bremer, 2004), with all the families presented in the Late Creta-
ceous and early Tertiary periods (Les et al., 2003; Janssen and Bremer, 2004; Chen et al., 2012a, 2012b). The breakup of Pangaea occurred during 230–148 Ma (Labails and Roest, 2010), resulting in Gondwana and Laurasia. The modern continents viz. South America, Africa, Eurasia, Australia and North America have been separated by oceans since at least ca. 105 Ma (Davis et al., 2002).
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Table 1 Results of biogeographic analysis of Alismatidae. The first three area(s) with highest probability for major nodes of Alismatidae under S-DIVA are shown (separated by a slash). The mean ages for some nodes are presented, cited from (1) Janssen and Bremer (2004); (2) Chen et al. (2012a); (3) Chen et al. (2012b). Node
S-DIVA
Age (Ma)
Node
S-DIVA
Age (Ma)
1 2 3 4 5 6 7 8 9 10 11
ACE (0.82)/ABCE (0.18) C (0.82)/BC (0.18) C (1.00) C (1.00) C (0.84)/CD (0.09) C (0.90)/CD (0.09) C (0.86)/CDE (0.06)/CD/(0.06) CD (0.64)/BCD (0.10)/BC (0.06) C (0.86)/CDE (0.06) C (0.69)/CF (0.14)/ACF (0.09) ACF (0.17)/CF (0.17)/BC (0.16)
– – – – Ca. Ca. – Ca. Ca. Ca. Ca.
12 13 14 15 16 17 18 19 20 21 22
F (0.50)/BF (0.50) ABF (0.33)/BF (0.33)/B (0.33) F (1.00) F (1.00) F (1.00) F (1.00) CF (0.15)/DF (0.15)/EF (0.15) F (1.00) F (1.00) F (1.00) F (1.00)
Ca. Ca. Ca. – Ca. Ca. – – – –
1081 951 792 663 98 1 92 1
Therefore, the transoceanic distribution of Alismatidae among the modern continents might be resulted from dispersals involving land bridges, island chains or long-distance dispersal. The MRCAs of the two major clades were also suggested to have occurred in Eurasia (Fig. 1b). For clade A, Hydrocharitaceae was found to have originated in Eurasia (probability 86%), a result similar to Chen et al. (2012b) which suggested the family originated in Asia. Alismataceae and the clade (Alismataceae + Butomaceae) were suggested to occur most probably in Eurasia. Alismataceae split into two major clades, mainly diversified in Eurasia and Africa separately (Fig. 1b). Dispersal of Alismataceae plants from Eurasia to Africa might have occurred (Fig. 1b, node 7 ? 23; Fig. 1c, arrow 1). For example, the clade (Limnophyton (Wiesneria + Sagittaria)) diversified in Africa, and radiated into South America, Asia, Australia, etc. (detailedly discussed in Chen et al. (2012a)). For clade B, the early plants have dispersed from Eurasia to Australia (Fig. 1b, node 10 ? 14; Fig. 1c, arrow 2), consistent with the viewpoint that biota exchanges between southern Asia and Australia during the Tertiary existed, via the Ninetyeast Ridge (Cruaud et al., 2011), Malay Archipelago (van Welzen et al., 2005) or transoceanic dispersals. Clade B mainly diversified in Australia (Fig. 1b, node 14). From Australia, the plants dispersed to all over the world. The dispersal from Eurasia to Africa and Australia also occurred in Hydrocharitaceae and Alismataceae plants (Chen et al., 2012a, 2012b), e.g., Vallisneria. In addition, other three major dispersal routes involving in the world widely distribution of Alismatidae: (1) Transoceanic dispersal from Africa to South America during the Late Cretaceous and Tertiary periods (Fig. 1c, arrow 3). For example, Ottelia and Sagittaria were proposed to have dispersed from Africa to South America in the Tertiary (Chen et al., 2012a, 2012b). In South America, some Alismatid plants diversified and radiated into North America, e.g., Echinodorus (Chen et al., 2012a). (2) Dispersal from Europe to North America via the North Atlantic Land Bridge (NALB) (Fig. 1c, arrow 4), which connected western Europe and eastern North America from the early Paleocene to the Late Miocene (Denk et al., 2010). (3) Dispersal from eastern Asia to North America, via the Bering Land Bridge (BLB) (Fig. 1c, arrow 5), which connected western North America and eastern Asia from at least the early Paleocene until 7.4–4.8 Ma (Marincovich and Gladenkov, 1999). For example, the clade comprises Luronium, Alisma, Baldellia and Damasonium was inferred to have occurred in Eurasia, and radiated into North America, via the NALB and BLB (Fig. 1b). Moreover, ocean currents have played an important role in the widespread distribution of Alismatidae, especially the seagrasses (Brasier, 1975). Mukai (1993) proposed that the Kuroshio Current taken seagrasses such as Thalassia and Halophila from the equator to the Nansei Islands. Aponogetonaceae comprises one genus Aponogeton, with approximate 50 species that are mainly distributed in tropical or subtropical regions of the Old World (Les et al., 2005). Les et al. (2005) proposed that Aponogeton originated and diversified in Aus-
821 521 751 471 171
tralia. Our biogeographic anlaysis suggested that early plants of Alismatidae have dispersed from southern Asia to Australia. Therefore, the ancestor of Aponogeton would be from Eurasia. On the other hand, Aponogeton is widely distributed in India, Southeast Asia and Africa. The plants might have dispersed from Australia to these areas (Les et al., 2005). However, divergence times of the family are not well resolved. Further studies are required to resolve this problem. The seagrass families Posidoniaceae, Cymodoceaceae, Zosteraceae and Ruppiaceae are suggested to have originated from Australia. Les et al. (1997) and Kato et al. (2003) proposed that seagrasses had independently arisen from their fresh water relatives in the course of habitat alteration from fresh to salty waters. This viewpoint supported the Australian origin, because the dispersal event from southern Asia to Australia (across the ocean systems of the western Pacific) presented the habitat changes from fresh to salty water crucial for seagrass development. Mukai (1993) proposed that the coastal waters of Malesia enclosed by Indonesia, Borneo, Papua New Guinea and Torres Strait (northern Australia) were the centers of origin for the seagrass species in the western Pacific. His viewpoint contradicts with our finding that seargrasses might have originated from Australia. This is probably due to the widespread distribution of seagrasses in coastal waters of Malesia and Australia. Eurasia, Africa, Southeast Asia and Australia (the Old World) were found to be the ancestral areas for the subclade formed by genera of Potamogetonaceae. In addition, Australia was found to be the ancestral area for the deep nodes within this subclade (Fig. 1b). The Old World origin of Potamogeton inferred from our analysis contradicts the suggestion that the genus originated in North America (Lindqvist et al., 2006). However, the result is supported by the fact that the most ancestral species of Potamogeton are endemic to Australia (Lindqvist et al., 2006), and also supported by Miki (1937) and Les (1983) who suggested that the genus originated in Asia. Therefore, Potamogeton might have originated in the Old World (mostly probably in Australia) and dispersed to North America. Janssen and Bremer (2004) estimated the stem node age of Potamogetonaceae to be 47 Ma. This age coincides with the existence of biotic exchanges between southern Asia and Australia, and the BLB, which facilitated biotic exchanges between Asia and North America from at least the early Paleocene until 7.4– 4.8 Ma. This study suggests that the MRCA of Alismatidae most probably originated in Eurasia. The clade comprises Hydrocharitaceae, Alismataceae and Butomaceae mainly diversified in Eurasia and Africa; the clade comprises other families would have dispersed to southern hemisphere and diversified in Australia and South America. Although our study has resolved the geographical origin of Alismatidae, biogeography for several families (e.g., Juncaginaceae, Zosteraceae) may suffer from underrepresentation in sampling. To thoroughly understand the origin and dispersal of
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Alismatidae, future studies should try to include comprehensive samples for underrepresented families. Acknowledgments We thank Can Dai for revising this manuscript. We thank Kuo Liao, Yong-Qing Zhu, Shu-Ying Zhao and Suman Neupane for their comments on this manuscript. We appreciate two anonymous reviewers for their valuable suggestions to improve the manuscript. We appreciate Susanne S. Renner for suggestion on the title of this manuscript. We appreciate Laszlo Csiba for providing the DNA samples of Butomopsis latifolia. This work was supported by grants from One Hundred Person Project of the Chinese Academy of Sciences (KSCX2-YW-Z-0805), National Natural Science Foundation of China (30970202) and Strategic Pilot Science and Technology Projects of the Chinese Academy of Sciences (XDAO5090305). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.ympev.2013.01.001. References Azuma, H., Tobe, H., 2011. Molecular phylogenetic analyses of Tofieldiaceae (Alismatales): family circumscription and intergeneric relationships. J. Plant. Res. 124, 349–357. Brasier, M.D., 1975. An outline history of seagrass communities. Palaeontology 18, 681–702. Bremer, K., Janssen, T., 2006. Gondwanan origin of major monocot groups inferred from dispersal–vicariance analysis. Aliso 22, 22–27. Cabrera, L.I., Salazar, G.A., Chase, M.W., Mayo, S.J., Bogner, J., Davila, P., 2008. Phylogenetic relationships of aroids and duckweeds (Araceae) inferred from coding and noncoding plastid DNA. Am. J. Bot. 95, 1153–1165. Chen, J.M., Robert, G.W., Wang, Q.F., 2004. Evolution of aquatic life-forms in Alismatidae: Phylogenetic estimation from chloroplast rbcL gene sequence data. Isr. J. Plant Sci. 52, 323–329. Chen, L.Y., Chen, J.M., Gituru, R.W., Temam, T.D., Wang, Q.F., 2012a. Generic phylogeny and historical biogeography of Alismataceae, inferred from multiple DNA sequences. Mol. Phylogenet. Evol. 63, 407–416. Chen, L.Y., Chen, J.M., Gituru, R.W., Wang, Q.F., 2012b. Generic phylogeny, historical biogeography and character evolution of the cosmopolitan aquatic plant family Hydrocharitaceae. BMC Evol. Biol. 12, 30. Cook, C.D.K., 1990. Aquatic Plant Book. SPB Academic Publishing, Hague. Cruaud, A., Jabbour-Zahab, R., Genson, G., Couloux, A., Peng, Y.Q., Rong, Y.D., Ubaidillah, R., Pereira, R.A.S., Kjellberg, F., van Noort, S., Kerdelhue, C., Rasplus, J.Y., 2011. Out of Australia and back again: the world-wide historical biogeography of non-pollinating fig wasps (Hymenoptera: Sycophaginae). J. Biogeogr. 38, 209–225. Cuenca, A., Petersen, G., Seberg, O., Davis, J.I., Stevenson, D.W., 2010. Are substitution rates and RNA editing correlated? BMC Evol. Biol. 10, 349. Davis, C.C., Bell, C.D., Mathews, S., Donoghue, M.J., 2002. Laurasian migration explains Gondwanan disjunctions: evidence from Malpighiaceae. Proc. Natl. Acad. Sci. USA 99, 6833–6837. Denk, T., Grimsson, F., Zetter, R., 2010. Episodic migration of oaks to Iceland: evidence for a North Atlantic ‘‘land bridge’’ in the latest Miocene. Am. J. Bot. 97, 276–287.
Janssen, T., Bremer, K., 2004. The age of major monocot groups inferred from 800+rbcL sequences. Bot. J. Linn. Soc. 146, 385–398. Kato, Y., Aioi, K., Omori, Y., Takahata, N., Satta, Y., 2003. Phylogenetic analyses of Zostera species based on rbcL and matK nucleotide sequences: Implications for the origin and diversification of seagrasses in Japanese waters. Genes Genet. Syst. 78, 329–342. Labails, C., Roest, W.R., 2010. Comment on ‘Breakup of Pangaea and plate kinematics of the central Atlantic and Atlas regions’ by Antonio Schettino and Eugenio Turco. Geophys. J. Int. 183, 96–98. Les, D.H., 1983. Taxonomic implications of aneuploidy and polyploidy in Potamogeton (Potamogetonaceae). Rhodora 85, 301–323. Les, D.H., Cleland, M.A., Waycott, M., 1997. Phylogenetic studies in Alismatidae, II: evolution of marine angiosperms (seagrasses) and hydrophily. Syst. Bot. 22, 443–463. Les, D.H., Crawford, D.J., Kimball, R.T., Moody, M.L., Landolt, E., 2003. Biogeography of discontinuously distributed hydrophytes: a molecular appraisal of intercontinental disjunctions. Int. J. Plant Sci. 164, 917–932. Les, D.H., Garvin, D.K., Wimpee, C.F., 1993. Phylogenetic studies in the monocot subclass Alismatidae: evidence for a reappraisal of the aquatic order Najadales. Mol. Phylogenet. Evol. 2, 304–314. Les, D.H., Jacobs, S.W.L., Tippery, N.P., Chen, L., Moody, M.L., WilstermannHildebrand, M., 2008. Systematics of Vallisneria (Hydrocharitaceae). Syst. Bot. 33, 49–65. Les, D.H., Moody, M.L., Jacobs, S.W.L., 2005. Phylogeny and systematics of Aponogeton (Aponogetonaceae): the Australian species. Syst. Bot. 30, 503–519. Li, X.X., Zhou, Z.K., 2009. Phylogenetic studies of the core Alismatales inferred from morphology and rbcL sequences. Prog. Nat. Sci. 19, 931–945. Lindqvist, C., De Laet, J., Haynes, R.R., Aagesen, L., Keener, B.R., Albert, V.A., 2006. Molecular phylogenetics of an aquatic plant lineage, Potamogetonaceae. Cladistics 22, 568–588. Magallon, S., Castillo, A., 2009. Angiosperm diversification through time. Am. J. Bot. 96, 349–365. Marincovich, L., Gladenkov, A.Y., 1999. Evidence for an early opening of the Bering Strait. Nature 397, 149–151. Miki, S., 1937. The origin of Najas and Potamogeton. Bot. Mag. 51, 472–481. Mukai, H., 1993. Biogeography of the tropical seagrasses in the Western Pacific. Mar. Freshw. Res. 44, 1–17. Nauheimer, L., Metzler, D., Renner, S.S., 2012. Global history of the ancient monocot family Araceae inferred with models accounting for past continental positions and previous ranges based on fossils. New Phytol. 195, 938–950. Nylander, J.A.A. (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. Petersen, G., Seberg, O., Davis, J.I., Stevenson, D.W., 2006. RNA editing and phylogenetic reconstruction in two monocot mitochondrial genes. Taxon 55, 871–886. Ronquist, F., Huelsenbeck, J.P., 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574. Stevens, P.F., 2012. Angiosperm Phylogeny Website. Version 12. (accessed December 2012).
By Saravanan K at 2:36 pm, Feb 01, 2013
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Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev
Short Communication
Eurasian origin of Alismatidae inferred from statistical dispersal–vicariance analysis Ling-Yun Chen a,b, Jin-Ming Chen a,b, Robert Wahiti Gituru c, Qing-Feng Wang a,b,⇑ a
Key Laboratory of Aquatic Botany and Watershed Ecology, The Chinese Academy of Sciences, Wuhan 430074, Hubei, PR China Wuhan Botanical Garden, The Chinese Academy of Sciences, Wuhan 430074, Hubei, PR China c Botany Department, Jomo Kenyatta University of Agriculture and Technology, P.O. Box 62000-00200, Nairobi, Kenya b
a r t i c l e
i n f o
Article history: Received 7 July 2012 Revised 26 December 2012 Accepted 4 January 2013 Available online 16 January 2013 Keywords: Alismatidae Phylogeny Biogeography Dispersal
a b s t r a c t Alismatidae is a wetland or aquatic herb lineage of monocots with a cosmopolitan distribution. Although considerable progress in systematics and biogeography has been made in the past several decades, geographical origin of this group remains unresolved. In this study, we used statistical dispersal–vicariance analysis implemented in program RASP to investigate the biogeography of Alismatidae. Six areas of endemism were used to describe the distribution: North America, South America, Eurasia, Africa, Southeast Asia and Australia. 18,000 trees retained from Bayesian inference of rbcL served as a framework to reconstruct the ancestral areas. The results suggested that the most recent common ancestor of Alismatidae most probably occurred in Eurasia, followed by a split into two major clades. The clade comprising Hydrocharitaceae, Butomaceae and Alismataceae mainly diversified in Eurasia and Africa. The other clade comprising the remaining families dispersed to southern hemisphere. Australia played an important role in diversification of this clade. Several families were suggested to have occurred in Australia, such as Ruppiaceae, Cymodoceaceae, Posidoniaceae and Zosteraceae. Ó 2013 Elsevier Inc. All rights reserved.
1. Introduction Alismatidae is a monocot group with a worldwide distribution. The group is imbedded within the order Alismatales, which includes two other families, Araceae and Tofieldiaceae (Stevens, 2012). According to Les et al. (1997), the group consists of 14 families, 57 genera and about 500 species. However, as currently circumscribed, Alismatidae consists of 12 families (Stevens, 2012) and 56 genera, in which, Limnocharitaceae was merged into Alismataceae (Stevens, 2012; Chen et al., 2012a), Lilaeaceae was merged into Juncaginaceae (Stevens, 2012), Zannichelliaceae was merged into Potamogetonaceae (Stevens, 2012), Maundia was treated as a separate family Maundiaceae (von Mering and Kadereit, 2010) and Maidenia was merged into Vallisneria (Les et al., 2008). All marine angiosperms and most water-pollinated angiosperms are taxonomically confined to this group (Cook, 1990; Les et al., 1997). Members of Alismatidae are wetland or aquatic herbs. Additionally, most of the members have a completely submerged seedling phase, and flowers could either be floating or emergent. Vegetation may be totally submerged, with the leaves floating, or protruding from water (Chen et al., 2004). In the past several years, there has been a substantial improvement of our knowledge on the evolution of monocots. Presently, Alismatidae is largely considered as one of the most ancient groups ⇑ Corresponding author at: Wuhan Botanical Garden, The Chinese Academy of Sciences, Wuhan 430074, Hubei, PR China. Fax: +86 27 87510526. E-mail address: [email protected] (Q.-F. Wang). 1055-7903/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2013.01.001
of monocots (e.g. Tamura et al., 2004). The first phylogeny of Alismatidae with comprehensive samples was proposed by Les et al. (1997) based on rbcL. Les et al. (1997) divided Alismatidae into two major groups. One group consists of Alismataceae, Butomaceae and Hydrocharitaceae, while the other consists of the remaining families. Several studies based on rbcL (Chen et al., 2004; von Mering and Kadereit, 2010) and combined rbcL and morphological data (Li and Zhou, 2009) also supported the result of Les et al. (1997). The interfamilial relationships within Alismatidae inferred from mitochondrial genes (Petersen et al., 2006; Cuenca et al., 2010) were generally congruent with those based on rbcL data except for the position of Alismataceae. Therefore, the phylogeny of Alismatidae inferred from rbcL was widely accepted by researchers. Great progress has been made in the last decade in the estimation of divergence times of Alismatidae. Les et al. (2003) used molecular data to estimate the divergence times for some closely related taxa within Alismatidae. The study suggested that the genus level divergence occurred in the Eocene and Oligocene. Based on the analysis using rbcL and fossil calibration points, Janssen and Bremer (2004) proposed that Alismatidae originated around 108 Ma, which is similar to the result by Magallon and Castillo (2009). In addition, the ages of the major lineages within Alismatidae were also estimated by Janssen and Bremer (2004), although they may be affected by a comparatively limited taxon sampling. Recently, we presented the dated phylogenies of Alismataceae and Hydrocharitaceae, which suggested Late Cretaceous or Paleocene origin times of the two families (Chen et al., 2012a,
L.-Y. Chen et al. / Molecular Phylogenetics and Evolution 67 (2013) 38–42
2012b). The above-mentioned divergence times of Alismatidae provided us with a solid basis for understanding the historical biogeography of the group. However, the geographical origin of Alismatidae remains unresolved. Lindqvist et al. (2006) thought that aquatic angiosperms, in general, have a wider distribution than their terrestrial relatives. This remarkably wide distribution has in itself become a challenge in pinpointing geographic origins for aquatic angiosperms. Alismatidae is no exception, although several biogeographic studies related to this group have been reported. Bremer and Janssen (2006) had suggested a Gondwanan origin of the major monocot groups based on a dispersal–vicariance analysis with 79 of the 81 monocot families. However, the study failed to resolve the geographic origin of Alismatales and Alismatidae due to a high number of possible area combinations suggested in the analysis. This may be attributed to their use of families rather than genera or species as terminal taxa in the dispersal–vicariance analysis. The geographical origin of several genera within Alismatidae is still a subject of debate. For example, Miki (1937) and Les (1983) considered East Asia as the area of origin of Potamogeton, based on fossil records and chromosome number. However, the opinion was challenged by Lindqvist et al. (2006) who argued Potamogeton originated in North America. With respect to the transoceanic distributions of organisms, two competing processes have been proposed: vicariance and dispersal. It is interesting to investigate which process was mainly responsible for the transoceanic distribution pattern of Alismatidae. To address the geographical origin of Alismatidae, this paper aims to reconstruct the possible ancestral ranges of Alismatidae using statistical dispersal–vicariance analysis (S-DIVA). Combined with the available information of divergence times of the group (Les et al., 2003; Janssen and Bremer, 2004; Chen et al., 2012a, 2012b), we try to obtain a hypothesis explaining its biogeographical history.
39
ally, and all gaps were treated as missing. The gene after manual edit was 1191 bp in length, starting at 30 bp downstream of the start site, and ending at 226 bp upstream of the end site (Data 1, Supplementary). 2.2. Biogeograhical analysis The recently developed statistical dispersal–vicariance analysis (S-DIVA) implemented in RASP (Yu et al., 2012) was used to reconstruct the possible ancestral ranges of Alismatidae on phylogenetic trees. In S-DIVA, the frequencies of an ancestral range at a node in ancestral reconstructions are averaged over all trees. To account for phylogenetic uncertainty, we inferred the distributions by integrating 18,000 trees from Bayesian MCMC analysis. The Bayesian trees were generated using MrBayes v3.1.2 (Ronquist and Huelsenbeck, 2003) with rbcL, run for 10,000,000 generations, sampled every 1000 generations. GTR + I + G was selected as the best-fit model of DNA substitution with the Akaike Information Criterion (AIC) in MrModeltest v2.3 (Nylander, 2004). The first 10% generations were discarded. The remaining 18,000 trees (9000 2) (Data 2, Supplementary) were used for computing Condense Tree and SDIVA in RASP. We defined the geological criterion according to Bremer and Janssen (2006), and palaeogeographical history (i.e. plate tectonics). In all, six geographical areas were used to describe the distribution of Alismatidae and outgroup taxa: A, North America; B, South America; C, Eurasia; D, Africa; E, Southeast Asia; F, Australia (Fig. 1a). We used genera as terminal taxa. Each genus was coded based on its current distribution, which was mainly compiled from literatures (e.g. Cook, 1990; von Mering and Kadereit, 2010; Azuma and Tobe, 2011). The distribution data was presented (Data 3, Supplementary). The number of maximum areas at each node was setted as 4. Divergence times of Alismatidae was cited from Chen et al. (2012a, 2012b) and Janssen and Bremer (2004).
2. Materials and methods 2.1. Taxa sampling and sequence alignment Fifty-two terminals representing 52 genera in 12 families of Alismatidae were selected. Eighteen genera were chosen as outgroup taxa. Tofieldiaceae (Alismatales) and Araceae (Alismatales) are the closest relatives of Alismatidae (Tamura et al., 2004). All genera of Tofieldiaceae (viz. Tofieldia, Pleea, Harperocallis, Isidrogalvia, Triantha) were selected as outgroup taxa. Based on molecular phylogenetic analyses, Araceae, which includes 117 genera (Nauheimer et al., 2012), was separated into ten major groups (Cabrera et al., 2008). Therefore, one genus for each group was selected as outgroup taxa. Petrosaviales (Petrosaviaceae), which includes two genera (viz. Japonolirion and Petrosavia), is a sister to Alismatales (Tamura et al., 2004). The two genera were chosen as outgroups. In addition, Acorus, the lone genus in Acoraceae (Acorales), was also selected as an outgroup following the methodology in Les et al. (1997). Prior to present study, large numbers of rbcL sequences for Alismatid plants except three genera (viz. Appertiella, Althenia and Pseudalthenia) have been reported. Therefore, all the rbcL sequences used in our analyses, except Butomopsis latifolia, were obtained from GenBank (Table A1, Supplementary). In order to improve the credibility of sequences, the sequences generated by Les et al. (1993, 1997) and our lab were preferentially selected. The rbcL of B. latifolia was amplified according to methodology in Chen et al. (2012a). Purified PCR product was ligated to pMD18-T vector (Takara Biotech Co., Dalian, China), and six positive clones were sequenced. The newly generated sequence was submitted to GenBank (Table A1, Supplementary). Sequences were aligned using Clustal X v2.0 (Thompson et al., 1997) with default parameters. The output was inspected manu-
3. Results The Condense Tree retained from computing the Bayesian MCMC trees divided Alismatidae into two major clades (Fig. 1b). (1) Clade A consists of Alismataceae, Butomaceae and Hydrocharitaceae. Alismataceae was divided into two major suclades. Limnocharis, Hydrocleys and Butomopsis were nested within Alismataceae, and Butomaceae clustered together with it. (2) Clade B consists of the remaining nine families of Alismatidae. From the S-DIVA, it could be inferred that the most recent common ancestor (MRCA) of Alismatidae occurred in Eurasia with a relative probability of 84% (Fig. 1b, Table 1). The result shows that a Eurasian origin for the two major clades (Clade A (probability 90%) and B (probability 69%)), Hydrocharitaceae (probability 86%), subclade Alismataceae + Butomaceae (probability 86%) is most likely. In addition, the clade formed by Alismatidae, Araceae and Tofieldiaceae (excluding Isidrogalvia) share a common ancestor whose ancestral distribution area is Eurasia (probability 100%). Clade B suggested a widespread occurrence in Australia (Fig. 1b), pointing to an Australian origin for some families of this clade, e.g. Zosteraceae, Cymodoceaceae. The possible ancestral ranges of Juncaginaceae were suggested to be South America (a probability of 33%), South America and Australia (probability 33%), Americas and Australia (probability 33%).
4. Discussion Alismatidae was divided into two major clades in our analysis. The interfamilial relationships of the group were generally similar
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L.-Y. Chen et al. / Molecular Phylogenetics and Evolution 67 (2013) 38–42
(c)
(b)
5
4 1
Tertiary
2
3
D
Limnophyton sp. (DEF) Wiesneria triandra (DE) Sagittaria latifolia (ABCDE) BD ABD 23 Echinodorus grandiflorus (AB) Caldesia parnassifolia (CDEF) 5 D D Burnatia enneandra (D) Alisma plantago-aquatica (ACD) C C 8 Baldellia ranunculoides (C) Alismataceae C Damasonium alisma (ACDEF) CD Luronium natans (C) Hydrocleys nymphoides (BCDE) 7C C Butomopsis latifolia (DEF) BC Limnocharis flava (BCDE) B Ranalisma rostratum (CDE) Butomus umbellatus (CDE) Butomaceae Vallisneria natans (ABCDEF) C E Nechamandra alternifolia (E) C Hydrilla verticillata (CE) CE E E Enhalus acoroides (CDEF) 6 E CE Thalassia hemprichii (BCDEF) C Halophila engelmannii (ABCDEF) CE CE C C E C Najas marina (ABCDEF) Hydrocharitaceae C AB Stratiotes aloides (C) CD Egeria densa (B) B Elodea nuttallii (A) CDE C Apalanthe granatensis (B) D C Ottelia alismoides (BCDEF) 9 BC Blyxa aubertii (CDEF) BCD C Lagarosiphon muscoides (D) Hydrocharis morsus-ranae (CDEF) Limnobium spongia (AB) Ruppia megacarpa (ABCDEF) Ruppiaceae 20 F Syringodium filiforme (BCEF) F Cymodocea serrulata (CEF) 21 Cymodoceaceae F 19 Amphibolis antarctica (F) F F Thalassodendron pachyrhizum (DEF) Posidonia oceanica (CEF) Posidoniaceae 22 F Halodule beaudettei (ABCDEF) Cymodoceaceae 15 Phyllospadix torreyi (ABCEF) F 17 F Heterozostera tasmanica (F) Zosteraceae F Zostera marina (ABCDEF) 16 F Potamogeton crispus (ABCDEF) 14 F Coleogeton pectinatus (ABCDEF) F F Lepilaena australis (F) 18 F Zannichellia palustris (ABCDEF) Potamogetonaceae BF CF EF DF Groenlandia densa (CDE) 12 F Maundia triglochinoides (F) Maundiaceae Lilaea scilloides (AB) B 11 Triglochin maritimum (ABCDF) AF F Juncaginaceae 13 Cycnogeton procerum (F) BF BF ACF 10 ABF Tetroncium magellanicum (B) Scheuchzeria palustris (AC) Scheuchzeriaceae C Aponogeton elongatus (CDEF) Aponogetonaceae C Tofieldia glutinosa (AC) C Triantha japonica (AC) Tofieldiaceae C Harperocallis flava (C) (Alismatales) Pleea tenuifolia (C) Lysichiton americanus (AC) CF ACF Gymnostachys anceps (F) Callopsis volkensii (D) DE Podolasia stipitata (E) Stenospermation ulei (B) Araceae BDF Pothoidium lobbianum (CE) (Alismatales) E C Stylochaeton bogneri (D) CD CDE Calla palustris (AC) CE Pseudodracontium lacourii (E) BC Spirodela polyrrhiza (ABCDEF) BC C BC Isidrogalvia schomburgkiana (B) Tofieldiaceae (Alismatales) Petrosavia sakuraii (CE) BCE Japonolirion osense (C) Petrosaviaceae (Petrosaviales) C Acorus tatarinowii (ACE) Acoraceae (Acorales) AD
D
Clade A
Ancestral area of Alismatidae Major dispersal routes
(a)
C
5
4C
3C
1 ACE
C
BC
ABCE
Outgroup
2
Clade B
Undefined A North America B South America C Eurasia D Africa E Southeast Asia F Australia
Fig. 1. Biogeography of Alismatidae. (a) Area delimitation in biogeographic analysis; distribution of each genus is indicated along with species name. (b) Reconstruction of ancestral distributions of Alismatidae using statistical dispersal–vicariance analysis in RASP. The pie charts represent the relative probability of ancestral areas reconstructed for each node. The area(s) with highest probability are also marked with letters. (c) Ancestral area of Alismatidae and the five main possible dispersal routes.
to those based on rbcL in previous studies (Les et al., 1997; Chen et al., 2004; von Mering and Kadereit, 2010). Our biogeographical analysis suggested that the MRCA of Alismatidae most probably originated in Eurasia. Previous studies proposed that Alismatidae originated around 108 Ma (Janssen and Bremer, 2004), with all the families presented in the Late Creta-
ceous and early Tertiary periods (Les et al., 2003; Janssen and Bremer, 2004; Chen et al., 2012a, 2012b). The breakup of Pangaea occurred during 230–148 Ma (Labails and Roest, 2010), resulting in Gondwana and Laurasia. The modern continents viz. South America, Africa, Eurasia, Australia and North America have been separated by oceans since at least ca. 105 Ma (Davis et al., 2002).
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Table 1 Results of biogeographic analysis of Alismatidae. The first three area(s) with highest probability for major nodes of Alismatidae under S-DIVA are shown (separated by a slash). The mean ages for some nodes are presented, cited from (1) Janssen and Bremer (2004); (2) Chen et al. (2012a); (3) Chen et al. (2012b). Node
S-DIVA
Age (Ma)
Node
S-DIVA
Age (Ma)
1 2 3 4 5 6 7 8 9 10 11
ACE (0.82)/ABCE (0.18) C (0.82)/BC (0.18) C (1.00) C (1.00) C (0.84)/CD (0.09) C (0.90)/CD (0.09) C (0.86)/CDE (0.06)/CD/(0.06) CD (0.64)/BCD (0.10)/BC (0.06) C (0.86)/CDE (0.06) C (0.69)/CF (0.14)/ACF (0.09) ACF (0.17)/CF (0.17)/BC (0.16)
– – – – Ca. Ca. – Ca. Ca. Ca. Ca.
12 13 14 15 16 17 18 19 20 21 22
F (0.50)/BF (0.50) ABF (0.33)/BF (0.33)/B (0.33) F (1.00) F (1.00) F (1.00) F (1.00) CF (0.15)/DF (0.15)/EF (0.15) F (1.00) F (1.00) F (1.00) F (1.00)
Ca. Ca. Ca. – Ca. Ca. – – – –
1081 951 792 663 98 1 92 1
Therefore, the transoceanic distribution of Alismatidae among the modern continents might be resulted from dispersals involving land bridges, island chains or long-distance dispersal. The MRCAs of the two major clades were also suggested to have occurred in Eurasia (Fig. 1b). For clade A, Hydrocharitaceae was found to have originated in Eurasia (probability 86%), a result similar to Chen et al. (2012b) which suggested the family originated in Asia. Alismataceae and the clade (Alismataceae + Butomaceae) were suggested to occur most probably in Eurasia. Alismataceae split into two major clades, mainly diversified in Eurasia and Africa separately (Fig. 1b). Dispersal of Alismataceae plants from Eurasia to Africa might have occurred (Fig. 1b, node 7 ? 23; Fig. 1c, arrow 1). For example, the clade (Limnophyton (Wiesneria + Sagittaria)) diversified in Africa, and radiated into South America, Asia, Australia, etc. (detailedly discussed in Chen et al. (2012a)). For clade B, the early plants have dispersed from Eurasia to Australia (Fig. 1b, node 10 ? 14; Fig. 1c, arrow 2), consistent with the viewpoint that biota exchanges between southern Asia and Australia during the Tertiary existed, via the Ninetyeast Ridge (Cruaud et al., 2011), Malay Archipelago (van Welzen et al., 2005) or transoceanic dispersals. Clade B mainly diversified in Australia (Fig. 1b, node 14). From Australia, the plants dispersed to all over the world. The dispersal from Eurasia to Africa and Australia also occurred in Hydrocharitaceae and Alismataceae plants (Chen et al., 2012a, 2012b), e.g., Vallisneria. In addition, other three major dispersal routes involving in the world widely distribution of Alismatidae: (1) Transoceanic dispersal from Africa to South America during the Late Cretaceous and Tertiary periods (Fig. 1c, arrow 3). For example, Ottelia and Sagittaria were proposed to have dispersed from Africa to South America in the Tertiary (Chen et al., 2012a, 2012b). In South America, some Alismatid plants diversified and radiated into North America, e.g., Echinodorus (Chen et al., 2012a). (2) Dispersal from Europe to North America via the North Atlantic Land Bridge (NALB) (Fig. 1c, arrow 4), which connected western Europe and eastern North America from the early Paleocene to the Late Miocene (Denk et al., 2010). (3) Dispersal from eastern Asia to North America, via the Bering Land Bridge (BLB) (Fig. 1c, arrow 5), which connected western North America and eastern Asia from at least the early Paleocene until 7.4–4.8 Ma (Marincovich and Gladenkov, 1999). For example, the clade comprises Luronium, Alisma, Baldellia and Damasonium was inferred to have occurred in Eurasia, and radiated into North America, via the NALB and BLB (Fig. 1b). Moreover, ocean currents have played an important role in the widespread distribution of Alismatidae, especially the seagrasses (Brasier, 1975). Mukai (1993) proposed that the Kuroshio Current taken seagrasses such as Thalassia and Halophila from the equator to the Nansei Islands. Aponogetonaceae comprises one genus Aponogeton, with approximate 50 species that are mainly distributed in tropical or subtropical regions of the Old World (Les et al., 2005). Les et al. (2005) proposed that Aponogeton originated and diversified in Aus-
821 521 751 471 171
tralia. Our biogeographic anlaysis suggested that early plants of Alismatidae have dispersed from southern Asia to Australia. Therefore, the ancestor of Aponogeton would be from Eurasia. On the other hand, Aponogeton is widely distributed in India, Southeast Asia and Africa. The plants might have dispersed from Australia to these areas (Les et al., 2005). However, divergence times of the family are not well resolved. Further studies are required to resolve this problem. The seagrass families Posidoniaceae, Cymodoceaceae, Zosteraceae and Ruppiaceae are suggested to have originated from Australia. Les et al. (1997) and Kato et al. (2003) proposed that seagrasses had independently arisen from their fresh water relatives in the course of habitat alteration from fresh to salty waters. This viewpoint supported the Australian origin, because the dispersal event from southern Asia to Australia (across the ocean systems of the western Pacific) presented the habitat changes from fresh to salty water crucial for seagrass development. Mukai (1993) proposed that the coastal waters of Malesia enclosed by Indonesia, Borneo, Papua New Guinea and Torres Strait (northern Australia) were the centers of origin for the seagrass species in the western Pacific. His viewpoint contradicts with our finding that seargrasses might have originated from Australia. This is probably due to the widespread distribution of seagrasses in coastal waters of Malesia and Australia. Eurasia, Africa, Southeast Asia and Australia (the Old World) were found to be the ancestral areas for the subclade formed by genera of Potamogetonaceae. In addition, Australia was found to be the ancestral area for the deep nodes within this subclade (Fig. 1b). The Old World origin of Potamogeton inferred from our analysis contradicts the suggestion that the genus originated in North America (Lindqvist et al., 2006). However, the result is supported by the fact that the most ancestral species of Potamogeton are endemic to Australia (Lindqvist et al., 2006), and also supported by Miki (1937) and Les (1983) who suggested that the genus originated in Asia. Therefore, Potamogeton might have originated in the Old World (mostly probably in Australia) and dispersed to North America. Janssen and Bremer (2004) estimated the stem node age of Potamogetonaceae to be 47 Ma. This age coincides with the existence of biotic exchanges between southern Asia and Australia, and the BLB, which facilitated biotic exchanges between Asia and North America from at least the early Paleocene until 7.4– 4.8 Ma. This study suggests that the MRCA of Alismatidae most probably originated in Eurasia. The clade comprises Hydrocharitaceae, Alismataceae and Butomaceae mainly diversified in Eurasia and Africa; the clade comprises other families would have dispersed to southern hemisphere and diversified in Australia and South America. Although our study has resolved the geographical origin of Alismatidae, biogeography for several families (e.g., Juncaginaceae, Zosteraceae) may suffer from underrepresentation in sampling. To thoroughly understand the origin and dispersal of
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Alismatidae, future studies should try to include comprehensive samples for underrepresented families. Acknowledgments We thank Can Dai for revising this manuscript. We thank Kuo Liao, Yong-Qing Zhu, Shu-Ying Zhao and Suman Neupane for their comments on this manuscript. We appreciate two anonymous reviewers for their valuable suggestions to improve the manuscript. We appreciate Susanne S. Renner for suggestion on the title of this manuscript. We appreciate Laszlo Csiba for providing the DNA samples of Butomopsis latifolia. This work was supported by grants from One Hundred Person Project of the Chinese Academy of Sciences (KSCX2-YW-Z-0805), National Natural Science Foundation of China (30970202) and Strategic Pilot Science and Technology Projects of the Chinese Academy of Sciences (XDAO5090305). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.ympev.2013.01.001. References Azuma, H., Tobe, H., 2011. Molecular phylogenetic analyses of Tofieldiaceae (Alismatales): family circumscription and intergeneric relationships. J. Plant. Res. 124, 349–357. Brasier, M.D., 1975. An outline history of seagrass communities. Palaeontology 18, 681–702. Bremer, K., Janssen, T., 2006. Gondwanan origin of major monocot groups inferred from dispersal–vicariance analysis. Aliso 22, 22–27. Cabrera, L.I., Salazar, G.A., Chase, M.W., Mayo, S.J., Bogner, J., Davila, P., 2008. Phylogenetic relationships of aroids and duckweeds (Araceae) inferred from coding and noncoding plastid DNA. Am. J. Bot. 95, 1153–1165. Chen, J.M., Robert, G.W., Wang, Q.F., 2004. Evolution of aquatic life-forms in Alismatidae: Phylogenetic estimation from chloroplast rbcL gene sequence data. Isr. J. Plant Sci. 52, 323–329. Chen, L.Y., Chen, J.M., Gituru, R.W., Temam, T.D., Wang, Q.F., 2012a. Generic phylogeny and historical biogeography of Alismataceae, inferred from multiple DNA sequences. Mol. Phylogenet. Evol. 63, 407–416. Chen, L.Y., Chen, J.M., Gituru, R.W., Wang, Q.F., 2012b. Generic phylogeny, historical biogeography and character evolution of the cosmopolitan aquatic plant family Hydrocharitaceae. BMC Evol. Biol. 12, 30. Cook, C.D.K., 1990. Aquatic Plant Book. SPB Academic Publishing, Hague. Cruaud, A., Jabbour-Zahab, R., Genson, G., Couloux, A., Peng, Y.Q., Rong, Y.D., Ubaidillah, R., Pereira, R.A.S., Kjellberg, F., van Noort, S., Kerdelhue, C., Rasplus, J.Y., 2011. Out of Australia and back again: the world-wide historical biogeography of non-pollinating fig wasps (Hymenoptera: Sycophaginae). J. Biogeogr. 38, 209–225. Cuenca, A., Petersen, G., Seberg, O., Davis, J.I., Stevenson, D.W., 2010. Are substitution rates and RNA editing correlated? BMC Evol. Biol. 10, 349. Davis, C.C., Bell, C.D., Mathews, S., Donoghue, M.J., 2002. Laurasian migration explains Gondwanan disjunctions: evidence from Malpighiaceae. Proc. Natl. Acad. Sci. USA 99, 6833–6837. Denk, T., Grimsson, F., Zetter, R., 2010. Episodic migration of oaks to Iceland: evidence for a North Atlantic ‘‘land bridge’’ in the latest Miocene. Am. J. Bot. 97, 276–287.
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