Publications

Forthcoming
Emily K. Meineke, Charles C. Davis, and Jonathan Davies. Forthcoming. “The unrealized potential of herbaria for global change biology.” Ecological Monographs, Pp. 1-21.Abstract

 

Plant and fungal specimens in herbaria are becoming primary resources for investigat-

ing how plant phenology and geographic distributions shift with climate change, greatly expanding

inferences across spatial, temporal, and phylogenetic dimensions. However, these specimens contain a

wealth of additional data, including nutrients, defensive compounds, herbivore damage, disease

lesions, and signatures of physiological processes, that capture ecological and evolutionary responses

to the Anthropocene but which are less frequently utilized. Here, we outline the diversity of herbarium

data, global change topics to which they have been applied, and new hypotheses they could inform.

We find that herbarium data have been used extensively to study impacts of climate change and inva-

sive species, but that such data are less commonly used to address other drivers of biodiversity loss,

including habitat conversion, pollution, and overexploitation. In addition, we note that fungal speci-

mens are under-explored relative to vascular plants. To facilitate broader application of plant and fun-

gal specimens in global change research, we consider the limitations of these data and modern

sampling and statistical tools that may be applied to surmount challenges they present. Using a case

study of insect herbivory, we illustrate how novel herbarium data may be employed to test hypotheses

for which few data exist. With the goal of positioning herbaria as hubs for global change research, we

suggest future research directions and curation priorities.

Key words: climate change; extinction; global change; habitat conversion; herbarium; historical data; invasive

species; museum specimens.

 

2020
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. salsaC. 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: ChrysochlamysClusiaDystovomitaTovomita, 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 ClusiaTovomita 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 angustataA. lanceolataA. lingulataA. longicuneataA. macrocarpaA. oblanceolataA. pithecobiaA. 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
Cintia Iha, Christopher J. Grassa, Goia M. de Lyra, Charles C. Davis, Heroen Verbruggen, and Mariana C. Oliveira. 9/12/2018. “Organellar Genomics: A Useful Tool to Study the Evolutionary Relationships and Molecular Evolution in Gracilarilacae (Rhodophyta).” Journal of Phycology, 54, Pp. 775-787. Publisher's VersionAbstract
Gracilariaceae has a worldwide distribution including numerous economically important species. We applied high‐throughput sequencing to obtain organellar genomes (mitochondria and chloroplast) from 10 species of Gracilariaceae and, combined with published genomes, to infer phylogenies and compare genome architecture among species representing main lineages. We obtained similar topologies between chloroplast and mitochondrial genomes phylogenies. However, the chloroplast phylogeny was better resolved with full support. In this phylogeny, Melanthalia intermedia is sister to a monophyletic clade including Gracilaria and Gracilariopsis, which were both resolved as monophyletic genera. Mitochondrial and chloroplast genomes were highly conserved in gene synteny, and variation mainly occurred in regions where insertions of plasmid‐derived sequences (PDS) were found. In mitochondrial genomes, PDS insertions were observed in two regions where the transcription direction changes: between the genes cob and trnL, and trnA and trnN. In chloroplast genomes, PDS insertions were in different positions, but generally found between psdD and rrs genes. Gracilariaceae is a good model system to study the impact of PDS in genome evolution due to the frequent presence of these insertions in organellar genomes. Furthermore, the bacterial leuC/leuD operon was found in chloroplast genomes of Gracilaria tenuistipitata, G. chilensis, and M. intermedia, and in extrachromosomal plasmid of G. vermiculophylla. Phylogenetic trees show two different origins of leuC/leuD: genes found in chloroplast and plasmid were placed with proteobacteria, and genes encoded in the nucleus were close to Viridiplantae and cyanobacteria.
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Daniel S. Park, Aaron M. Ellison, and Charles C. Davis. 7/2018. “Mating system does not predict niche breath.” Global Ecology and Biogeography, 27, 7, Pp. 804-813. Publisher's VersionAbstract
Self‐pollinating plants (‘selfers’) have larger geographical ranges and inhabit higher latitudes than their outcrossing relatives. This finding has led to the hypothesis that selfers also have broader climatic niches (‘niches’) because the increased likelihood of successful colonization into new areas and the initial purging of deleterious mutations could offset the inability of selfers to adapt to new environments owing to low heterozygosity. Here, we examine the niches of hundreds of closely related selfing and outcrossing species to determine whether selfers do indeed have larger niche breadths.
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Joel H. Nitta, Saad Amer, and Charles C. Davis. 6/21/2018. “Microsorum× tohieaense (Polypodiaceae), a New Hybrid Fern from French Polynesia, with Implications for the Taxonomy of Microsorum.” Systematic Botany, 43, 2, Pp. 397-413. Publisher's VersionAbstract
A new hybrid microsoroid fern, Microsorum × tohieaense (Microsorum commutatum × Microsorum membranifolium) from Moorea, French Polynesia is described based on morphology and molecular phylogenetic analysis. Microsorum × tohieaense can be distinguished from other French Polynesian Microsorum by the combination of sori that are distributed more or less in a single line between the costae and margins, apical pinna wider than lateral pinnae, and round rhizome scales with entire margins. Genetic evidence is also presented for the first time supporting the hybrid origin of Microsorum × maximum(Microsorum grossum × Microsorum punctatum), and possibly indicating a hybrid origin for the Hawaiian endemic Microsorum spectrum. The implications of hybridization for the taxonomy of microsoroid ferns are discussed, and a key to the microsoroid ferns of the Society Islands is provided.
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Patrick W. Sweeney, Binil Starly, Paul J. Morris, Yiming Xy, Aimee Jones, Sridhar Radhakrishnan, Christopher J. Grassa, and Charles C. Davis. 6/3/2018. “Large-scale digitization of herbarium specimens: Development and usage of an automated, high-throughput conveyor system.” International Association for Plant Taxonomy, 67, 1, Pp. 165-178. Publisher's VersionAbstract
The billions of specimens housed in natural science collections provide a tremendous source of under-utilized data that are useful for scientific research, conservation, commerce, and education. Digitization and mobilization of specimen data and images promises to greatly accelerate their utilization. While digitization of natural science collection specimens has been occurring for decades, the vast majority of specimens remain un-digitized. If the digitization task is to be completed in the near future, innovative, high-throughput approaches are needed. To create a dataset for the study of global change in New England, we designed and implemented an industrial-scale, conveyor-based digitization workflow for herbarium specimen sheets. The workflow is a variation of an object-to-image-to-data workflow that prioritizes imaging and the capture of storage container-level data. The workflow utilizes a novel conveyor system developed specifically for the task of imaging flattened herbarium specimens. Using our workflow, we imaged and transcribed specimen-level data for almost 350,000 specimens over a 131-week period; an additional 56 weeks was required for storage container-level data capture. Our project has demonstrated that it is possible to capture both an image of a specimen and a core database record in 35 seconds per herbarium sheet (for intervals between images of 30 minutes or less) plus some additional overhead for container-level data capture. This rate was in line with the pre-project expectations for our approach. Our throughput rates are comparable with some other similar, high-throughput approaches focused on digitizing herbarium sheets and is as much as three times faster than rates achieved with more conventional non-automated approaches used during the project. We report on challenges encountered during development and use of our system and discuss ways in which our workflow could be improved. The conveyor apparatus software, database schema, configuration files, hardware list, and conveyor schematics are available for download on GitHub.
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