evolution from gymnosperms to angiospermsevolution from gymnosperms to angiosperms

APG IV. ADS Sci. Evol. Bot. Fossil evidence (see the figure below) indicates that flowering plants first appeared in the Lower Cretaceous, about 125 million years ago, and were rapidly diversifying by the Middle Cretaceous, about 100 million years ago. From a functional perspective, it may seem difficult to explain why the hypothesized ancestral flower had more perianth organs than most extant flowers. Magalln, S., Gmez-Acevedo, S., Snchez-Reyes, L. L. & Hernndez-Hernndez, T. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. Initial tests showed that for some characters, the prior on the root state could affect results in terms of both transition rates and ancestral states62. (credit: W. T. Lee, USGS). The exact number of organs could not be reconstructed precisely. In addition, we tested two unidirectional models for all binary characters (UNI01 and UNI10: rates from 1 to 0 or 0 to 1, respectively, set to zero)52,62, a symmetrical model for all multistate characters (SYM: rates equal for transitions between two given states), and three ordered models for all multistate characters derived from quantitative variables (ORD: rates between non-adjacent states set to zero; ORDSYM: symmetrical version; ORDER: single-rate version). In total, the data set presented here contains 13,444 floral trait data records obtained from 947 distinct sources. Angiosperms produce their gametes in separate organs, which are usually housed in a flower. In addition, each analysis was replicated using alternative hypotheses for early angiosperm phylogeny (for example, whether Amborella alone or Amborella and Nymphaeales together are the sister group of all remaining angiosperms) and two alternative estimates for the age of the angiosperms, which remain highly debated topics (Supplementary Discussion)1,2,4,23. Res. Sauquet, H. et al. Stevens, P. F. Angiosperm Phylogeny Website. A. Ancestral traits and specializations in the flowers of the basal grade of living angiosperms. Grey branches denote missing, inapplicable or polymorphic data. Article Although we cannot be absolutely sure and we must not make assumptions without evidence, it seems very likely that all plants earlier than the flowering ones were entirely in shades of green or perhaps yellow. Non-equilibrium dynamics and floral trait interactions shape extant angiosperm diversity. Traditional methods involve comparison of homologous anatomical structures and embryonic development, assuming that closely related organisms share anatomical features during embryo development. New Phytol. Gymnosperm roots The ancestors of gymnosperms most likely evolved from a group of plants called the seed ferns (pteridosperms), which are known only from the fossil record. Preprint at http://www.R-project.org/ (2014). As for our single-trait analyses, we used both an ML and a Bayesian rjMCMC approach to test for correlations and their impact on reconstructed ancestral states, using again the rayDISC function of corHMM 1.18 (ref. In some cases, prior results from morphological studies have been confirmed: for example, confirming Amborella trichopoda as the most primitive angiosperm known. (c) Symmetry of perianth (character 207_B). CAS 98, 370396 (2011). This process, known as synorganization, is thought to have increased pollination efficiency and helped trigger some of the most spectacular radiations in angiosperms, such as the Asteraceae and Orchidaceae35. It will be understood, therefore, that when Caytonia [Fig.21] was first discovered in rocks about 160 million years old there was considerable interest among palaeobotanists. BMC Evol. S.M., J.A.D. & Barker, D. Bayesian estimation of ancestral character states on phylogenies. The Faculty of Life Sciences and the Key Research Area Patterns and Processes of Plant Evolution and Ecology of the University of Vienna, and Agence Nationale de la Recherche grant ANR-12-JVS7-0015-01 (MAGNIPHY) to H.S. PubMed Central Thus, integrating phylogenetic uncertainty in our Bayesian analyses of trait evolution was the primary motivation for reanalysing the data set in BEAST without fixing the topology. R. Soc. PubMed A. However, flowers are a relatively recent evolutionary innovation on the geological timescale of plant diversification. Natl Acad. Huelsenbeck, J. P., Nielsen, R. & Bollback, J. P. Stochastic mapping of morphological characters. Natl Acad. The floral morphospacea modern comparative approach to study angiosperm evolution. Second, the BEAST analyses had been conducted with a fixed topology, producing a collection of trees that differed in branch lengths (times) but not topology. Preprint at http://www.mobot.org/MOBOT/research/APweb/ (2012). Biol. (b) Fusion of perianth (character 204_A). Using chronograms from molecular dating analyses calibrated with 136 fossil constraints1, we provide the first model-based reconstructions of ancestral flowers at the deepest nodes in the phylogeny of angiosperms. Endress, P. K. Development and evolution of extreme synorganization in angiosperm flowers and diversity: a comparison of Apocynaceae and Orchidaceae. Foster, C. S. P. et al. However, we recommend caution with the use of these trees for purposes other than this study. Philos. In particular, complete mitogenomes are available for all major seed plant lineages except Conifer II (non-Pinaceae conifers or Cupressophyta), an . ADS In their turn, plants started to produce brightly coloured structures to attract the insects. PubMed Commun. Syst. Proc. 328 Citations 144 Altmetric Metrics Abstract Angiosperms are by far the most species-rich clade of land plants, but their origin and early evolutionary history remain poorly understood. We also infer that the perianth and the androecium probably had whorled phyllotaxis with three organs per whorl. In the D series, we constrained Chloranthaceae, Magnoliidae, Ceratophyllaceae and Eudicotyledoneae to form a clade23. When we come to discuss the angiosperms we shall see that a distinct advantage appears to be conferred on seed plants that have their seeds in some sort of container. 44, 161 (2006). CAS In this history of plants on Earth we are now approaching a time of important events which gradually brought about the situation we see today with the flowering plants being the most obvious ones because of the bright colours of their flowers. As flowers are highly complex and integrated structures, floral traits are unlikely to evolve independently from one another25,26,27,28,29,30. CAS Cantino, P. D. et al. A few other angiosperm groups called basal angiosperms, are viewed as primitive because they branched off early from the phylogenetic tree. Syst. and JavaScript. In addition, we tested the impact of the age of the angiosperms on our ancestral state reconstructions. A. Recognising angiosperm clades in the Early Cretaceous fossil record. DNA from minute amounts of living organisms or fossils can be amplified by polymerase chain reaction (PCR) and sequenced, targeting the regions of the genome that are most likely to be conserved between species. 314, 204215 (2012). Key Points Gymnosperms produce both male and female cones, each making the gametes needed for fertilization; this makes them heterosporous. PubMed Gray branches represent missing data. Many attract animals that will eat the fruit and pass the seeds through their digestive systems, then deposit the seeds in another location. As the tools of molecular biology and computational analysis have been developed and perfected in recent years, a new generation of tree-building methods has taken shape. This allowed us to produce trees of 792 species and prepare a matching data set of floral traits for exactly the same species, following a strict exemplar approach (see below). Summary (MCC) BEAST trees are provided as Supplementary Data 312 and a complete list of morphological data records and references (extracted from PROTEUS) is provided as Supplementary Data 13. This group is called the gymnosperms, which means naked seeds. and J.S. 57, 34713503 (2006). We also evaluated the level of correlation among floral traits and its impact on reconstructed ancestral states. Article Google Scholar. This approach is particularly useful where model space is very large, such as for multistate discrete characters (see Supplementary Methods). USA 107, 46234628 (2010). Minimum numbers were chosen for this representation, but reconstructions with more floral organs are also compatible with our results (for further details, see Supplementary Discussion, section Reconstructing the ancestral flower). They produce microspores, which develop into pollen grains (the male gametophytes), and megaspores, which form an ovule containing the female gametophytes. To address this problem, there are three complementary approaches7. & Endress, P. K. in Flowers on the Tree of Life eds Wanntorp L., Ronse De Craene L. P. 88119Cambridge University Press (2011). 48, 612622 (1999). http://www.mobot.org/MOBOT/research/APweb/, http://creativecommons.org/licenses/by/4.0/, Climate windows of opportunity for plant expansion during the Phanerozoic, The accessory neural arch: development, morphology, and systematic distribution, The pineapple MADS-box gene family and the evolution of early monocot flower, Insights into angiosperm evolution, floral development and chemical biosynthesis from the Aristolochia fimbriata genome, Probing the floral developmental stages, bisexuality and sex reversions in castor (Ricinus communis L.). (a) Ovary position (character 102_B). Syst. However, for most traits, nodes and trees, the three approaches reconstructed the same ancestral state and rjMCMC CIs were narrow (Supplementary Data 1 and Supplementary Discussion). Angiosperms did not evolve from gymnosperms, but instead evolved in parallel with the gymnosperms; however, it is unclear as to what type of plant actually gave rise to angiosperms. These analyses produced trees with Amborella sister to Nymphaeales rather than to all other angiosperms, and with monocots sister to Chloranthaceae+Magnoliidae rather than to Ceratophyllaceae+Eudicotyledoneae (see Supplementary Discussion and Supplementary Fig. Chartier, M. et al. Biol. Cite this article. 6, 13111319 (2015). 14, 23 (2014). Syst. Bot. Herendeen, P. S., Friis, E. M., Pedersen, K. R. & Crane, P. R. Palaeobotanical redux: revisiting the age of the angiosperms. Flowers are the reproductive structures of angiosperms (flowering plants), which represent ca. In this study, we make these inferences based on the distribution of traits in extant angiosperms and their phylogenetic relationships, and, for the first time, methods using explicit models of stochastic evolution for morphological characters. Specifically, for each character pair, we fitted four correlated models (ARDnodual, ARDnodualeq, differing only in the root state prior: see above; SYMnodual, SYMnodualeq) and three uncorrelated models (ERnodual, UNCORRnodual, UNCORRnodualeq; UNCORRnodual corresponds to the most general, 4-parameter independent model from ref. Biology Seed Plants Evolution of Seed Plants. We found that our results are generally robust and unaffected by the choice of ancestral state reconstruction method, alternative phylogenies and different divergence time estimates. The images or other third party material in this article are included in the articles Creative Commons license, unless indicated otherwise in a credit line to the material. 4). All primary characters used in data entry were transformed for analysis (discrete characters were simplified and continuous characters were discretized; see Supplementary Methods for justification and details of these transformations). These were the first plants to reproduce by seeds, despite looking deceptively like ferns. Among the fossil cycads and cycadeoids are also to be found specimens of another group which flourished from about 190 million years ago. Both fertilization and embryo development take place inside an anatomical structure that provides a stable system of sexual reproduction largely sheltered from environmental fluctuations. New data in comparative genomics and paleobotany have, however, shed some light on the evolution of angiosperms. Third, a reduced number of whorls may have been a prerequisite for secondary elaboration of floral structure (for example, bilateral symmetry, fusion of organs; Fig. For each floral trait, we tested and compared at least two distinct Markov models of discrete character evolution in our ML analyses: the equal rates (ER) or Mk model59, which assumes a single rate of transition among all possible states, and the all rates different (ARD) or AsymmMk model60,61, which allows a distinct rate for each possible transition between two states. We thus obtained a new set of 22 presumably independent characters and analysed all 231 pairwise correlations among these characters (Table 1). We use cookies and similar technologies to ensure our website works properly, personalize your browsing experience, analyze how you use our website, and deliver relevant ads to you. With only 1,000 living species, gymnosperms represent four of the five seed plant lineages including conifers (Pinophyta), cycads (Cycadophyta), ginkgos (Ginkgophyta), and gnetophytes (Gnetophyta; Wang & Ran, 2014 ). Sauquet, H. PROTEUS: A database for recording morphological data and creating NEXUS matrices, Version 1.26. Other relationships and divergence times were very similar to those found in the A series, but with some variation among trees of the posterior sample regarding the more weakly supported nodes. New data in comparative genomics and paleobotany have, however, shed some light on the evolution of angiosperms. Although reconstruction of ancestral floral phyllotaxis proved relatively uncertain in this study (Supplementary Discussion), as in previous work based on parsimony alone18,19,20, the implications of our result are important to consider for two reasons. the evolution of the gymnosperms? Nat. New Phytol. Instead, we recorded the total number of perianth parts (sepals plus petals, or tepals). The absolute timescale provided here corresponds to divergence time estimated with a narrow constraint on the maximum age of angiosperms1; relaxing this constraint to reflect alternative studies that yielded older age estimates for angiosperms resulted in nearly identical ancestral reconstructions (see Supplementary Discussion). This particularly so in older rocks because the discovery of carpels might pre-date all other known occurrences and could be very valuable in determining the evolution of flowering plants. Natl Acad. Discuss the purpose of pollen grains and seeds. Ancestral state reconstruction using model-based methods requires a phylogenetic tree with branch lengths proportional to time (that is, a chronogram) or to the number of inferred molecular substitutions (that is, a phylogram). Article Other states need to be interpreted with caution as their reconstruction was either associated with higher uncertainty (for example, perianth phyllotaxis, number of stamen whorls) or inconsistent across methods (for example, sex reconstructed as equivocal with parsimony). 2004 Feb;37(4 . Int. For instance, it was still unknown whether the ancestral flower was unisexual or bisexual21. Evolution of mitochondrial RNA editing sites in gymnosperms. Taken together, there seems to be a general trend of increasing relative embryo size during evolution (higher E : S ratio) for both angiosperms and gymnosperms (Forbis et al., 2002; Baskin & Baskin, 2004). Evol. Gymnosperm seeds are typically formed in unisexual cones and are known as "naked" seeds since they lack the protective cover angiosperms provide their seeds. B 283, 20152304 (2016). The cockleburs that clung to the velvet trousers of an enterprising Swiss hiker, George de Mestral, inspired his invention of the loop and hook fastener he named Velcro. Sci. This implies that all extant flowers, including those of the earliest-diverging lineages of angiosperms (for example, Amborella and Nymphaeales), are derived in several aspects24. Key Terms clade : a group of animals or other organisms derived from a common ancestor species New Phytol doi: 10.1111/nph.14483 (2017). This framework includes: i) the placement of Zygnematophyceace as sister to land plants ( Embryophyta ), ii) a clade of extant gymnosperms ( Acrogymnospermae) with cycads + Ginkgo sister to remaining extant gymnosperms and with gnetophytes ( Gnetophyta) sister to non- Pinaceae conifers (Gnecup trees), and iii) within the monilophyte clade ( Moni. However, graphical MP and ML reconstructions for the entire tree are available (Supplementary Data 1423). Support for correlation is here measured by the Bayes Factor comparing the dependent models to the independent models, rewritten as the ratio of the posterior to the prior odds of the two models56: BFDI=[P(MD|D)/P(MI|D)]/[(2114651)/51], where P(MD|D) and P(MI|D) are the sampling frequencies of dependent and independent models, respectively. Rambaut, A., Suchard, M. A., Xie, D. & Drummond, A. J. Tracer v.1.6. The ancestral flower of angiosperms and its early diversification. Here, we focus on and report results for 15 key nodes in the phylogeny of angiosperms, corresponding to well-recognized major clades (including Angiospermae, Mesangiospermae, Magnoliidae, Monocotyledoneae, Eudicotyledoneae, Pentapetalae, Rosidae and Asteridae). In summary, we use cookies to ensure that we give you the best experience on our website. 1). H.S., M.v.B., E.B., E.B.M., K.B.-H., L.C., M.C., G.C., M.C., J.H.L.E.O., C.E., F.J., T.H., R.H., S.A.L., S.L., J.A.L., J.M., S.N., S.S., C.P., E.R., P.d.S., K.S., A.S., Y.S., G.F.T., A.W.-S.L. Gomez, B., Daviero-Gomez, V., Coiffard, C., Martn-Closas, C. & Dilcher, D. L. Montsechia, an ancient aquatic angiosperm. (credit: United States Geological Survey) Cookies are small files that are stored on your browser. OMeara, B. C. et al. Therefore, we tested correlations among all possible pairs of binary floral traits in our data set. Here we report model-based reconstructions for ancestral flowers at the deepest nodes in the phylogeny of angiosperms, using the largest data set of floral traits ever assembled. How (much) do flowers vary? In angiosperms, individual flowers can be unisexual, with separate male and female flower structures, or . Interestingly, we found that this is not always true (about half of the floral traits examined yielded highly confident estimates; Fig. USA 112, 1098510988 (2015). Note that there is uncertainty associated with some of these reconstructions (especially for Angiospermae, Magnoliidae and Eudicotyledoneae). MP and ML reconstructions were conducted on the MCC tree from each BEAST analysis, whereas Bayesian rjMCMC analyses were conducted on collections of at least 1,000 trees sampled from the posterior stationary distribution from the BEAST analyses. Based on fossil evidence and molecular clock calibration, the divergence between gymnosperms and angiosperms could be dated to about 300-350 million years ago (Mya) in the Carboniferous (Hedges et al., 2006, Won and Renner, 2006, Clarke et al., 2011, Crisp and Cook, 2011, Magalln et al., 2013). The botanical name for the seed container in flowering plants is the carpel. Trans. (d) Number of perianth whorls (character 231_A). The Importance of Seed Plants in Human Life, Continue With the Mobile App | Available on Google Play, http://cnx.org/contents/185cbf87-c72e-48f5-b51e-f14f21b5eabd@11.2, log Moore, M. J., Bell, C. D., Soltis, P. S. & Soltis, D. E. Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Biol. The genes encoding the ribosomal RNA from the small 18S subunit and plastid genes are frequently chosen for DNA alignment analysis. Basal angiosperms, such as water lilies, are considered more primitive because they share morphological traits with both monocots and eudicots. Bot. Maddison, W. P., Midford, P. E. & Otto, S. P. Estimating a binary characters effect on speciation and extinction. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. 53, 673684 (2004). In seed plants, the evolutionary trend led to a dominant sporophyte generation, in which the larger and more ecologically significant generation for a species is the diploid plant. Various plant species evolved in different eras. Ann. The ancestral flower of angiosperms and its early diversification. Am. Plant Sci. A. 100, 603619 (2007). Article Angiosperms means seeds in containers. Schliep, K. P. phangorn: phylogenetic analysis in R. Bioinformatics 27, 592593 (2011). 0 to 1. Discarding the first 1M generations as burn-in was sufficient for all analyses and effective sample size values were nearly always very high (above 200), except for a few particular traits characterized by frequent jumps of the chain between very different models. 40, 301326 (2012). The divergence of angiosperms from gymnosperms occurred between 200 and 250 million years ago. We note that the effective sample size for some parameters of these analyses did not all reach 200 as recommended, suggesting that longer runs might be needed for accurate estimation of phylogenetic relationships and divergence times, consistent with the previous finding that this large data set is difficult to analyse with a Bayesian relaxed clock without fixing the topology1. Syst. For the latter (Bayesian rjMCMC), we also report the 95% CI for the probability of the state. Jahrb. We thank Ursula Schachner for help in organizing this event; Ralf Buchner for set-up of the eFLOWER server; and Purificacin Lpez-Garca, Susanne Renner and Erik Smets for critical input on an earlier draft of this paper. In particular, this scenario implies that the two perianth whorls of Monocotyledoneae could be homologous with the corolla (inner perianth whorl) of Pentapetalae (Fig. Proc. PubMed PubMedGoogle Scholar. Most of these approaches are imprecise and lend themselves to multiple interpretations. However, some groups and relationships have been rearranged as a result of DNA analysis. Nat. In several cases, these CIs are very wide, with probabilities ranging from ca. 1 INTRODUCTION Gymnosperms are an ancient and widespread nonflowering plant lineage of great economic and ecological importance. J. Endress, P. K. Angiosperm floral evolution: morphological developmental framework. The origin of the angiosperm flower remains among the most difficult and most important unresolved topics in evolutionary biology4,6,7,8,9,10,11. The roughly 200 million years between the appearance of the gymnosperms and the flowering plants gives us some appreciation for the evolutionary experimentation that ultimately produced flowers and fruit. Thus, our sample is independent from the floral traits. As for single-trait analyses, the ancestral states reconstructed using this approach integrate over model, parameter, tree and dating uncertainty, as measured by the CIs associated with the probability (proportional likelihood) of each state (Supplementary Data 2). S.M. Am. 1. Some may be carried away by the wind. 115, 895914 (2015). In spite of similarities with some extant flowers, there is no living species that shares this exact combination of characters. Posada, D. & Buckley, T. R. Model selection and model averaging in phylogenetics: advantages of Akaike Information Criterion and Bayesian approaches over likelihood ratio tests. The relationship between pollinator and flower characteristics is one of the great examples of coevolution. Ruhfel, B. R., Gitzendanner, M. A., Soltis, P. S., Soltis, D. E. & Burleigh, J. G. From algae to angiospermsinferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. The key assumption is that genes for essential proteins or RNA structures, such as the ribosomal RNA, are inherently conserved because mutations (changes in the DNA sequence) could compromise the survival of the organism. 181, 120 (2016). Crane, P. R., Friis, E. M. & Pedersen, K. R. The origin and early diversification of angiosperms. wrote the first draft of the paper, with subsequent contributions from most coauthors. Flower development in angiosperms is regulated by the family of MADS-box transcription factors. Sci. Botanists studying fossil plants are therefore always on the lookout for reproductive structures bearing carpels when collecting fossil plants from rock exposures. However, most sequenced plant mitochondrial genomes (mitogenomes) have been generated for angiosperms, whereas mitogenomic sequences have been generated for only six gymnosperms. Soc. PubMed Nature Communications (Nat Commun) Describe the significance of angiosperms bearing both flowers and fruit. Species are found at the tips of the branches. . Our strict exemplar approach also means that data are missing for some traits in some species (total missing data: 27%, including cases of inapplicability). Megaspores made in cones develop into the female gametophytes inside the ovules of gymnosperms, while pollen grains develop from cones that produce microspores. We propose that early reduction in the number of whorls of ancestral flowers presented selective advantages that eventually led to the extinction of its original, multiparted floral groundplan. Conservation of class C function of floral organ development during 300 million years of evolution from gymnosperms to angiosperms Plant J. Endress, P. K. Floral phyllotaxis and floral evolution. Don't want to keep filling in name and email whenever you want to comment? USA 111, E4859E4868 (2014). All living organisms display patterns of relationships derived from their evolutionary history. Thus, the evolution that produced the plants which were eventually recognized as the angiosperms must have been taking place during the . The colours, shapes and relative sizes of organs were not inferred from our analyses and were chosen here for artistic reasons. In particular, the structure of the ancestral flower of all living angiosperms is still uncertain. Proc. 169, 816843 (2008). This leaf imprint shows a Ficus speciosissima, an angiosperm that flourished during the Cretaceous period. We here report the ML results from the best-fit model. Unbalanced disparity among flower functional modules and a mosaic pattern of morphospace occupation in the order Ericales. Floral traits were recorded from a diversity of published and online sources, including many focused morphological studies and a few personal observations. The Gnetales includes three morphologically isolated genera . Based on fieldwork in 13 countries over 6 years, the duo examined the venation of 504 flowering plants and 225 other plants, including 166 extinct species, and looked for trends in venation patterns through time. Because missing or inapplicable data are more or less evenly and haphazardly distributed across our tree, and species with such data are in effect pruned out in the ancestral reconstruction analyses, it is unlikely that missing data had a strong impact on our results. However, model-based methods (ML and Bayesian) resolve some long-standing questions where parsimony continues to give equivocal answers. In the meantime, to ensure continued support, we are displaying the site without styles Am. Therefore, although there is a probable time lag in fossil preservation of the earliest angiosperm lineages, the sequence of origin of floral traits in the fossil record is largely consistent with our reconstructed initial stages of floral evolution. In the E series, we constrained Chloranthaceae and Ceratophyllaceae to be sister taxa46,47. Get the most important science stories of the day, free in your inbox. 164, S329S363 (2003). Article in. However, it should be possible to quantify this uncertainty. Following fertilization of the egg, the ovule grows into a seed. First, both the protective function of the perianth and its role in pollinator attraction could be achieved through fewer organ whorls, potentially explaining the progressive loss or merging of whorls. Endress, P. K. & Doyle, J. Syst. Theissen, G. & Melzer, R. Molecular mechanisms underlying origin and diversification of the angiosperm flower. Sci. Preprint at http://beast.bio.ed.ac.uk/Tracer (2014). As a complete contrast to this situation the flowering plants, the angiosperms, always have definite containers for their seeds such as poppy capsules or pea pods. provided support for the Summer School and continued development of the eFLOWER project. The third approach, which we apply here using a massive new data set and state-of-the-art analytical methods, is to infer the structure of ancestral flowers using the distribution of floral traits among extant angiosperms, the latest estimates of their phylogeny and models of morphological evolution. Preprint at http://eflower.myspecies.info/proteus (2016). Yet, the origin and early evolution of their most characteristic feature, the flower, remains poorly understood. 207, 437453 (2015). Ser. Syst. Biol. The earliest seedlike bodies are found in rocks of the Upper Devonian Series (about 382.7 million to 358.9 million years ago). Ann. It is always recommended to visit an institution's official website for more information. Ann. 66). The complete list of records and linked sources (references) is available in Supplementary Data 13. Annu. For this study, we transformed the trees of hybrid terminal taxa into trees of species by choosing the species with the most genes sampled for each hybrid (genus-level) terminal taxon. If material is not included in the articles Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. All new phylogenetic and molecular dating analyses were conducted with BEAST 1.8 (ref. Google Scholar. The surrounding tissues of the ovary thicken, developing into a fruit that will protect the seed and often ensure its dispersal over a wide geographic range.