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Reconstructing the age and historical biogeography of the ancient flowering-plant family Hydatellaceae… Iles, William J D; Lee, Christopher; Sokoloff, Dmitry D; Remizowa, Margarita V; Yadav, Shrirang R; Barrett, Matthew D; Barrett, Russell L; Macfarlane, Terry D; Rudall, Paula J; Graham, Sean W May 13, 2014

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RESEARCH ARTICLE Open AccessReconstructing the age and historicalbiogeography of the ancient flowering-plantfamily Hydatellaceae (Nymphaeales)William J D Iles1,2*, Christopher Lee1, Dmitry D Sokoloff3, Margarita V Remizowa3, Shrirang R Yadav4,Matthew D Barrett5, Russell L Barrett5, Terry D Macfarlane6, Paula J Rudall7 and Sean W Graham1,2AbstractBackground: The aquatic flowering-plant family Hydatellaceae has a classic Gondwanan distribution, as it is foundin Australia, India and New Zealand. To shed light on the biogeographic history of this apparently ancient branchof angiosperm phylogeny, we dated the family in the context of other seed-plant divergences, and evaluated itsbiogeography using parsimony and likelihood methods. We also explicitly tested the effect of different extinctionrates on biogeographic inferences.Results: We infer that the stem lineage of Hydatellaceae originated in the Lower Cretaceous; in contrast, its crownoriginated much more recently, in the early Miocene, with the bulk of its diversification after the onset of thePliocene. Biogeographic reconstructions predict a mix of dispersal and vicariance events, but considerations ofgeological history preclude most vicariance events, besides a split at the root of the family between southern andnorthern clades. High extinction rates are plausible in the family, and when these are taken into account there isgreater uncertainty in biogeographic inferences.Conclusions: A stem origin for Hydatellaceae in the Lower Cretaceous is consistent with the initial appearance offossils attributed to its sister clade, the water lilies. In contrast, the crown clade is young, indicating that vicariantexplanations for species outside Australia are improbable. Although long-distance dispersal is likely the primarydriver of biogeographic distribution in Hydatellaceae, we infer that the recent drying out of central Australia dividedthe family into tropical vs. subtropical/temperate clades around the beginning of the Miocene.Keywords: Aquatic plants, Austral, Ephemeral habitats, Extinction rates, Intercontinental dispersal, ANITA-gradeangiosperms, Trithuria, VicarianceBackgroundAustralia has seen widespread rainforest replaced withdeserts, savannah and sclerophyll biomes since theEocene, in response to global cooling [1]. Despite the dra-matic loss of mesophytic habitat, it has a well-developedwetland flora, with many endemic species [2]. Perhaps themost unique of these habitats are ephemeral bodies ofwater that are home to communities characterized by ex-treme reduction in plant size, and annual or geophytic lifehistories [3,4]. Common Australian members of thisephemeral aquatic habitat include Centrolepidaceae(a family closely related to or possibly embeddedwithin the southern rushes [5], Restionaceae), the sun-dew genus Drosera L. (Droseraceae), and HydrocotyleL. (Araliaceae) [3,6], but its most noteworthy compo-nent may be the family Hydatellaceae [7]. Most mem-bers of Hydatellaceae exemplify the ephemeral aquaticsyndrome, apart from a recently derived pair of peren-nial apomictic species that live submerged in more per-manent bodies of water [8,9].Hydatellaceae were recently recognized as the sistergroup of the water lilies (Cabombaceae and Nym-phaeaceae), placing their divergence close to the root* Correspondence: will.jd.iles@gmail.com1Department of Botany, University of British Columbia, 3529-6270 UniversityBlvd, Vancouver, British Columbia, V6T 1Z4, Canada2UBC Botanical Garden & Centre for Plant Research, University of BritishColumbia, 6804 Marine Dr SW, Vancouver, British Columbia, V6T 1Z4, CanadaFull list of author information is available at the end of the article© 2014 Iles et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly credited. The Creative Commons Public DomainDedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,unless otherwise stated.Iles et al. BMC Evolutionary Biology 2014, 14:102http://www.biomedcentral.com/1471-2148/14/102of angiosperm phylogeny e.g., [10]. They have sinceattracted considerable attention because of the insightsthey may provide into the evolution of early angiosperms[11-16]. Of particular interest is the nature of the repro-ductive structures in the family, which may represent floral,prefloral, or pseudanthial arrangements of reproductiveorgans, and the incidence of unisexual and bisexual re-productive units. These may bear on our understand-ing of the ancestral floral Bauplan of angiosperms[8,9,13]. Contemporary taxonomic and phylogenetic workon the family recognizes one genus, Trithuria Hook. f., and12 species in four monophyletic sections [8,9].The distribution of the Southern Hemisphere biotahas been traditionally framed in terms of vicarianceevents resulting from the breakup of Gondwana [17].However, recent studies have suggested a more import-ant role for long-distance dispersal, especially in plants[17]. Within Australia, the constriction and fragmenta-tion of mesophytic and rainforest habitats since theEocene [1] have led to congruent patterns of vicariantspeciation across a number of plant lineages [18]. Hyda-tellaceae display a classic Gondwanan distribution, beingpresent in Australia, India and New Zealand (Figure 1;the distribution is based on online herbarium records[19] and new collection records), which may imply arelictual intercontinental distribution and great antiquityfor the crown clade [20]. While vicariant processesat both the hemispheric and continental scale couldexplain the extant distribution of Hydatellaceae, thisdistribution may also result from long-distance dispersal[9,17] (the wide and potentially trans-oceanic distribu-tion of many aquatic plant species is widely suspected tobe facilitated by the enhanced dispersal capabilities oftheir diaspores, often considered to be due to water-fowlvectors [21]). Evaluating these biogeographic hypothesesrequires placing geological and geographical events inthe context of dated phylogenies [22]. Most organismslack an extensive fossil record, and so molecular datinganalyses use age information from parts of the phyl-ogeny with a good fossil record to inform the age ofnodes that lack it [23].Since the recognition that Hydatellaceae represents anancient angiosperm lineage, a few fossils have been linkedwith it [7,24-26]. The most spectacular of these may be theaquatic plant Archaefructus, represented by whole fruitingplants from the Yixian Formation of Liaoning, China[27,28]. However, the timing and interpretation of theseand other records remains contentious [7,29]. Unlikethe fossil record of Hydatellaceae, water lilies have anextensive record that extends to the Lower Cretaceous1000 kmIndiaT. konkanensisT. austinensis, T. australis, T. bibracteata, T. occidentalis, T. submersa Wsouth-western Australiasouth-eastern AustraliaT. filamentosa, T. submersa ENew ZealandT. inconspicuanorthern AustraliaT. cookeana, T. cowieana, T. lanterna, T. polybracteataFigure 1 Global distribution of Hydatellaceae. The distribution is based on online herbarium resources [19] and new collection records; each collectionlocality is represented by a 120 km radial sweep. Five biogeographic areas are delineated by labelled ovals: India, New Zealand, northernAustralia, south-eastern Australia, and south-western Australia. Species found in each area are listed; note that Trithuria submersa is treatedhere as south-eastern and south-western species. We created the map using ArcMAP version 9.3 (Environmental Systems Research Institute,Redlands, CA, USA); the projection is Lambert’s cylindrical equal area.Iles et al. BMC Evolutionary Biology 2014, 14:102 Page 2 of 10http://www.biomedcentral.com/1471-2148/14/102[29-31]. Collectively these fossils suggest that aquaticniches were exploited early in the evolution of angio-sperms, although the aquatic life-form is unlikely to beancestral in flowering plants as a whole [32,33]. Nonethe-less, an improved understanding of the diversification ofHydatellaceae may help illuminate early angiospermecology and how plants colonize ephemeral wetlands,which represent a unique and potentially stressful en-vironment [4,34].To address these questions we dated the earliest splitsin Hydatellaceae using 17 plastid-genes sampled fromacross the seed plants, and used the resulting posteriorage distributions as secondary calibrations for a species-tree analysis of the entire family, which lacks suitablefossil calibrations. Although the use of secondary cali-bration points has been criticized for propagating “errorfree” values into downstream analyses [35], here we usethe entire posterior distribution from the seed-plant ana-lysis as a prior for the subsequent analysis, accountingfor the associated uncertainty [36]. We used the datedspecies tree to explore biogeographic hypotheses usingparsimony and likelihood. In particular, likelihood-basedapproaches allow the estimation of parameters such asspeciation rate. We also explicitly test the effect of ex-tinction rate on biogeographic reconstruction, as thismay be high in Hydatellaceae due to the patchy distribu-tion of their habitat in space and time [4,34] and is alsosuggested by the “broom-and-handle” shape of the phyl-ogeny [9,37-39].MethodsFossil selection and molecular datingFossils with unequivocal affinity to Hydatellaceae are un-known [7]. We therefore first estimated the crown-age ofthe family in a seed-plant analysis with 17 exemplar taxaconstrained by eight fossils (Table 1; see [24,40-52]). Weadded Trithuria cowieana D.D. Sokoloff, Remizowa, T.D.Macfarl. & Rudall (Macfarlane & al. 4217, MW; [GenBank:JQ284074, JQ284187, JQ284224, KJ725347–KJ725349]) toan existing data set that included T. filamentosa Rodwayand T. submersa Hook. f. [10,53,54] as these three speciesdefine the deepest phylogenetic splits in Hydatellaceae [9].This seed-plant matrix includes three gymnosperms andmajor lineages of angiosperms [53]. Genomic samplingfocused on 13 single-copy plastid genes (comprising fourmulti-gene clusters, psbD–psbC, psbE–psbF–psbL–psbJ,psbB–psbT–psbN–psbH, and three single-gene regions,ndhF, rbcL, and atpB). Only protein-coding regionswere considered. Details of DNA extraction, amplifica-tion, sequencing, contig assembly and alignment aredescribed elsewhere [9,10,55,56]; for a list of accessionsand the alignment matrix, see Additional files 1 and 2,respectively.To test for and accommodate non-clocklike behaviourin the seed-plant data set we used the Bayesian randomlocal clocks (RLC) method [57]. This accommodates mo-lecular rate variation by allowing different sub-branches ofthe tree to have unique molecular clocks. Dornberg et al.[58] examined the performance of this method against themore widely used uncorrelated lognormal (UCLN) method[59] for real and simulated data sets that show highamounts of inter-clade rate variability, and found that theRLC model performed better in the presence of clade-specific rate shifts. This may be pertinent to angiospermstudies like ours, as there are known to be substantial shiftsin rates among major angiosperm clades that are associ-ated with changes in habit and life history [60]. In par-ticular, Hydatellaceae occupy a part of the tree wherethere were multiple shifts in habit (for example, Hyda-tellaceae are mostly herbaceous annuals, water liliesare mostly perennial herbs, Amborella Baill. and Aus-trobaileyales include shrubs, small trees and lianas).The method is implemented in BEAST version 1.6.1.We used a GTR + Γ model of sequence evolution, withdefault priors (or those suggested by http://code.goo-gle.com/p/beast-mcmc/wiki/ParameterPriors if notautomatically implemented). The BEAST analysis re-quires that each of the fossil calibrations have an asso-ciated prior. We used lognormal priors with 95% priorintervals of ~10–20% of the fossil age (Table 1),Table 1 Fossil calibrations for seed-plant phylogenyNode Calibration Fossil Age (Ma) Priors ReferencesA Crown seed plants Cordaites 315 316.0–367.5 (2, 1) [40,41]C Stem angiosperms Glossopterid, Gangamopteris McCoy 293.8 294.8–346.3 (2, 1) [24,40,42,43]G Stem Cabombaceae Pluricarpellatia peltata B. Mohr, Bernardes-de-Oliveira & D.W. Taylor 98.7* 99.1–118.0 (1, 1) [44,45]H Crown Nymphaeaceae Monetianthus mirus Friis, Pedersen, von Balthazar, Grimm & Crane 92.8* 93.2–112.1 (1, 1) [46,47]M Stem Trimeniaceae Unnamed seed 98.7 98.9–110.4 (0.5, 1) [48]N Stem eudicots Tricolpate pollen 124* 124.2–135.7 (0.5, 1) [49,50]O Stem Araceae Mayoa portugallica Friis, Pedersen & Crane 96.1* 96.5–115.4 (1, 1) [51]P Stem Platanaceae West Brothers platanoid and Sapindopsis Fontaine 92.8* 93.2–112.1 (1, 1) [52]‘Node’ refers to placement on phylogeny in Additional file 3. Fossil ages follow the references, except that some ages are modified following [49], indicated withan asterisk. Calibration priors are lognormal; the 95% prior interval is given, followed by the lognormal mean and standard deviation in parentheses.Iles et al. BMC Evolutionary Biology 2014, 14:102 Page 3 of 10http://www.biomedcentral.com/1471-2148/14/102consistent with some other studies, e.g., [61] (the RLCmethod is also more robust than the UCLN method tovariation in the width of the 95% prior interval [58]).We ran seven runs of 4.0 × 107 generations, and con-sidered four that converged on the same posterior andlikelihood scores after 10% burnin. The estimated samplesizes of run statistics (posterior, prior, likelihood, parameterestimates) were all over 200 when these runs were pooled.The seed-plant chronogram and a table of divergence timesis presented in Additional file 3, and the tree file is providedin Additional file 4. In all analyses we constrained Nym-phaeaceae s.s. (i.e., excluding Cabombaceae) to be mono-phyletic, consistent with molecular and morphologicalanalyses [62-64]. We also tested a constraint that forcesAmborella to be the sister group of all other angiosperms;this arrangement contrasts with a clade comprisingAmborella and Nymphaeales that we recovered in theRLC analysis, see below (these two alternative arrange-ments have been recovered in different studies, see [53],for example). We constrained cycads to be the sistergroup of angiosperms among extant seed plants, consistentwith some recent studies [24,42,43,54], but also exploredalternative gymnosperm sister groups to angiosperms(conifers alone, Ginkgo L. alone, or pairwise combinationsof conifers, cycads and Ginkgo), or used no outgroup con-straints. For these different constraint analyses we ran a sin-gle 4.0 × 107 generation replicate; they all indicated only aminimal effect on the two ages within Hydatellaceae (<1Myr difference; data not shown).To date the Hydatellaceae species tree we consideredthe data set of [9], which consists of two unlinked loci(four plastid regions and the nuclear ribosomal internaltranscribed spacer region, ITS) for all species exceptTrithuria occidentalis Benth. which was only sampledfor one plastid region. In all analyses T. submersa wasprovisionally considered to comprise separate eastern andwestern species, following [9]. The data were analysed with*BEAST, which estimates the species tree with a Bayesianimplementation of the multi-species coalescent [65]. Weused the settings outlined in [9], with the exception that weassigned the two Hydatellaceae posterior distributions de-termined from the RLC seed-plant analysis (see Additionalfile 3) as Gaussian priors for the corresponding splits in thespecies tree (i.e., the crown node of Hydatellaceae and thecrown node of the clade consisting of sect. Hydatella andsect. Trithuria). These priors were only applied to the plas-tid loci (for which there was outgroup data), using the root-ing of Hydatellaceae determined in the seed-plant analysis(see Additional file 3).Biogeographic reconstructionsWe reconstructed ancestral areas using three methods:maximum parsimony dispersal-vicariance (DIVA; [66]),maximum likelihood (ML) dispersal-extinction-cladogenesis(DEC; [67]), and ML ancestral-state reconstruction (ASR;cf. [68]). The DIVA and DEC methods allow the range ofextant species and internal nodes (ancestral species) toencompass multiple discrete areas, and identify dispersal,vicariance or area extinction events. When vicarianceevents predicted in these analyses could not be explainedby contemporaneous geographic division, we treated themas indicative of long-distance dispersal events. In contrast,ASR implicitly only considers dispersal/extinction, and re-stricts each species range and internal node to a single area.In all cases we used the species tree as the reference phyl-ogeny (Figure 2a) and considered the five major biogeo-graphic areas that define the range of Hydatellaceae: (1)India; (2) northern Australia; (3) New Zealand; (4) south-eastern Australia; (5) south-western Australia (Figure 1).We treated south-eastern Australia as one area, despite itbeing climatically variable, because species ranges there(Trithuria filamentosa and T. submersa) are essentiallycontiguous within Tasmania, and there is no evidence of astrong geographic barrier between them [8]. We usedRASP version 2.0 Beta [66,69] to perform the DIVA ana-lysis, and for DEC we used Lagrange version 20110117(http://www.reelab.net/lagrange/configurator/index; [67]).We constrained some of the area connectivities for theDEC analysis, following the advice of the Lagrange website,which we based on our understanding of niche profiles ofthe species (unpublished data) and the underlying phylo-genetic relationships. In particular, we constrained theconnectivity of India to northern Australia only, and ofNew Zealand to south-eastern Australia only. To makecomparisons more meaningful between methods we alsoconstrained the DIVA analysis in the same way. In addition,for the DEC analysis we considered all dispersal paths tohave the same rate (as the allowed distances are comparablein magnitude; ~1500–6500 km), so we set all values in thedispersal rate scaling matrix to 1.0 (i.e., all dispersal pathrates are multiplied by “1”). Simulation studies show thatarea extinction rates in Lagrange are strongly biased to-wards zero [67]; as an alternative we evaluated lineage(species) extinction rates [70] as a proxy for the area extinc-tion rate, the parameter used in our analyses (species ex-tinction can be thought to occur when all the areas thatencompass the species range go extinct, and may be anunderestimate of the area extinction rate). We used the Rpackage Diversitree version 0.7-2 [71,72] to evaluate extinc-tion and speciation rates on the Hydatellaceae species treealone, or on the species tree with the addition of oneoutgroup separated by 127 Myr (see below). Based on theresults of the extinction-speciation analysis we chose sixarea extinction rates (0.001, 0.01, 0.05, 0.1, 0.5, and 1.0Myr-1) spanning the range of lineage extinction rates toexplore the effect of different rates on biogeographic recon-structions. Dispersal rates were iteratively optimized inLagrange for each extinction rate.Iles et al. BMC Evolutionary Biology 2014, 14:102 Page 4 of 10http://www.biomedcentral.com/1471-2148/14/102The ASR analyses were performed with BayesTraitsversion 1.0 (www.evolution.rdg.ac.uk; [73]). We consid-ered three nested models which were evaluated usingthe corrected Akaike information criterion (AICc; [74]).The most complex model (hereafter the ‘full model’)assumed three separate symmetrical transition rates:between Australia and India or New Zealand (assumingtrans-oceanic dispersals to be equivalent), between south-western and south-eastern Australia (dispersals across theNullarbor Plain), and between northern Australia andsouth-western or south-eastern Australia (dispersals acrossthe arid zone). The simplest model (‘simple model’) consistsof a single rate between all the allowed transition rates inthe full model. The two-rate transition model has symmet-ric rates between Australia and India or New Zealand,contrasting with a separate rate for all transitions withinAustralia (‘continental model’). Root state frequencies wereset to empirical values.ResultsMolecular dating and diversificationHydatellaceae are estimated to have diverged from thewater lilies 126.7 Ma (120.6–133.2 Ma, 95% HPD), inthe Lower Cretaceous, with a crown clade age of 19.1 Ma(15.7–23.4 Ma, 95% HPD), in the early Miocene (seeAdditional file 3). The estimated multi-species coalescent(a)Miocene Pliocene Pleist.T. cookeanaT. cowieanaT. polybracteataT. konkanensisT. lanternaT. austinensisT. australisT. filamentosaT. inconspicuaT. occidentalisT. bibracteataT. submersa WT. submersa E(d)1.000.540.520.660.770.731.001.000.701.000.671.00south-western Australiasouth-eastern Australianorthern AustraliaIndia New ZealandMiocene Pliocene Pleist.T. cookeanaT. cowieanaT. polybracteataT. konkanensisT. lanternaT. austinensisT. australisT. filamentosaT. inconspicuaT. occidentalisT. bibracteataT. submersa WT. submersa E(b)T. cookeanaT. cowieanaT. polybracteataT. konkanensisT. lanternaT. austinensisT. australisT. filamentosaT. inconspicuaT. occidentalisT. bibracteataT. submersa WT. submersa E02.55.07.510.012.515.017.520.0(c) cookeanaT. cowieanaT. polybracteataT. konkanensisT. austinensisT. australisT. filamentosaT. inconspicuaT. occidentalisT. bibracteataT. submersa WT. submersa E123456789101112–59100100100939410010010098 T. lanternaFigure 2 Dated species tree and biogeographic inferences for Hydatellaceae. (a) Timing of divergences in Hydatellaceae inferred usinga multi-species coalescent analysis, based on four plastid genes and nuclear ITS regions, with prior dating estimates for the first two nodes derived from aseparate seed-plant analysis (see Additional file 3; labelled nodes are referred to in Additional file 5). Numbers beside branches are support values (posteriorprobabilities expressed as percentages); dashes indicate <50% support. Divergence time uncertainty is noted by blue bars, representing 95% HPD. The timescale is in Ma. Letters adjacent to tips represent: E = east, T. =Trithuria, W =west. Historical biogeography inferred in (b) with the full model of MLancestral-state reconstruction, in (c) with MP based dispersal-vicariance analysis, and in (d) with ML based dispersal-extinction cladogenesis analysis.Pie fractions in (b) represent relative likelihoods; in (c) and (d) they represent joint areas where the species is inferred to have existed in multiple areas.The relative likelihood of the best geographic range pair is shown in (d) adjacent to individual nodes.Iles et al. BMC Evolutionary Biology 2014, 14:102 Page 5 of 10http://www.biomedcentral.com/1471-2148/14/102age for the crown of Hydatellaceae is 17.6 Ma (14.7–20.6 Ma, 95% HPD), in the early Miocene, with most di-versification occurring after ~6 Ma, in the late Miocene(Figure 2a; see Additional file 5 for a table of divergencetimes, and Additional file 6 for the tree file). For thespeciation-extinction analysis we estimated a speciationrate of 0.430 Myr-1 (0.107–0.881 Myr-1; 95% HPD) and alineage extinction rate of 0.446 Myr-1 (0.003–0.955 Myr-1;95% HPD). Including a distantly related outgroup did notsubstantially change speciation or extinction parameterestimates (data not shown).Biogeographic reconstructionsThe full ASR model had the best AICc score (Figure 2b;differences between best and alternative models: simpleΔ = 1.06; continental Δ = 2.135). It shows a split betweenthe tropical (northern Australia and India) and subtrop-ical/temperate (south western Australia, south easternAustralia, and New Zealand) clades (Figure 2b). Withinthe tropical clade we infer that the Indian species,Trithuria konkanensis S.R. Yadav & Janarth, represents arelatively recent long-distance dispersal event fromnorthern Australia (Figure 2b). Within the subtropical/temperate clade, the New Zealand species T. inconspicuarepresents a long-distance dispersal event from south-eastern Australia. There is no significant support for aparticular direction of dispersal between south-westernand south-eastern Australia (Figure 2b).The DIVA analysis reconstructed several vicarianceevents across the phylogeny (Figure 2c). There is an in-ferred vicariance event at the root of the family, betweenthe tropical and subtropical/temperate clades (Figure 2c).An additional one was predicted between northernAustralia and India in the tropical clade, and in thesubtropical/temperate clade two more were predictedbetween south-western Australia and south-easternAustralia, and one between south-eastern Australiaand New Zealand (Figure 2c). The DEC analysis recoveredsimilar patterns of vicariance across Hydatellaceae, al-though it also inferred dispersals, for example fromsouth-eastern Australia to New Zealand (Figure 2d). Inboth analyses, vicariance is implausible in the contextof dating analyses, except for the one involving theroot split between the tropical and subtropical/temper-ate clade. Increasing the extinction rate in the DECanalysis served to depress confidence in the estimatedancestral ranges for all nodes, considering both therelative likelihood of the best reconstructed range pair(Figure 3) and the relative likelihood of the individualranges at nodes (Figure 4).DiscussionThe phylogenetic origin of Hydatellaceae near the rootof angiosperm phylogeny [10] and lack of reliable fossils[7] make consideration of the family age infeasibleoutside the context of angiosperm divergence times.Unfortunately the crown age and subsequent timing ofdiversification of angiosperms remains one of the mostvexing questions in evolutionary biology, with some mo-lecular estimates [42,49,61] substantially older (~100 Myr)than the oldest reported crown angiosperm fossils [29].Our estimated age of 158.7 Ma (151.0–167.7 Ma, 95%HPD; see Additional file 3) is more in-line with less ex-treme results reported elsewhere [75,76]. A stem age forHydatellaceae of ~127 Ma (see Results and Additionalfile 3) suggests that stem lineage Hydatellaceae werecolonizing aquatic environments in the Lower Cretaceous,although when Hydatellaceae acquired the unique suite oftraits suited for ephemeral aquatic habitats is unclear.A crown age for Hydatellaceae in the early Miocene(~18 Ma, see Figure 2a and Additional file 5) indicates0.000.250.500.751.000.00 0.25 0.50 0.75 1.00Extinction rateRelative likelihoodNode 1Node 2Node 3Node 4Node 5Node 6Node 7Node 8Node 9Node 10Node 11Node 12Figure 3 Relationship between area extinction rate and relativelikelihood of range pairs in the dispersal-extinction-cladogenesis(DEC) analysis. The plot depicts the value of the range pair with thelargest relative likelihood at each node and extinction rate; notethat the top pair of ranges is not necessarily consistent acrossextinction rates. The ‘zero’ extinction value is the auto-optimizedestimate (4.285 × 10-9 Myr-1). Node numbers correspond to those inFigure 2a.Iles et al. BMC Evolutionary Biology 2014, 14:102 Page 6 of 10http://www.biomedcentral.com/1471-2148/14/102that a proposed Gondwanan explanation for the currentintercontinental distribution [20] is incorrect, as it wouldrequire that the Indian and north Australian species pairTrithuria konkanensis and T. lanterna diverged ~125Ma, according to the timing of the breakup of EastGondwana [77], instead of the estimated divergencetime of 0.76 Ma (0.24–1.33 Ma, 95% HPD; see Figure 2aand Additional file 5). This highlights the importanceof assessing proposed vicariant patterns with a carefulconsideration of phylogeny, geology, and estimated di-vergence times [22].Within Australia, climate driven vicariance events aremore plausible, although here as well, the last submer-sion of the Nullarbor Plain (~15 Ma), which separatesExtinction rateCumalitive relative likelihood1 to 2 1 to 310 to 1110 to T. occidentalis11 to 1211 to T. bibracteata 12 to T. submersa E12 to T. submersa W2 to 102 to 73 to 4 3 to 5 4 to T. cookeana 4 to T. cowieana5 to 65 to T. polybracteata 6 to T. konkanensis 6 to T. lanterna7 to 87 to T. austinensis00.0010.010.05 0.1 0.5 1.08 to 98 to T. australis9 to T. filamentosa 9 to T. inconspicuaSEAIndia MissingNA SWANew Zealand00.0010.010.05 0.1 0.5 1.0 00.0010.010.05 0.1 0.5 1.0 00.0010.010.05 0.1 0.5 1.0Figure 4 Relationship between extinction rate and relative likelihood of geographic ranges in each descendant lineage of a range-pairin the dispersal-extinction-cladogenesis (DEC) analysis. The likelihoods sum to unity in each bar; subdivisions represent the relative likelihoodof each range. Hashed ranges comprise more than one area. NA, northern Australia; SEA, south-eastern Australia; SWA, south-western Australia.The ‘zero’ extinction rate is the auto-optimized estimate (4.285 × 10-9 Myr-1). Node numbers correspond to those in Figure 2a; the range pairdepicted in Figure 2d reports the best pair descending from each node (e.g., node 1 to 2 and 1 to 3) at the auto-optimized rate.Iles et al. BMC Evolutionary Biology 2014, 14:102 Page 7 of 10http://www.biomedcentral.com/1471-2148/14/102the south-eastern and south-western regions, substan-tially predated the relevant phylogenetic splits (Figure 2a;[18]). However, the DIVA and DEC analyses indicate acontinent-scale vicariance event at the root of extantHydatellaceae (Figure 2c,d). The interior of Australiawas still relatively wet in the early Miocene (up to themid-Miocene), and although there were permanentlakes, there was also a marked dry season, indicating thepotential for ephemeral aquatic habitats [1]. The contin-ued aridification of central Australia presumably led tothis vicariance event. Our analyses therefore support aminimum of four long-distance dispersal events inHydatellaceae (Australia to India, Australia to New Zea-land, and two instances from south-western to south-eastern Australia; Figure 2). The inferred long-distancedispersal events likely involved selfers or apomicts, con-sistent with Baker's Law [78]. The New Zealand speciesTrithuria inconspicua and its Tasmanian sister species T.filamentosa are both thought to be perennial apomicts[79,80]; selfing is thought to characterize the Indian T.konkanensis and its sister species, T. lanterna, in north-ern Australia [8,81]. Baker’s Law has been extended todispersal in general, not just islands, and as a result weexpect selfing taxa to have wider distributions than out-crossing ones [82]. This seems to be the case in Hydatel-laceae, where dioecious species are generally much morelimited in distribution than related cosexual species [8].Statistical biogeographic methods such as DEC allownot only an examination of the biogeographic history ofa clade and an estimate of the processes involved in pro-ducing that history (dispersal, vicariance and extinction),but also quantification of how confident we are in thesereconstructions, via consideration of (relative) likelihoods.A strong bias towards estimating zero area extinction ratesmay occur in the DEC framework, both for real and simu-lated data sets [67]. We examined the effect that this mayhave on our reconstructions by manually varying the ex-tinction rate based on the range of values seen in ourspeciation-extinction analysis (see Results). Our confidencein reconstructing both (a) range pairs (thereby indicatingpossible processes such as vicariance or dispersal; Figure 3),and (b) each individual descendent lineage’s range (as indi-cated by the relative likelihoods for each range across allpossible range pairs; Figure 4), is compromised at higherrates. For the estimated extinction rate based on tree shape(~0.5 Myr-1), there is very little confidence in any particularrange pair (relative likelihoods are <0.6, Figure 3), and inthe ranges of individual descendent lineages, besides a fewof the very shallowest and youngest nodes (Figure 4). Esti-mating extinction rates from phylogenies is contentiousand often leads to large confidence intervals [37,83,84],which is what we infer with our data. Nevertheless, our re-sults are potentially in line with estimates for other herb-aceous groups [85]. Even relatively moderate extinctionrates may limit our ability to confidently reconstruct bio-geographic history, and so inferences based on the very lowoptimal extinction rate predicted in the DEC analysisshould be treated cautiously. However, despite the greateruncertainty in biogeographic reconstructions at higher ex-tinction rates, the New Zealand and Indian species mustrepresent recent long-distance dispersal events, given theirvery recent separation from closely related Australian spe-cies. The Indian species was discovered only recently (1994;[20]) and yet has a relatively extensive range [20], whichmay add further weight to the possibility that the globaldistribution of the family may be more extensive than iscurrently reported [7,10,86]. Further phylogeographic workin individual species may also reveal additional instances ofintra-specific migration and extinction (e.g., with regards tothe substantially disjunct distribution of Trithuria inconspi-cua in New Zealand).ConclusionsOur analyses suggest the Hydatellaceae lineage arose in theLower Cretaceous, but that extant species diversity datesfrom the Miocene. The former age highlights the early ex-ploitation of aquatic environments by angiosperms. Our re-sults also emphasize the potentially high extinction rateassociated with ephemeral aquatic habitats. Despite havinga classical Gondwanan intercontinental pattern, the youngage of the crown clade of Hydatellaceae contradicts the roleof vicariance events in shaping the family’s distribution.This suggests instead that long-distance dispersal is pre-dominately responsible for its disjunct distribution bothwithin and outside Australia.Availability of supporting dataThe new data sets supporting the results of this articleare included within the article (and its additional files).Additional filesAdditional file 1: Voucher and accession information for seed-plantmolecular dating.Additional file 2: Seed plant alignment matrix.Additional file 3: Chronogram and table of inferred ages from theBayesian random local clock molecular dating analysis of theseed plants.Additional file 4: Tree file for the seed-plant Bayesian random localclock tree.Additional file 5: Table of inferred ages in the Bayesian multi-speciescoalescent molecular dating of Hydatellaceae.Additional file 6: Tree file for the Hydatellaceae Bayesian multi-speciescoalescent tree.AbbreviationsAICc: Corrected Akaike information criterion; ASR: Ancestral statereconstruction; BI: Bayesian inference; DEC: Dispersal extinction cladogenesis;DIVA: Dispersal vicariance; HPD: Highest posterior density; Ma: Millions ofIles et al. BMC Evolutionary Biology 2014, 14:102 Page 8 of 10http://www.biomedcentral.com/1471-2148/14/102years ago; ML: Maximum likelihood; Myr: Millions of years; RLC: Random localclock; UCLN: Uncorrelated lognormal.Competing interestsThe authors declare that they have no competing interests.Authors' contributionsWJDI designed the study and carried out the analyses. CL constructed thedistribution map. All authors contributed to drafting the manuscript; writingwas led by WJDI and SWG. All authors read and approved the finalmanuscript.AcknowledgementsWe thank Marc Jopson and Rick Ree for technical assistance withprogramming and data analysis, John Conran for advice on ephemeralaquatic plant ecology, and Darren Irwin for advice on biogeographicanalyses. This work was supported by a University of British ColumbiaGraduate Scholarship to WJDI and an NSERC (Natural Sciences andEngineering Research Council of Canada) Discovery Grant to SWG.Author details1Department of Botany, University of British Columbia, 3529-6270 UniversityBlvd, Vancouver, British Columbia, V6T 1Z4, Canada. 2UBC Botanical Garden &Centre for Plant Research, University of British Columbia, 6804 Marine Dr SW,Vancouver, British Columbia, V6T 1Z4, Canada. 3Department of Higher Plants,Biological Faculty, M.V. Lomonosov Moscow State University, 119234Moscow, Russia. 4Department of Botany, Shivaji University, Kolhapur 416 004,Maharashtra, India. 5Botanic Gardens and Parks Authority, Kings Park andBotanic Garden, West Perth, WA 6005, Australia and School of Plant Biology,University of Western Australia, Nedlands, WA 6009, Australia. 6Department ofParks & Wildlife, Western Australian Herbarium, Science Division, Brain Street,Manjimup 6258, WA, Australia. 7Jodrell Laboratory, Royal Botanic Gardens,Kew, Richmond, Surrey, TW9 3AB, UK.Received: 21 February 2014 Accepted: 1 May 2014Published: 13 May 2014References1. Martin HA: Cenozoic climatic change and the development of the aridvegetation in Australia. J Arid Environ 2006, 66:533–563.2. Aston HI: Aquatic Plants of Australia. Melbourne: Melbourne University Press;1973:368.3. Diels L: Die Pflanzenwelt von West-Australien südlich des Wendekreisesmit einer Einleitung über die Pflanzenwelt Gesamt-Australiens inGrundzügen. 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