P. K. Endress, C. C. Davis, and M. L. Matthews. 2013. “
Advances in the floral structural characterization of the major subclades of Malpighiales, one of the largest orders of flowering plants.” Ann Bot, 111, Pp. 969-85.
AbstractBACKGROUND AND AIMS: Malpighiales are one of the largest angiosperm orders and have undergone radical systematic restructuring based on molecular phylogenetic studies. The clade has been recalcitrant to molecular phylogenetic reconstruction, but has become much more resolved at the suprafamilial level. It now contains so many newly identified clades that there is an urgent need for comparative studies to understand their structure, biology and evolution. This is especially true because the order contains a disproportionally large diversity of rain forest species and includes numerous agriculturally important plants. This study is a first broad systematic step in this endeavour. It focuses on a comparative structural overview of the flowers across all recently identified suprafamilial clades of Malpighiales, and points towards areas that desperately need attention. METHODS: The phylogenetic comparative analysis of floral structure for the order is based on our previously published studies on four suprafamilial clades of Malpighiales, including also four related rosid orders (Celastrales, Crossosomatales, Cucurbitales, Oxalidales). In addition, the results are compiled from a survey of over 3000 publications on macrosystematics, floral structure and embryology across all orders of the core eudicots. KEY RESULTS: Most new suprafamilial clades within Malpighiales are well supported by floral structural features. Inner morphological structures of the gynoecium (i.e. stigmatic lobes, inner shape of the locules, placentation, presence of obturators) and ovules (i.e. structure of the nucellus, thickness of the integuments, presence of vascular bundles in the integuments, presence of an endothelium in the inner integument) appear to be especially suitable for characterizing suprafamilial clades within Malpighiales. CONCLUSIONS: Although the current phylogenetic reconstruction of Malpighiales is much improved compared with earlier versions, it is incomplete, and further focused phylogenetic and morphological studies are needed. Once all major subclades of Malpighiales are elucidated, more in-depth studies on promising structural features can be conducted. In addition, once the phylogenetic tree of Malpighiales, including closely related orders, is more fully resolved, character optimization studies will be possible to reconstruct evolution of structural and biological features within the order.
PDF William R. Anderson and Charles C. Davis. 2013. “
Combination of Mascagnia and Triopterys (Malpighiaceae).” In Memoirs of the New York Botanical Garden. Harmony and Grit: papers celebrating the Holmgrens' completion of Intermountain Flora, Pp. 191-203.
PDF B. R. Ruhfel, P. Stevens, and C. C. Davis. 2013. “
Combined morphological and molecular phylogeny of the clusioid clade (Malpighiales) and the placement of the ancient rosid macrofossil Paleoclusia.” Int J Plant Sci, 174, Pp. 910-936.
AbstractPremise of research. The clusioid clade is a member of the large rosid order Malpighiales and contains ∼1900 species in five families: Bonnetiaceae, Calophyllaceae, Clusiaceae sensu stricto (s.s.), Hypericaceae, and Podostemaceae. Despite recent efforts to clarify their phylogenetic relationships using molecular data, no such data are available for several critical taxa, including especially Hypericum ellipticifolium (previously recognized in Lianthus), Lebrunia, Neotatea, Thysanostemon, and the second-oldest rosid fossil (∼90 Ma), Paleoclusia chevalieri. Here, we (i) assess congruence between phylogenies inferred from morphological and molecular data, (ii) analyze morphological and molecular data simultaneously to place taxa lacking molecular data, and (iii) use ancestral state reconstructions (ASRs) to examine the evolution of traits that have been important for circumscribing clusioid taxa and to explore the placement of Paleoclusia. Methodology. We constructed a morphological data set including 69 characters and 81 clusioid species (or species groups). These data were analyzed individually and in combination with a previously published molecular data set of four genes (plastid matK, ndhF, and rbcL and mitochondrial matR) using parsimony, maximum likelihood (ML), and Bayesian inference. We used ML ASRs to infer the evolution of morphological characters. Pivotal results. Our phylogeny inferred from morphology alone was poorly supported but largely in agreement with molecular data. Moreover, our combined analyses were much better supported and largely confirm taxonomic hypotheses regarding relationships of extant taxa newly included here. The extinct Paleoclusia was placed as a member of stem group Clusiaceae s.s. or within crown group Clusiaceae s.s. as sister to one of its two major subclades. Conclusions. Despite poor overall bootstrap support for the placement of Paleoclusia, ancestral character state reconstructions are generally in agreement with our placements. Our recommendation is that Paleoclusia be treated as either a minimum stem group or a crown group age constraint of Clusiaceae s.s. Keywords: Clusiaceae, combined analysis, Guttiferae, morphology, Paleoclusia, rosids. Online enhancements: appendixes, figures, supplementary table.
PDF E. G. DeChaine, B. R. Forester, H. Schaefer, and C. C. Davis. 2013. “
Deep genetic divergence between disjunct Refugia in the Arctic-Alpine King's Crown, Rhodiola integrifolia (Crassulaceae).” PLoS One, 8, Pp. e79451.
AbstractDespite the strength of climatic variability at high latitudes and upper elevations, we still do not fully understand how plants in North America that are distributed between Arctic and alpine areas responded to the environmental changes of the Quaternary. To address this question, we set out to resolve the evolutionary history of the King's Crown, Rhodiola integrifolia using multi-locus population genetic and phylogenetic analyses in combination with ecological niche modeling. Our population genetic analyses of multiple anonymous nuclear loci revealed two major clades within R. integrifolia that diverged from each other ~ 700 kya: one occurring in Beringia to the north (including members of subspecies leedyi and part of subspecies integrifolia), and the other restricted to the Southern Rocky Mountain refugium in the south (including individuals of subspecies neomexicana and part of subspecies integrifolia). Ecological niche models corroborate our hypothesized locations of refugial areas inferred from our phylogeographic analyses and revealed some environmental differences between the regions inhabited by its two subclades. Our study underscores the role of geographic isolation in promoting genetic divergence and the evolution of endemic subspecies in R. integrifolia. Furthermore, our phylogenetic analyses of the plastid spacer region trnL-F demonstrate that among the native North American species, R. integrifolia and R. rhodantha are more closely related to one another than either is to R. rosea. An understanding of these historic processes lies at the heart of making informed management decisions regarding this and other Arctic-alpine species of concern in this increasingly threatened biome.
PDF L. A. Nikolov, P. K. Endress, M. Sugumaran, S. Sasirat, S. Vessabutr, E. M. Kramer, and C. C. Davis. 2013. “
Developmental origins of the world's largest flowers, Rafflesiaceae.” Proc Natl Acad Sci U S A, 110, Pp. 18578-83.
AbstractRafflesiaceae, which produce the world's largest flowers, have captivated the attention of biologists for nearly two centuries. Despite their fame, however, the developmental nature of the floral organs in these giants has remained a mystery. Most members of the family have a large floral chamber defined by a diaphragm. The diaphragm encloses the reproductive organs where pollination by carrion flies occurs. In lieu of a functional genetic system to investigate floral development in these highly specialized holoparasites, we used comparative studies of structure, development, and gene-expression patterns to investigate the homology of their floral organs. Our results surprisingly demonstrate that the otherwise similar floral chambers in two Rafflesiaceae subclades, Rafflesia and Sapria, are constructed very differently. In Rafflesia, the diaphragm is derived from the petal whorl. In contrast, in Sapria it is derived from elaboration of a unique ring structure located between the perianth and the stamen whorl, which, although developed to varying degrees among the genera, appears to be a synapomorphy of the Rafflesiaceae. Thus, the characteristic features that define the floral chamber in these closely related genera are not homologous. These differences refute the prevailing hypothesis that similarities between Sapria and Rafflesia are ancestral in the family. Instead, our data indicate that Rafflesia-like and Sapria-like floral chambers represent two distinct derivations of this morphology. The developmental repatterning we identified in Rafflesia, in particular, may have provided architectural reinforcement, which permitted the explosive growth in floral diameter that has arisen secondarily within this subclade.
PDF W. Zhang, V. W. Steinmann, L. Nikolov, E. M. Kramer, and C. C. Davis. 2013. “
Divergent genetic mechanisms underlie reversals to radial floral symmetry from diverse zygomorphic flowered ancestors.” Front Plant Sci, 4, Pp. 302.
AbstractMalpighiaceae possess flowers with a unique bilateral symmetry (zygomorphy), which is a hypothesized adaptation associated with specialization on neotropical oil bee pollinators. Gene expression of two representatives of the CYC2 lineage of floral symmetry TCP genes, CYC2A and CYC2B, demarcate the adaxial (dorsal) region of the flower in the characteristic zygomorphic flowers of most Malpighiaceae. Several clades within the family, however, have independently lost their specialized oil bee pollinators and reverted to radial flowers (actinomorphy) like their ancestors. Here, we investigate CYC2 expression associated with four independent reversals to actinomorphy. We demonstrate that these reversals are always associated with alteration of the highly conserved CYC2 expression pattern observed in most New World (NW) Malpighiaceae. In NW Lasiocarpus and Old World (OW) Microsteria, the expression of CYC2-like genes has expanded to include the ventral region of the corolla. Thus, the pattern of gene expression in these species has become radialized, which is comparable to what has been reported in the radial flowered legume clade Cadia. In striking contrast, in NW Psychopterys and OW Sphedamnocarpus, CYC2-like expression is entirely absent or at barely detectable levels. This is more similar to the pattern of CYC2 expression observed in radial flowered Arabidopsis. These results collectively indicate that, regardless of geographic distribution, reversals to similar floral phenotypes in this large tropical angiosperm clade have evolved via different genetic changes from an otherwise highly conserved developmental program.
PDF S. C. Cappellari, H. Schaefer, and C. C. Davis. 2013. “
Evolution: pollen or pollinators - which came first?” Curr BiolCurr Biol, 23, Pp. R316-8.
AbstractA new study provides the first broad timeline of bee diversification. Several ancient bee clades are identified as ghost lineages that have left little fossil evidence of their existence. This timeline suggests that the rise of bees coincided with the largest flowering plant clade, the eudicots.
PDF Z. Xi, Y. Wang, R. K. Bradley, M. Sugumaran, C. J. Marx, J. S. Rest, and C. C. Davis. 2013. “
Massive mitochondrial gene transfer in a parasitic flowering plant clade.” PLoS Genet, 9, 2, Pp. e1003265.
AbstractRecent studies have suggested that plant genomes have undergone potentially rampant horizontal gene transfer (HGT), especially in the mitochondrial genome. Parasitic plants have provided the strongest evidence of HGT, which appears to be facilitated by the intimate physical association between the parasites and their hosts. A recent phylogenomic study demonstrated that in the holoparasite Rafflesia cantleyi (Rafflesiaceae), whose close relatives possess the world's largest flowers, about 2.1% of nuclear gene transcripts were likely acquired from its obligate host. Here, we used next-generation sequencing to obtain the 38 protein-coding and ribosomal RNA genes common to the mitochondrial genomes of angiosperms from R. cantleyi and five additional species, including two of its closest relatives and two host species. Strikingly, our phylogenetic analyses conservatively indicate that 24%-41% of these gene sequences show evidence of HGT in Rafflesiaceae, depending on the species. Most of these transgenic sequences possess intact reading frames and are actively transcribed, indicating that they are potentially functional. Additionally, some of these transgenes maintain synteny with their donor and recipient lineages, suggesting that native genes have likely been displaced via homologous recombination. Our study is the first to comprehensively assess the magnitude of HGT in plants involving a genome (i.e., mitochondria) and a species interaction (i.e., parasitism) where it has been hypothesized to be potentially rampant. Our results establish for the first time that, although the magnitude of HGT involving nuclear genes is appreciable in these parasitic plants, HGT involving mitochondrial genes is substantially higher. This may represent a more general pattern for other parasitic plant clades and perhaps more broadly for angiosperms.
PDF Z. Xi, J. S. Rest, and C. C. Davis. 2013. “
Phylogenomics and coalescent analyses resolve extant seed plant relationships.” PLoS One, 8, Pp. e80870.
AbstractThe extant seed plants include more than 260,000 species that belong to five main lineages: angiosperms, conifers, cycads, Ginkgo, and gnetophytes. Despite tremendous effort using molecular data, phylogenetic relationships among these five lineages remain uncertain. Here, we provide the first broad coalescent-based species tree estimation of seed plants using genome-scale nuclear and plastid data By incorporating 305 nuclear genes and 47 plastid genes from 14 species, we identify that i) extant gymnosperms (i.e., conifers, cycads, Ginkgo, and gnetophytes) are monophyletic, ii) gnetophytes exhibit discordant placements within conifers between their nuclear and plastid genomes, and iii) cycads plus Ginkgo form a clade that is sister to all remaining extant gymnosperms. We additionally observe that the placement of Ginkgo inferred from coalescent analyses is congruent across different nucleotide rate partitions. In contrast, the standard concatenation method produces strongly supported, but incongruent placements of Ginkgo between slow- and fast-evolving sites. Specifically, fast-evolving sites yield relationships in conflict with coalescent analyses. We hypothesize that this incongruence may be related to the way in which concatenation methods treat sites with elevated nucleotide substitution rates. More empirical and simulation investigations are needed to understand this potential weakness of concatenation methods.
PDF E. R. Ellwood, S. A. Temple, R. B. Primack, N. L. Bradley, and C. C. Davis. 2013. “
Record-breaking early flowering in the eastern United States.” PLoS One, 8, Pp. e53788.
AbstractFlowering times are well-documented indicators of the ecological effects of climate change and are linked to numerous ecosystem processes and trophic interactions. Dozens of studies have shown that flowering times for many spring-flowering plants have become earlier as a result of recent climate change, but it is uncertain if flowering times will continue to advance as temperatures rise. Here, we used long-term flowering records initiated by Henry David Thoreau in 1852 and Aldo Leopold in 1935 to investigate this question. Our analyses demonstrate that record-breaking spring temperatures in 2010 and 2012 in Massachusetts, USA, and 2012 in Wisconsin, USA, resulted in the earliest flowering times in recorded history for dozens of spring-flowering plants of the eastern United States. These dramatic advances in spring flowering were successfully predicted by historical relationships between flowering and spring temperature spanning up to 161 years of ecological change. These results demonstrate that numerous temperate plant species have yet to show obvious signs of physiological constraints on phenological advancement in the face of climate change.
PDF E. M. Wolkovich, T. J. Davies, H. Schaefer, E. E. Cleland, B. I. Cook, S. E. Travers, C. G. Willis, and C. C. Davis. 2013. “
Temperature-dependent shifts in phenology contribute to the success of exotic species with climate change.” Am J Bot, 100, Pp. 1407-1421.
AbstractPREMISE OF THE STUDY: The study of how phenology may contribute to the assembly of plant communities has a long history in ecology. Climate change has brought renewed interest in this area, with many studies examining how phenology may contribute to the success of exotic species. In particular, there is increasing evidence that exotic species occupy unique phenological niches and track climate change more closely than native species. METHODS: Here, we use long-term records of species' first flowering dates from fi ve northern hemisphere temperate sites (Chinnor, UK and in the United States, Concord, Massachusetts; Fargo, North Dakota; Konza Prairie, Kansas; and Washington,D.C.) to examine whether invaders have distinct phenologies. Using a broad phylogenetic framework, we tested for differences between exotic and native species in mean annual flowering time, phenological changes in response to temperature and precipitation,and longer-term shifts in first flowering dates during recent pronounced climate change ("flowering time shifts"). KEY RESULTS: Across North American sites, exotic species have shifted flowering with climate change while native species, on average, have not. In the three mesic systems, exotic species exhibited higher tracking of interannual variation in temperature,such that flowering advances more with warming, than native species. Across the two grassland systems, however, exotic species differed from native species primarily in responses to precipitation and soil moisture, not temperature. CONCLUSIONS: Our findings provide cross-site support for the role of phenology and climate change in explaining species' invasions.Further, they support recent evidence that exotic species may be important drivers of extended growing seasons observed with climate change in North America.
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