On the evolutionary history of Ephedra: Cretaceous fossils and extant molecules

Department of Botany, Stockholm University, SE-106 91 Stockholm, Sweden.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 11/2004; 101(47):16571-6. DOI: 10.1073/pnas.0407588101
Source: PubMed


Gnetales comprise three unusual genera of seed plants, Ephedra, Gnetum, and Welwitschia. Their extraordinary morphological diversity suggests that they are survivors of an ancient, more diverse group. Gnetalean antiquity is also supported by fossil data. Dispersed "ephedroid" (polyplicate) pollen first appeared in the Permian >250 million years ago (Myr), and a few megafossils document the presence of gnetalean features in the early Cretaceous. The Cretaceous welwitschioid seedling Cratonia cotyledon dates the split between Gnetum and Welwitschia to before 110 Myr. Ages and character evolution of modern diversity are, however, controversial, and, based on molecular data, it has recently been suggested that Ephedra is very young, only 8-32 Myr. Here, we present data on the evolutionary history of Ephedra. Fossil seeds from Buarcos, Portugal, unequivocally link one type of Cretaceous polyplicate pollen to Ephedra and document that plants with unique characters, including the peculiar naked male gametophyte, were established already in the Early Cretaceous. Clades in our molecular phylogeny of extant species correspond to geographical regions, with African species in a basal grade/clade. The study demonstrates extremely low divergence in both molecular and morphological characters in Ephedra. Features observed in the fossils are present in all major extant clades, showing that modern species have retained unique reproductive characters for >110 million years. A recent origin of modern species of Ephedra would imply that the Cretaceous Ephedra fossils discussed here were members of widespread, now extinct sister lineage(s), and that no morphological innovations characterized the second diversification.

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    • "Primers were newly developed for the present study or obtained from the literature (Table 1). In order to minimise problems with fungal contamination , the nrITS primers used (18SF and 26SR, Rydin & al., 2004) were designed to amplify on most land plants but not on fungi. Double bands were not observed following PCR amplification and double peaks were not observed in the original reading frames of the sequences. "
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    ABSTRACT: Gnetum (Gnetales: Gnetaceae) constitutes an evolutionarily isolated gymnosperm clade, comprising about 40 species that inhabit tropical areas of the world. While its closest living relative, the monotypic Welwitschia, has a well-documented fossil record from the Early Cretaceous, Gnetum-like fossils are rare and poorly understood. The phylogeny of Gnetum has been studied previously but the distant relationship to outgroups and the difficulty of obtaining plant material mean it is not yet fully resolved. Most species are tropical lianas with an angiospermous vegetative habit that are difficult to find and identify. Here a new phylogeny is presented based on nuclear and chloroplast data from 58 Gnetum accessions, representing 27 putative species, and outgroup information from other seed plants. The results provide support for South American species being sister to the remaining species. The two African species constitute a monophyletic group, sister to an Asian clade, within which the two arborescent species of the genus are the earliest diverging. Estimated divergence times indicate, in contrast with previous results, that the major lineages of Gnetum diverged in the Late Cretaceous. This result is obtained regardless of tree prior used in the BEAST analyses (Yule or birth-death). Together these findings suggest a correlation between early divergence events in extant Gnetum and the breakup of Gondwana in the Cretaceous. Compared to the old stem ages of major subclades of Gnetum, crown nodes date to the Cenozoic: the Asian crown group dates to the Cretaceous-Paleogene (K-Pg) boundary, the African crown group to the mid-Paleogene, and the South American crown group to the Paleogene-Neogene boundary. Although dispersal must have contributed to the current distribution of Gnetum, e.g., within South America and from Southeast Asian islands to the East Asian mainland, dispersal has apparently not occurred across major oceans, at least not during the Cenozoic.
    Taxon 05/2015; 64(2):239–253. DOI:10.12705/642.12 · 3.30 Impact Factor
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    • "Th e same low support pattern for the position of these two species has been repeatedly retrieved in previous studies (Ickert-Bond and Wojciechowski 2004, Rydin and Korall 2009, Rydin et al. 2010), with diff erent topological patterns for their phylogenetic position but without strong support for any specifi c position. As in previous studies (Ickert-Bond and Wojciechowski 2004, Rydin et al. 2004, Huang et al. 2005, Wang et al. 2005, Ickert-Bond et al. 2009, Rydin and Korall 2009), the S. Am. species form a monophyletic group with strong support, however, relationships within this clade are not well resolved, probably because of its recent origin or due to incomplete lineage sorting. "
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    ABSTRACT: In this study we selected the New World species of Ephedra to understand the ecological consequences of different dispersal syndromes. The twenty-three species of Ephedra in the New World have a disjunct distribution in North and South American arid and semi-arid habitats, exhibiting three dispersal syndromes related to dispersal by birds, wind and rodents. Using DNA sequence data we inferred phylogenetic relationships and lineage divergence times, and used these estimates to test different ecological assumptions. Using comparative methods we tested for correlations between dispersal syndromes and a set of ecological variables (niche breadth, niche evolution, distributional ranges and niche position). We found that speciation events in the New World coincided with the expansion of arid habitats in this region. We suggest that the bird dispersal syndrome is related with higher rates of climatic niche evolution for all variables used, including aridity index, mean annual temperature and mean annual precipitation. Distribution ranges were correlated with niche breadth, they were however not significantly different between dispersal syndromes. Species inhabiting the extremely arid regions on niche axes had narrower niche breadths. We conclude that species whose seeds are dispersed by birds have colonized a broader set of habitats and that those with wind and rodent dispersal syndromes might have promoted the colonization of more arid environments.
    Ecography 02/2015; 38. DOI:10.1111/ecog.01264 · 4.77 Impact Factor
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    • "In recent decades, numerous Ephedra and Ephedra-like meso- and macrofossils have been reported from the Early Cretaceous of South Europe, Northeast China, Mongolia, North America, and South America [17]–[19], [21]–[23]. Seed mesofossils with in situ pollen were reported from the Early Cretaceous of South Europe (Portugal) and North America [18], [24]. Macrofossils of reproductive shoots or female cones were found in the Early Cretaceous of South America [25], [26], and Mongolia [27], [28] and adjacent Northeast China [17], [19], [21]–[23], [29], [30]. "
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    ABSTRACT: Bracts of female cones of extant gymnosperm Ephedra (Joint fir) are either colorful and fleshy (section Ephedra), or dry-winged and membranous (section Alatae), or dry and coriaceous (section Asarca), which have played a crucial role in long-distance seed dispersal that is responsible for a wide distribution of the genus in semiarid and arid areas of Eurasia, North Africa, North America, and South America. Recent molecular systematic studies on Ephedra have suggested that the fleshy bracts in character evolution may be plesiomorphic relative to the dry, membranous and coriaceous bracts. However, little is known about when the fleshy bracts of Ephedra have made their debut in the geological past. Herein, we describe a novel, fleshy bract-bearing female cone macrofossil from the Early Cretaceous (ca. 120-125 Ma) Yixian Formation in Liaoning, northeastern China. This cone bears three ellipsoid seeds subtended by only one whorl of fleshy bracts. Each seed has a thin outer envelope and an inner integument that extends upward and passes through the opening of the outer envelope, forming a thin and straight micropylar tube. Such a syndrome shows the closest similarity to an extant triovulate species Ephedra intermedia in the section Ephedra, but the latter bears a whorl of terminal fertile bracts and more than one whorl of inferior sterile bracts, and a thick outer envelope. Hence, we establish a new fossil species Ephedra carnosa. Our discovery provides the first direct macrofossil evidence for the previous molecular systematics of Ephedra, implying that the origin of fleshy bracts in Ephedra should not have been later than that of the membranous and coriaceous bracts by at least the Early Cretaceous.
    PLoS ONE 10/2013; 8(1):e53652. DOI:10.1371/journal.pone.0053652 · 3.23 Impact Factor
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