Person: Davis, Charles
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Charles
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Davis, Charles
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Publication Prickly waterlily and rigid hornwort genomes shed light on early angiosperm evolution(Springer Science and Business Media LLC, 2020-02-24) Yang, Yongzhi; Sun, Pengchuan; Lv, Leke; Wang, Donglei; Ru, Dafu; Li, Ying; Ma, Tao; Zhang, Lei; Shen, Xingxing; Meng, Fanbo; Jiao, Beibei; Shan, Lanxing; Liu, Man; Wang, Qingfeng; Qin, Zhiji; Xi, Zhenxiang; Wang, Xiyin; Davis, Charles; Liu, JianquanAngiosperms represent one of the most spectacular terrestrial radiations on the planet, but their early diversification and phylogenetic relationships remain uncertain. A key reason for this impasse is due to the paucity of complete genomes representing early-diverging angiosperms. Here, we present high-quality, chromosomal-level genome assemblies of two species, prickly waterlily (Euryale ferox; Nymphaeales) and the rigid hornwort (Ceratophyllum demersum; Ceratophyllales), thus expanding genomic representation for key sectors of the angiosperm tree of life. We identify multiple independent polyploidization events in each of the five major clades (i.e., Nymphaeales, magnoliids, monocots, Ceratophyllales, and eudicots). In addition, our phylogenomic analyses spanning multiple data sets and diverse methods confirm that Amborella and Nymphaeales are successively sister to all other angiosperms. Furthermore, these genomes help elucidate the relationships among the major subclades within Mesangiospermae, which contain about 350,000 species. In particular, the species-poor lineage Ceratophyllales is supported as sister to eudicots, and monocots and magnoliids are placed as successively sister to Ceratophyllales + eudicots. Finally, our analyses indicate that incomplete lineage sorting may well account for the incongruent placement of magnoliids between nuclear and plastid genomes.Publication The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae)(John Wiley and Sons Inc., 2016) Lagomarsino, Laura P.; Condamine, Fabien L.; Antonelli, Alexandre; Mulch, Andreas; Davis, CharlesSummary The tropical Andes of South America, the world's richest biodiversity hotspot, are home to many rapid radiations. While geological, climatic, and ecological processes collectively explain such radiations, their relative contributions are seldom examined within a single clade.We explore the contribution of these factors by applying a series of diversification models that incorporate mountain building, climate change, and trait evolution to the first dated phylogeny of Andean bellflowers (Campanulaceae: Lobelioideae). Our framework is novel for its direct incorporation of geological data on Andean uplift into a macroevolutionary model.We show that speciation and extinction are differentially influenced by abiotic factors: speciation rates rose concurrently with Andean elevation, while extinction rates decreased during global cooling. Pollination syndrome and fruit type, both biotic traits known to facilitate mutualisms, played an additional role in driving diversification. These abiotic and biotic factors resulted in one of the fastest radiations reported to date: the centropogonids, whose 550 species arose in the last 5 million yr.Our study represents a significant advance in our understanding of plant evolution in Andean cloud forests. It further highlights the power of combining phylogenetic and Earth science models to explore the interplay of geology, climate, and ecology in generating the world's biodiversity.Publication Widespread sampling biases in herbaria revealed from large-scale digitization(Wiley-Blackwell, 2017) Daru, Barnabas; Park, Daniel; Willis, Richard; Barrington, David; Whitfield, Timothy; Seidler, Tristram; Sweeney, Patrick; Foster, David; Ellison, Aaron; Davis, CharlesSUMMARY 1. Non-random collecting practices may bias conclusions drawn from analyses of herbarium records. Recent efforts to fully digitize and mobilize regional floras online offer a timely opportunity to assess commonalities and differences in herbarium sampling biases. 2. We determined spatial, temporal, trait, phylogenetic, and collector biases in ~5 million herbarium records, representing three of the most complete digitized floras of the world: Australia (AU), South Africa (SA), and New England, USA (NE). 3. We identified numerous shared and unique biases among these regions. Shared biases included specimens i) collected close to roads and herbaria; ii) collected more frequently during biological spring and summer; iii) of threatened species collected less frequently; and iv) of close relatives collected in similar numbers. Regional differences included i) over-representation of graminoids in SA and AU and of annuals in AU; and ii) peak collection during the 1910s in NE, 1980s in SA, and 1990s in AU. Finally, in all regions, a disproportionately large percentage of specimens were collected by very few individuals. We hypothesize that these mega-collectors, and along with their associated preferences and idiosyncrasies, shaped patterns of collection bias via ‘founder effects’. 4. Studies using herbarium collections should account for sampling biases, and future collecting efforts should avoid compounding these biases to the extent possible.Publication Phylogenomics and Coalescent Analyses Resolve Extant Seed Plant Relationships(Public Library of Science, 2013) Xi, Zhenxiang; Rest, Joshua S.; Davis, CharlesThe 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.Publication Deep Genetic Divergence between Disjunct Refugia in the Arctic-Alpine King’s Crown, Rhodiola integrifolia (Crassulaceae)(Public Library of Science, 2013) DeChaine, Eric G.; Forester, Brenna R.; Schaefer, Hanno; Davis, CharlesDespite 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.Publication Plastid phylogenomics and green plant phylogeny: almost full circle but not quite there(BioMed Central, 2014) Davis, Charles; Xi, Zhenxiang; Mathews, SarahA study in BMC Evolutionary Biology represents the most comprehensive effort to clarify the phylogeny of green plants using sequences from the plastid genome. This study highlights the strengths and limitations of plastome data for resolving the green plant phylogeny, and points toward an exciting future for plant phylogenetics, during which the vast and largely untapped territory of nuclear genomes will be explored.Publication Pitcher Plants (Sarracenia) Provide a 21st-Century Perspective on Infraspecific Ranks and Interspecific Hybrids: A Modest Proposal for Appropriate Recognition and Usage(The American Society of Plant Taxonomists, 2014) Ellison, Aaron; Davis, Charles; Calie, Patrick J.; Naczi, Robert F.C.The taxonomic use of infraspecific ranks (subspecies, variety, subvariety, form, and subform), and the formal recognition of interspecific hybrid taxa, is permitted by the International Code of Nomenclature for algae, fungi, and plants. However, considerable confusion regarding the biological and systematic merits is caused by current practice in the use of infraspecific ranks, which obscures the meaningful variability on which natural selection operates, and by the formal recognition of those interspecific hybrids that lack the potential for inter-lineage gene flow. These issues also may have pragmatic and legal consequences, especially regarding the legal delimitation and management of Threatened and Endangered Species. A detailed comparison of three contemporary floras highlights the degree to which infraspecific and interspecific variation are treated inconsistently. An in depth analysis of taxonomy of the North American flowering plant genus Sarracenia (Sarraceniaceae) provides an ideal case study illustrating the confusion that can arise from inconsistent and apparently arbitrary designation of infraspecific ranks and hybrid taxa. To alleviate these problems, we propose the abandonment of infraspecific ranks of “variety” and “form”, and discourage naming of sterile interspecific hybrids except for use in the horticultural or agronomic trade. Our recommendations for taxonomic practice are in accord with the objectives proposed in the Systematics Agenda 2000, Systematics Agenda 2020, and the Global Strategy for Plant Conservation.Publication Divergent genetic mechanisms underlie reversals to radial floral symmetry from diverse zygomorphic flowered ancestors(Frontiers Media S.A., 2013) Zhang, Wenheng; Steinmann, Victor W.; Nikolov, Lachezar; Kramer, Elena; Davis, CharlesMalpighiaceae 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.Publication The establishment of Central American migratory corridors and the biogeographic origins of seasonally dry tropical forests in Mexico(Frontiers Media S.A., 2014) Willis, Charles G.; Franzone, Brian; Xi, Zhenxiang; Davis, CharlesBiogeography and community ecology can mutually illuminate the formation of a regional species pool or biome. Here, we apply phylogenetic methods to a large and diverse plant clade, Malpighiaceae, to characterize the formation of its species pool in Mexico, and its occupancy of the seasonally dry tropical forest (SDTF) biome that occurs there. We find that the ~162 species of Mexican Malpighiaceae represent ~33 dispersals from South America beginning in the Eocene and continuing until the Pliocene (~46.4–3.8 Myr). Furthermore, dispersal rates between South America and Mexico show a significant six-fold increase during the mid-Miocene (~23.9 Myr). We hypothesize that this increase marked the availability of Central America as an important corridor for Neotropical plant migration. We additionally demonstrate that this high rate of dispersal contributed substantially more to the phylogenetic diversity of Malpighiaceae in Mexico than in situ diversification. Finally, we show that most lineages arrived in Mexico pre-adapted with regard to one key SDTF trait, total annual precipitation. In contrast, these lineages adapted to a second key trait, precipitation seasonality, in situ as mountain building in the region gave rise to the abiotic parameters of extant SDTF. The timing of this in situ adaptation to seasonal precipitation suggests that SDTF likely originated its modern characteristics by the late Oligocene, but was geographically more restricted until its expansion in the mid-Miocene. These results highlight the complex interplay of dispersal, adaptation, and in situ diversification in the formation of tropical biomes. Our results additionally demonstrate that these processes are not static, and their relevance can change markedly over evolutionary time. This has important implications for understanding the origin of SDTF in Mexico, but also for understanding the temporal and spatial origin of biomes and regional species pools more broadly.Publication Developmental origins of the world's largest flowers, Rafflesiaceae(Proceedings of the National Academy of Sciences, 2013) Nikolov, L. A.; Endress, P. K.; Sugumaran, M.; Sasirat, S.; Vessabutr, S.; Kramer, Elena; Davis, CharlesRafflesiaceae, 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.