Reconstructing the age and historical biogeography of the ancient flowering-plant family Hydatellaceae (Nymphaeales)
© Iles et al.; licensee BioMed Central Ltd. 2014
Received: 21 February 2014
Accepted: 1 May 2014
Published: 13 May 2014
The aquatic flowering-plant family Hydatellaceae has a classic Gondwanan distribution, as it is found in Australia, India and New Zealand. To shed light on the biogeographic history of this apparently ancient branch of angiosperm phylogeny, we dated the family in the context of other seed-plant divergences, and evaluated its biogeography using parsimony and likelihood methods. We also explicitly tested the effect of different extinction rates on biogeographic inferences.
We infer that the stem lineage of Hydatellaceae originated in the Lower Cretaceous; in contrast, its crown originated much more recently, in the early Miocene, with the bulk of its diversification after the onset of the Pliocene. Biogeographic reconstructions predict a mix of dispersal and vicariance events, but considerations of geological history preclude most vicariance events, besides a split at the root of the family between southern and northern clades. High extinction rates are plausible in the family, and when these are taken into account there is greater uncertainty in biogeographic inferences.
A stem origin for Hydatellaceae in the Lower Cretaceous is consistent with the initial appearance of fossils attributed to its sister clade, the water lilies. In contrast, the crown clade is young, indicating that vicariant explanations for species outside Australia are improbable. Although long-distance dispersal is likely the primary driver of biogeographic distribution in Hydatellaceae, we infer that the recent drying out of central Australia divided the family into tropical vs. subtropical/temperate clades around the beginning of the Miocene.
KeywordsAquatic plants, Austral, Ephemeral habitats, Extinction rates, Intercontinental dispersal, ANITA-grade angiosperms, Trithuria Vicariance
Australia has seen widespread rainforest replaced with deserts, savannah and sclerophyll biomes since the Eocene, in response to global cooling . Despite the dramatic loss of mesophytic habitat, it has a well-developed wetland flora, with many endemic species . Perhaps the most unique of these habitats are ephemeral bodies of water that are home to communities characterized by extreme reduction in plant size, and annual or geophytic life histories [3, 4]. Common Australian members of this ephemeral aquatic habitat include Centrolepidaceae (a family closely related to or possibly embedded within the southern rushes , Restionaceae), the sundew genus Drosera L. (Droseraceae), and Hydrocotyle L. (Araliaceae) [3, 6], but its most noteworthy component may be the family Hydatellaceae . Most members of Hydatellaceae exemplify the ephemeral aquatic syndrome, apart from a recently derived pair of perennial apomictic species that live submerged in more permanent bodies of water [8, 9].
Hydatellaceae were recently recognized as the sister group of the water lilies (Cabombaceae and Nymphaeaceae), placing their divergence close to the root of angiosperm phylogeny e.g., . They have since attracted considerable attention because of the insights they may provide into the evolution of early angiosperms [11–16]. Of particular interest is the nature of the reproductive structures in the family, which may represent floral, prefloral, or pseudanthial arrangements of reproductive organs, and the incidence of unisexual and bisexual reproductive units. These may bear on our understanding of the ancestral floral Bauplan of angiosperms [8, 9, 13]. Contemporary taxonomic and phylogenetic work on the family recognizes one genus, Trithuria Hook. f., and 12 species in four monophyletic sections [8, 9].
Since the recognition that Hydatellaceae represents an ancient angiosperm lineage, a few fossils have been linked with it [7, 24–26]. The most spectacular of these may be the aquatic plant Archaefructus, represented by whole fruiting plants from the Yixian Formation of Liaoning, China [27, 28]. However, the timing and interpretation of these and other records remains contentious [7, 29]. Unlike the fossil record of Hydatellaceae, water lilies have an extensive record that extends to the Lower Cretaceous [29–31]. Collectively these fossils suggest that aquatic niches were exploited early in the evolution of angiosperms, although the aquatic life-form is unlikely to be ancestral in flowering plants as a whole [32, 33]. Nonetheless, an improved understanding of the diversification of Hydatellaceae may help illuminate early angiosperm ecology and how plants colonize ephemeral wetlands, which represent a unique and potentially stressful environment [4, 34].
To address these questions we dated the earliest splits in Hydatellaceae using 17 plastid-genes sampled from across the seed plants, and used the resulting posterior age distributions as secondary calibrations for a species-tree analysis of the entire family, which lacks suitable fossil calibrations. Although the use of secondary calibration points has been criticized for propagating “error free” values into downstream analyses , here we use the entire posterior distribution from the seed-plant analysis as a prior for the subsequent analysis, accounting for the associated uncertainty . We used the dated species tree to explore biogeographic hypotheses using parsimony and likelihood. In particular, likelihood-based approaches allow the estimation of parameters such as speciation rate. We also explicitly test the effect of extinction rate on biogeographic reconstruction, as this may be high in Hydatellaceae due to the patchy distribution of their habitat in space and time [4, 34] and is also suggested by the “broom-and-handle” shape of the phylogeny [9, 37–39].
Fossil selection and molecular dating
Fossil calibrations for seed-plant phylogeny
Crown seed plants
316.0–367.5 (2, 1)
Glossopterid, Gangamopteris McCoy
294.8–346.3 (2, 1)
Pluricarpellatia peltata B. Mohr, Bernardes-de-Oliveira & D.W. Taylor
99.1–118.0 (1, 1)
Monetianthus mirus Friis, Pedersen, von Balthazar, Grimm & Crane
93.2–112.1 (1, 1)
98.9–110.4 (0.5, 1)
124.2–135.7 (0.5, 1)
Mayoa portugallica Friis, Pedersen & Crane
96.5–115.4 (1, 1)
West Brothers platanoid and Sapindopsis Fontaine
93.2–112.1 (1, 1)
To test for and accommodate non-clocklike behaviour in the seed-plant data set we used the Bayesian random local clocks (RLC) method . This accommodates molecular rate variation by allowing different sub-branches of the tree to have unique molecular clocks. Dornberg et al.  examined the performance of this method against the more widely used uncorrelated lognormal (UCLN) method  for real and simulated data sets that show high amounts of inter-clade rate variability, and found that the RLC model performed better in the presence of clade-specific rate shifts. This may be pertinent to angiosperm studies like ours, as there are known to be substantial shifts in rates among major angiosperm clades that are associated with changes in habit and life history . In particular, Hydatellaceae occupy a part of the tree where there were multiple shifts in habit (for example, Hydatellaceae are mostly herbaceous annuals, water lilies are mostly perennial herbs, Amborella Baill. and Austrobaileyales 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, with default priors (or those suggested by http://code.google.com/p/beast-mcmc/wiki/ParameterPriors if not automatically implemented). The BEAST analysis requires that each of the fossil calibrations have an associated prior. We used lognormal priors with 95% prior intervals of ~10–20% of the fossil age (Table 1), consistent with some other studies, e.g.,  (the RLC method is also more robust than the UCLN method to variation in the width of the 95% prior interval ). We ran seven runs of 4.0 × 107 generations, and considered four that converged on the same posterior and likelihood scores after 10% burnin. The estimated sample sizes of run statistics (posterior, prior, likelihood, parameter estimates) were all over 200 when these runs were pooled. The seed-plant chronogram and a table of divergence times is presented in Additional file 3, and the tree file is provided in Additional file 4. In all analyses we constrained Nymphaeaceae s.s. (i.e., excluding Cabombaceae) to be monophyletic, consistent with molecular and morphological analyses [62–64]. We also tested a constraint that forces Amborella to be the sister group of all other angiosperms; this arrangement contrasts with a clade comprising Amborella and Nymphaeales that we recovered in the RLC analysis, see below (these two alternative arrangements have been recovered in different studies, see , for example). We constrained cycads to be the sister group of angiosperms among extant seed plants, consistent with some recent studies [24, 42, 43, 54], but also explored alternative gymnosperm sister groups to angiosperms (conifers alone, Ginkgo L. alone, or pairwise combinations of conifers, cycads and Ginkgo), or used no outgroup constraints. For these different constraint analyses we ran a single 4.0 × 107 generation replicate; they all indicated only a minimal effect on the two ages within Hydatellaceae (<1 Myr difference; data not shown).
To date the Hydatellaceae species tree we considered the data set of , which consists of two unlinked loci (four plastid regions and the nuclear ribosomal internal transcribed spacer region, ITS) for all species except Trithuria occidentalis Benth. which was only sampled for one plastid region. In all analyses T. submersa was provisionally considered to comprise separate eastern and western species, following . The data were analysed with *BEAST, which estimates the species tree with a Bayesian implementation of the multi-species coalescent . We used the settings outlined in , with the exception that we assigned the two Hydatellaceae posterior distributions determined from the RLC seed-plant analysis (see Additional file 3) as Gaussian priors for the corresponding splits in the species tree (i.e., the crown node of Hydatellaceae and the crown node of the clade consisting of sect. Hydatella and sect. Trithuria). These priors were only applied to the plastid loci (for which there was outgroup data), using the rooting of Hydatellaceae determined in the seed-plant analysis (see Additional file 3).
The ASR analyses were performed with BayesTraits version 1.0 (http://www.evolution.rdg.ac.uk; ). We considered three nested models which were evaluated using the corrected Akaike information criterion (AICc; ). The most complex model (hereafter the ‘full model’) assumed three separate symmetrical transition rates: between Australia and India or New Zealand (assuming trans-oceanic dispersals to be equivalent), between south-western and south-eastern Australia (dispersals across the Nullarbor Plain), and between northern Australia and south-western or south-eastern Australia (dispersals across the arid zone). The simplest model (‘simple model’) consists of a single rate between all the allowed transition rates in the full model. The two-rate transition model has symmetric rates between Australia and India or New Zealand, contrasting with a separate rate for all transitions within Australia (‘continental model’). Root state frequencies were set to empirical values.
Molecular dating and diversification
Hydatellaceae are estimated to have diverged from the water lilies 126.7 Ma (120.6–133.2 Ma, 95% HPD), in the Lower Cretaceous, with a crown clade age of 19.1 Ma (15.7–23.4 Ma, 95% HPD), in the early Miocene (see Additional file 3). The estimated multi-species coalescent age for the crown of Hydatellaceae is 17.6 Ma (14.7–20.6 Ma, 95% HPD), in the early Miocene, with most diversification occurring after ~6 Ma, in the late Miocene (Figure 2a; see Additional file 5 for a table of divergence times, and Additional file 6 for the tree file). For the speciation-extinction analysis we estimated a speciation rate of 0.430 Myr-1 (0.107–0.881 Myr-1; 95% HPD) and a lineage extinction rate of 0.446 Myr-1 (0.003–0.955 Myr-1; 95% HPD). Including a distantly related outgroup did not substantially change speciation or extinction parameter estimates (data not shown).
The full ASR model had the best AICc score (Figure 2b; differences between best and alternative models: simple Δ = 1.06; continental Δ = 2.135). It shows a split between the tropical (northern Australia and India) and subtropical/temperate (south western Australia, south eastern Australia, and New Zealand) clades (Figure 2b). Within the tropical clade we infer that the Indian species, Trithuria konkanensis S.R. Yadav & Janarth, represents a relatively recent long-distance dispersal event from northern Australia (Figure 2b). Within the subtropical/temperate clade, the New Zealand species T. inconspicua represents a long-distance dispersal event from south-eastern Australia. There is no significant support for a particular direction of dispersal between south-western and south-eastern Australia (Figure 2b).
The phylogenetic origin of Hydatellaceae near the root of angiosperm phylogeny  and lack of reliable fossils  make consideration of the family age infeasible outside the context of angiosperm divergence times. Unfortunately the crown age and subsequent timing of diversification of angiosperms remains one of the most vexing questions in evolutionary biology, with some molecular estimates [42, 49, 61] substantially older (~100 Myr) than the oldest reported crown angiosperm fossils . Our estimated age of 158.7 Ma (151.0–167.7 Ma, 95% HPD; see Additional file 3) is more in-line with less extreme results reported elsewhere [75, 76]. A stem age for Hydatellaceae of ~127 Ma (see Results and Additional file 3) suggests that stem lineage Hydatellaceae were colonizing aquatic environments in the Lower Cretaceous, although when Hydatellaceae acquired the unique suite of traits 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) indicates that a proposed Gondwanan explanation for the current intercontinental distribution  is incorrect, as it would require that the Indian and north Australian species pair Trithuria konkanensis and T. lanterna diverged ~125 Ma, according to the timing of the breakup of East Gondwana , instead of the estimated divergence time of 0.76 Ma (0.24–1.33 Ma, 95% HPD; see Figure 2a and Additional file 5). This highlights the importance of assessing proposed vicariant patterns with a careful consideration of phylogeny, geology, and estimated divergence times .
Within Australia, climate driven vicariance events are more plausible, although here as well, the last submersion of the Nullarbor Plain (~15 Ma), which separates the south-eastern and south-western regions, substantially predated the relevant phylogenetic splits (Figure 2a; ). However, the DIVA and DEC analyses indicate a continent-scale vicariance event at the root of extant Hydatellaceae (Figure 2c,d). The interior of Australia was still relatively wet in the early Miocene (up to the mid-Miocene), and although there were permanent lakes, there was also a marked dry season, indicating the potential for ephemeral aquatic habitats . The continued aridification of central Australia presumably led to this vicariance event. Our analyses therefore support a minimum of four long-distance dispersal events in Hydatellaceae (Australia to India, Australia to New Zealand, and two instances from south-western to south-eastern Australia; Figure 2). The inferred long-distance dispersal events likely involved selfers or apomicts, consistent with Baker's Law . The New Zealand species Trithuria 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 northern Australia [8, 81]. Baker’s Law has been extended to dispersal in general, not just islands, and as a result we expect selfing taxa to have wider distributions than outcrossing ones . This seems to be the case in Hydatellaceae, where dioecious species are generally much more limited in distribution than related cosexual species .
Statistical biogeographic methods such as DEC allow not only an examination of the biogeographic history of a clade and an estimate of the processes involved in producing that history (dispersal, vicariance and extinction), but also quantification of how confident we are in these reconstructions, via consideration of (relative) likelihoods. A strong bias towards estimating zero area extinction rates may occur in the DEC framework, both for real and simulated data sets . We examined the effect that this may have on our reconstructions by manually varying the extinction rate based on the range of values seen in our speciation-extinction analysis (see Results). Our confidence in reconstructing both (a) range pairs (thereby indicating possible processes such as vicariance or dispersal; Figure 3), and (b) each individual descendent lineage’s range (as indicated by the relative likelihoods for each range across all possible range pairs; Figure 4), is compromised at higher rates. For the estimated extinction rate based on tree shape (~0.5 Myr-1), there is very little confidence in any particular range pair (relative likelihoods are <0.6, Figure 3), and in the ranges of individual descendent lineages, besides a few of the very shallowest and youngest nodes (Figure 4). Estimating extinction rates from phylogenies is contentious and often leads to large confidence intervals [37, 83, 84], which is what we infer with our data. Nevertheless, our results are potentially in line with estimates for other herbaceous groups . Even relatively moderate extinction rates may limit our ability to confidently reconstruct biogeographic history, and so inferences based on the very low optimal extinction rate predicted in the DEC analysis should be treated cautiously. However, despite the greater uncertainty in biogeographic reconstructions at higher extinction rates, the New Zealand and Indian species must represent recent long-distance dispersal events, given their very recent separation from closely related Australian species. The Indian species was discovered only recently (1994; ) and yet has a relatively extensive range , which may add further weight to the possibility that the global distribution of the family may be more extensive than is currently reported [7, 10, 86]. Further phylogeographic work in individual species may also reveal additional instances of intra-specific migration and extinction (e.g., with regards to the substantially disjunct distribution of Trithuria inconspicua in New Zealand).
Our analyses suggest the Hydatellaceae lineage arose in the Lower Cretaceous, but that extant species diversity dates from the Miocene. The former age highlights the early exploitation of aquatic environments by angiosperms. Our results also emphasize the potentially high extinction rate associated with ephemeral aquatic habitats. Despite having a classical Gondwanan intercontinental pattern, the young age of the crown clade of Hydatellaceae contradicts the role of vicariance events in shaping the family’s distribution. This suggests instead that long-distance dispersal is predominately responsible for its disjunct distribution both within and outside Australia.
Availability of supporting data
The new data sets supporting the results of this article are included within the article (and its additional files).
Corrected Akaike information criterion
Ancestral state reconstruction
Dispersal extinction cladogenesis
Highest posterior density
Millions of years ago
Millions of years
Random local clock
We thank Marc Jopson and Rick Ree for technical assistance with programming and data analysis, John Conran for advice on ephemeral aquatic plant ecology, and Darren Irwin for advice on biogeographic analyses. This work was supported by a University of British Columbia Graduate Scholarship to WJDI and an NSERC (Natural Sciences and Engineering Research Council of Canada) Discovery Grant to SWG.
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