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Publications

2020
Daniel S. Park, Charles G. Willis, Zhenxiang Xi, John T. Kartesz, Charles C. Davis, and Steven Worthington. 4/27/2020. “Machine learning predicts large scale declines in native plant phylogenetic diversity.” New Phytologist. PDF
Charles Davis, Goia Lyra, Caio Silva, Mariana Guimarães, Jean Wyllys, and Aaron Ellison. 4/17/2020. “As mídias sociais inflamam a destuição da Amazônia.” Estadão Política. PDF
Joel H. Nitta, James E. Watkins, and Charles C. Davis. 4/14/2020. “Life in the canopy: community trait assessments reveal substantial functional diversity among fern epiphytes.” New Phytologist. PDF
Charles Davis, Goia Lyra, Caio Silva, Mariana Guimarães, Jean Wyllys, and Aaron Ellison. 4/14/2020. “Social media are fueling the Amazon's destruction.” Nature, 580, 7803, Pp. 321. Publisher's Version
Rebecca A. Povilus, Jeffrey M. DaCosta, Christopher Grassa, Prasad R. V Satyaki, Morgan Moeglein, Johan Jaenisch, Zhenxiang Xi, Sarah Mathews, Mary Gehring, Charles C. Davis, and William E. Friedman. 4/14/2020. “Water lily (Nymphaea thermarum) genome reveals variable genomic signatures of ancient vascular cambium losses.” PNAS, 117, 15, Pp. 8649-8656.Abstract
For more than 225 million y, all seed plants were woody trees, shrubs, or vines. Shortly after the origin of angiosperms ∼140 million y ago (MYA), the Nymphaeales (water lilies) became one of the first lineages to deviate from their ancestral, woody habit by losing the vascular cambium, the meristematic population of cells that produces secondary xylem (wood) and phloem. Many of the genes and gene families that regulate differentiation of secondary tissues also regulate the differentiation of primary xylem and phloem, which are produced by apical meristems and retained in nearly all seed plants. Here, we sequenced and assembled a draft genome of the water lily Nymphaea thermarum, an emerging system for the study of early flowering plant evolution, and compared it to genomes from other cambium-bearing and cambium-less lineages (e.g., monocots and Nelumbo). This revealed lineage-specific patterns of gene loss and divergence. Nymphaea is characterized by a significant contraction of the HD-ZIP III transcription factors, specifically loss of REVOLUTA, which influences cambial activity in other angiosperms. We also found the Nymphaea and monocot copies of cambium-associated CLE signaling peptides display unique substitutions at otherwise highly conserved amino acids. Nelumbo displays no obvious divergence in cambium-associated genes. The divergent genomic signatures of convergent loss of vascular cambium reveals that even pleiotropic genes can exhibit unique divergence patterns in association with independent events of trait loss. Our results shed light on the evolution of herbaceousness—one of the key biological innovations associated with the earliest phases of angiosperm evolution.
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Brandon Hedrick, Mason Heberling, Emily Meineke, Kathryn Turner, Christopher Grassa, Daniel Park, Jonathan Kennedy, Julia A. Clarke, Joseph Cook, David Blackburn, Scott V. Edwards, and Charles C. Davis. 3/1/2020. “Digitization and the future of natural history collections.” BioScience, 70, 3, Pp. 243-251. Publisher's VersionAbstract
Natural history collections (NHCs) are the foundation of historical baselines for assessing anthropogenic impacts on biodiversity. Along these lines, the online mobilization of specimens via digitization–the conversion of specimen data into accessible digital content–has greatly expanded the use of NHC collections across a diversity of disciplines. We broaden the current vision of digitization (Digitization 1.0)–whereby specimens are digitized within NHCs–to include new approaches that rely on digitized products rather than the physical specimen (Digitization 2.0). Digitization 2.0 builds upon the data, workflows, and infrastructure produced by Digitization 1.0 to create digital-only workflows that facilitate digitization, curation, and data linkages, thus returning value to physical specimens by creating new layers of annotation, empowering a global community, and developing automated approaches to advance biodiversity discovery and conservation. These efforts will transform large-scale biodiversity assessments to address fundamental questions including those pertaining to critical modern issues of global change.
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Jianquan Liu, Charles C Davis, Xiyin Wang, Zhenxiang Xi, Zhiji Qin, Qinfeng Wang, Man Liu, Lanxing Shan, Beibei Jiao, Fanbo Meng, Xingxing Shen, Lei Zhang, Tao Ma, Ying Li, Dafu Ru, Donglei Wang, Leke Lv, Pengchuan Sun, and Yongzhi Yang. 2/24/2020. “Prickly waterlily and rigid hornwort genomes shed light on early angiosperm evolution.” Nature Plants, 2020, Pp. 1-8.Abstract
Angiosperms represent one of the most spectacular terrestrial radiations on the planet 1, but their early diversification and phylogenetic relationships remain uncertain 2, 3, 4, 5. A key reason for this impasse is the paucity of complete genomes representing early-diverging angiosperms. Here, we present high-quality, chromosomal-level genome assemblies of two aquatic species—prickly waterlily (Euryale ferox; Nymphaeales) and the rigid hornwort (Ceratophyllum demersum; Ceratophyllales)—and expand the genomic representation for key sectors of the angiosperm tree of life. We identify multiple independent polyploidization events in each of the five major clades (that is, Nymphaeales, magnoliids, monocots, Ceratophyllales and eudicots). Furthermore, our phylogenomic analyses, which spanned multiple datasets and diverse methods, confirm that Amborella and Nymphaeales are successively sister to all other …
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Xiaoqing Liu, Weirui Fu, Yiwei Tang, Wenju Zhang, Zhiping Soonog, Linfeng Li, Ji Yang, Hong Ma, Jianhua Yang, Chan Zhou, Charles C. Davis, and Yugu Wang. 1/23/2020. “Diverse trajectories of plastome degradation in holoparasitic Cistanche and the whereabouts of the lost plastid genes.” Journal of Experimental Botany, 71, 3, Pp. 877-892. Publisher's VersionAbstract
The plastid genomes (plastomes) of non-photosynthetic plants generally undergoes gene loss and pseudogenization. Despite massive plastomes reported in different parasitism types of the broomrape family (Orobanchaceae), more plastomes representing different degradation patterns in a single genus are expected to be explored. Here, we sequenced and assembled the complete plastomes of three holoparasitic Cistanche species (C. salsa, C. tubulosa and C. sinensis) and compared them with the available plastomes of Orobanchaceae. We identified that the diverse degradation trajectories under purifying selection existed among three Cistanche clades, showing obvious size differences on entire plastome, long single copy region and non-coding region, and different patterns of the retention/loss of functional genes. With few exception of putatively functional genes, massive plastid fragments which have been lost and transferred into the mitochondrial or nuclear genomes are nonfunctional. In contrast with the equivalents of the Orobanche species, some plastid-derived genes with diverse genomic locations are found in Cistanche. The early and initially diverged clades in different genera such as Cistanche and Aphyllon possess obvious patterns of plastome degradation, suggesting that such key lineages should be considered prior to comparative analysis of plastome evolution, especially in the same genus.
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Charles C Davis, Benjamin Goulet-Scott, and Jason Beckfield. 1/21/2020. “Climate Change: How to Pack a Punch at Meetings.” Nature, 577, 7791, Pp. 472. PDF
2019
Emily K Meineke, Charles C Davis, and Jonathan T Davies. 11/20/2019. “Herbivory through the ages: Herbarium specimens for determining effects of plant traits on changing insect damage to plants.” Entomology 11/20/2019. Abstract
Some of the most consequential interactions expected to shift with climate change are between insect herbivores and plants, both of which are highly sensitive to temperature. Historically, insect herbivores and their host plants display varying levels of synchrony that could be disrupted or enhanced by climate change. Here, we use herbarium specimens collected over the past 100+ years to explore how phenological sensitivity, bloom/leaf-out season, and plant growth form affect changing insect damage to leaves. Our results suggest that warming may lengthen growing seasons for phenologically sensitive species, exposing them to more damage from resident or novel herbivores early in the growing season.
Ricardo A. Segovia, Toby Pennington, Tim Baker, Fernanda Coelho de Souza, Danilo Neves, Charles C. Davis, Juan J. Armesto, Ary Olivera-Filho, and Kyle Dexter. 8/9/2019. “Freezing and water availability structure the evolutionary diversity of trees across the Americas.” bioRxiv, Pp. 728717. Publisher's Version PDF
Lucas Marinho, Liming Cai, Xiaoshan Duan, Brad R. Ruhfel, Pedro Fiaschi, André M. Amorim, Cássio van den Berg, and Charles C. Davis. 5/1/2019. “Plastomes resolve generic limits within tribe Clusieae (Clusiaceae) and reveal the new genus Arawakia.” Molecular Phylogenetics and Evolution, 134, Pp. 142-151. Publisher's VersionAbstract
Clusieae is an exclusively Neotropical tribe in the family Clusiaceae sensu stricto. Although tribes within Clusiaceae are morphologically and phylogenetically well-delimited, resolution among genera within these tribes remains elusive. The tribe Clusieae includes an estimated ∼500 species distributed among five genera: Chrysochlamys, Clusia, Dystovomita, Tovomita, and Tovomitopsis. In this study, we used nearly complete plastid genomes from 30 exemplar Clusieae species representing all genera recognized, plus two outgroups to infer the phylogeny of the tribe using Maximum Likelihood and Bayesian Inference. For comparison, we also inferred a phylogeny from the nuclear Internal Transcribed Spacer (ITS) region using the same methods. Our study corroborates earlier findings that Clusia is monophyletic while Tovomita is not. It also provides additional support to the hypothesis that Chrysochlamys and Tovomitopsis are not closely related despite gross morphological similarity. Tovomita is divided into three distantly related clades: (i) core Tovomita (including the type T. guianensis), (ii) T. croatii, and (iii) the T. weddelliana species complex. Members of the T. weddelliana complex are isolated from the core Tovomita, and placed in a well-supported clade that is sister to a clade composed of Chrysochlamys plus Clusia. Tovomita croatii is nested within Chrysochlamys. We propose taxonomic revisions to accommodate our phylogenetic findings, including the description of the new genus Arawakia, which includes the 18 species formerly recognized in the T. weddelliana species complex. Lectotypes are also designated for nine species (i.e., Arawakia angustata, A. lanceolata, A. lingulata, A. longicuneata, A. macrocarpa, A. oblanceolata, A. pithecobia, A. rhizophoroides, and A. weddelliana), and a taxonomic key for the identification of the six genera of Clusieae recognized is presented.
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Charles C. Davis and Sarah Matthews. 4/24/2019. “Evolution of Land Plants.” Oxford Bibliographies. Publisher's Version PDF
William D. Pearse, Charles C. Davis, David W. Inouye, RIchard B. Primack, and T. Jonathan Davis. 3/2019. “[Author Correction] A statistical estimator for determining the limits of contemporary and historic phenology.” Nature Ecology & Evolution, 3, 3, Pp. 499. Publisher's Version PDF
Liming Cai, André M. Amorim, Sugumaran Manickam, Liang Liu, Joshua S. Rest, and Charles C. Davis. 2/28/2019. “Thrive with Additional Sets of Genome: Widespread Paleopolyploidization Buffers plants Through Eocene Climatic Upheaval.” Oxford University Press 59, Pp. E29-E29.
Emily K Meineke, Jonathan T Davies, Barnabas H Daru, and Charles C Davis. 1/7/2019. “Biological Collections for understanding biodiversity in the Anthropocene.” Philosophical Transactions of the Royal Society B, 374, 1763, Pp. 20170386.Abstract
Global change has become a central focus of modern biology. Yet, our knowledge of how anthropogenic drivers affect biodiversity and natural resources is limited by a lack of biological data spanning the Anthropocene. We propose that the hundreds of millions of plant, fungal and animal specimens deposited in natural history museums have the potential to transform the field of global change biology. We suggest that museum specimens are underused, particularly in ecological studies, given their capacity to reveal patterns that are not observable from other data sources. Increasingly, museum specimens are becoming mobilized online, providing unparalleled access to physiological, ecological and evolutionary data spanning decades and sometimes centuries. Here, we describe the diversity of collections data archived in museums and provide an overview of the diverse uses and applications of these data as …
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Rebecca A Povilus, Jeffery M DaCosta, Christopher Grassa, Prasad RV Satyaki, Morgan Moeglein, Johan Jaenisch, Zhenxiang Xi, Sarah Mathews, Mary Gehring, Charles C Davis, and William E Friedman. 1/1/2019. “Water lily (Nymphaea thermarum) draft genome reveals variable genomic signatures of ancient vascular cambium losses.” bioRxiv.Abstract
For more than 225 million years, all seed plants were woody trees, shrubs, or vines (1,2,3,4). Shortly after the origin of angiosperms ~135 million years ago (MYA) (5), the Nymphaeales (water lilies) became one of the first lineages to deviate from their ancestral, woody habit by losing the vascular cambium (6), the meristematic population of cells that produces secondary xylem (wood) and phloem. Many of the genes and gene families that regulate differentiation of secondary tissues also regulate the differentiation of primary xylem and phloem (7,8,9), which are produced by apical meristems and retained in nearly all seed plants. Here we sequence and assemble a draft genome of the water lily Nymphaea thermarum, an emerging system for the study of early flowering plant evolution, and compare it to genomes from other cambium-bearing and cambium-less lineages (like monocots and Nelumbo). This reveals lineage-specific patterns of gene loss and divergence. Nymphaea is characterized by a significant contraction of the HD-ZIP III transcription factors, specifically loss of REVOLUTA, which influences cambial activity in other angiosperms. We also find the Nymphaea and monocot copies of cambium-associated CLE signaling peptides display unique substitutions at otherwise highly conserved amino acids. Nelumbo displays no obvious divergence in cambium-associated genes. The divergent genomic signatures of convergent vascular cambium loss reveals that even pleiotropic genes can exhibit unique divergence patterns in association with independent trait loss events. Our results shed light on the evolution of herbaceousness,which is one …
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Liming Cai, Zhenziang Xi, André M Amorim, Manickam Sugumaran, Joshua S. Rest, Liang Liu, and Charles C. Davis. 1/1/2019. “Widespread Ancient whole-genome duplications in Malpighiales coincide with Eocene global climatic upheval.” New Phytologist, 221, 1, Pp. 565-576. Publisher's Version PDF
William D. Pearse, Charles C. Davis, David W. Inouye, RIchard B. Primack, and T. Jonathan Davies. 2019. “A statistical estimator for determining the limits of contemporary and historic phenology.” Nature Ecology & Evolution, 3, 3, Pp. 499.
2018
Daniel S. Park, Ian Breckheimer, Alex C. Williams, Edith Law, Aaron M. Ellison, and Charles C. Davis. 11/19/2018. “Herbarium specimens reveal substantial and unexpected variation in phenological sensitivity across the eastern United States.” The Royal Society Publishing, 374, 1763. Publisher's VersionAbstract

Phenology is a key biological trait that can determine an organism's survival and provides one of the clearest indicators of the effects of recent climatic change. Long time-series observations of plant phenology collected at continental scales could clarify latitudinal and regional patterns of plant responses and illuminate drivers of that variation, but few such datasets exist. Here, we use the web tool CrowdCurio to crowdsource phenological data from over 7000 herbarium specimens representing 30 diverse flowering plant species distributed across the eastern United States. Our results, spanning 120 years and generated from over 2000 crowdsourcers, illustrate numerous aspects of continental-scale plant reproductive phenology. First, they support prior studies that found plant reproductive phenology significantly advances in response to warming, especially for early-flowering species. Second, they reveal that fruiting in populations from warmer, lower latitudes is significantly more phenologically sensitive to temperature than that for populations from colder, higher-latitude regions. Last, we found that variation in phenological sensitivities to climate within species between regions was of similar magnitude to variation between species. Overall, our results suggest that phenological responses to anthropogenic climate change will be heterogeneous within communities and across regions, with large amounts of regional variability driven by local adaptation, phenotypic plasticity and differences in species assemblages. As millions of imaged herbarium specimens become available online, they will play an increasingly critical role in revealing large-scale patterns within assemblages and across continents that ultimately can improve forecasts of the impacts of climatic change on the structure and function of ecosystems.

This article is part of the theme issue ‘Biological collections for understanding biodiversity in the Anthropocene’.

park_herbarium_specimens.pdf

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