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Biological collections for understanding biodiversity in the Anthropocene
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 discussed in the accompanying collection of papers within this theme issue. As these unparalleled resources are under threat owing to budget cuts and other institutional pressures, we aim to shed light on the unique discoveries that are possible in museums and, thus, the singular value of natural history collections in a period of rapid change. This article is part of the theme issue ‘Biological collections for understanding biodiversity in the Anthropocene’.
Journal Article
Widespread homogenization of plant communities in the Anthropocene
Native biodiversity decline and non-native species spread are major features of the Anthropocene. Both processes can drive biotic homogenization by reducing trait and phylogenetic differences in species assemblages between regions, thus diminishing the regional distinctiveness of biotas and likely have negative impacts on key ecosystem functions. However, a global assessment of this phenomenon is lacking. Here, using a dataset of >200,000 plant species, we demonstrate widespread and temporal decreases in species and phylogenetic turnover across grain sizes and spatial extents. The extent of homogenization within major biomes is pronounced and is overwhelmingly explained by non-native species naturalizations. Asia and North America are major sources of non-native species; however, the species they export tend to be phylogenetically close to recipient floras. Australia, the Pacific and Europe, in contrast, contribute fewer species to the global pool of non-natives, but represent a disproportionate amount of phylogenetic diversity. The timeline of most naturalisations coincides with widespread human migration within the last ~500 years, and demonstrates the profound influence humans exert on regional biotas beyond changes in species richness.
Human-driven movements and extinctions of species have made plant communities across biomes more homogenous. Here the authors quantify plant vascular species and phylogenetic homogenization across the globe, finding that non-native species naturalisations have been a major driver.
Journal Article
The unrealized potential of herbaria for global change biology
Plant and fungal specimens in herbaria are becoming primary resources for investigating 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 invasive 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 specimens are under-explored relative to vascular plants. To facilitate broader application of plant and fungal 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.
Journal Article
Widespread sampling biases in herbaria revealed from large-scale digitization
Nonrandom 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.
We determined spatial, temporal, trait, phylogenetic, and collector biases in c. 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).
We identified numerous shared and unique biases among these regions. Shared biases included specimens collected close to roads and herbaria; specimens collected more frequently during biological spring and summer; specimens of threatened species collected less frequently; and specimens of close relatives collected in similar numbers. Regional differences included overrepresentation of graminoids in SA and AU and of annuals in AU; and 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, with their associated preferences and idiosyncrasies, shaped patterns of collection bias via ‘founder effects’.
Studies using herbarium collections should account for sampling biases, and future collecting efforts should avoid compounding these biases to the extent possible.
Journal Article
The Impact of Missing Data on Species Tree Estimation
Phylogeneticists are increasingly assembling genome-scale data sets that include hundreds of genes to resolve their focal clades. Although these data sets commonly include a moderate to high amount of missing data, there remains no consensus on their impact to species tree estimation. Here, using several simulated and empirical data sets, we assess the effects of missing data on species tree estimation under varying degrees of incomplete lineage sorting (ILS) and gene rate heterogeneity. We demonstrate that concatenation (RAxML), gene-tree-based coalescent (ASTRAL, MP-EST, and STAR), and supertree (matrix representation with parsimony [MRP]) methods perform reliably, so long as missing data are randomly distributed (by gene and/or by species) and that a sufficiently large number of genes are sampled. When data sets are indecisive sensu Sanderson et al. (2010. Phylogenomics with incomplete taxon coverage: the limits to inference. BMC Evol Biol. 10:155) and/or ILS is high, however, high amounts of missing data that are randomly distributed require exhaustive levels of gene sampling, likely exceeding most empirical studies to date. Moreover, missing data become especially problematic when they are nonrandomly distributed. We demonstrate that STAR produces inconsistent results when the amount of nonrandom missing data is high, regardless of the degree of ILS and gene rate heterogeneity. Similarly, concatenation methods using maximum likelihood can be misled by nonrandom missing data in the presence of gene rate heterogeneity, which becomes further exacerbated when combined with high ILS. In contrast, ASTRAL, MP-EST, and MRP are more robust under all of these scenarios. These results underscore the importance of understanding the influence of missing data in the phylogenomics era.
Journal Article
The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae)
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.
Journal Article
Digitization and the Future of Natural History Collections
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 on the data, workflows, and infrastructure produced by Digitization 1.0 to create digital-only workflows that facilitate digitization, curation, and data links, 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 issues of global change.
Journal Article
Coalescent versus Concatenation Methods and the Placement of Amborella as Sister to Water Lilies
The molecular era has fundamentally reshaped our knowledge of the evolution and diversification of angiosperms. One outstanding question is the phylogenetic placement of Amborella trichopoda Baill., commonly thought represent the first lineage of extant angiosperms. Here, we leverage publicly available data and provide a broad coalescentbased species tree estimation of 45 seed plants. By incorporating 310 nuclear genes, our coalescent analyses strongly support a clade containing Amborella plus water lilies (i.e., Nymphaeales) that is sister to all other angiosperms across different nucleotide rate partitions. Our results also show that commonly applied concatenation methods produce strongly supported, but incongruent placements of Amborella: slow-evolving nucleotide sites corroborate results from coalescent analyses, whereas fast-evolving sites place Amborella alone as the first lineage of extant angiosperms. We further explored the performance of coalescent versus concatenation methods using nucleotide sequences simulated on (i) the two alternate placements of Amborella with branch lengths and substitution model parameters estimated from each of the 310 nuclear genes and (ii) three hypothetical species trees that are topologically identical except with respect to the degree of deep coalescence and branch lengths. Our results collectively suggest that the Amborella alone placement inferred using concatenation methods is likely misled by fast-evolving sites. This appears to be exacerbated by the combination of long branches in stem group angiosperms, Amborella, and Nymphaeales with the short internal branch separating Amborella and Nymphaeales. In contrast, coalescent methods appear to be more robust to elevated substitution rates.
Journal Article
Malpighiales phylogenetics: Gaining ground on one of the most recalcitrant clades in the angiosperm tree of life
The eudicot order Malpighiales contains ~16000 species and is the most poorly resolved large rosid clade. To clarify phylogenetic relationships in the order, we used maximum likelihood, Bayesian, and parsimony analyses of DNA sequence data from 13 gene regions, totaling 15604 bp, and representing all three genomic compartments (i.e., plastid: atpB, matK, ndhF, and rbcL; mitochondrial: ccmB, cob, matR, nad1B-C, nad6, and rps3; and nuclear: 18S rDNA, PHYC, and newly developed low-copy EMB2765). Our sampling of 190 taxa includes representatives from all families of Malpighiales. These data provide greatly increased support for the recent additions of Aneulophus, Bhesa, Centroplacus, Ploiarium, and Rafflesiaceae to Malpighiales; sister relations of Phyllanthaceae + Picrodendraceae, monophyly of Hypericaceae, and polyphyly of Clusiaceae. Oxalidales + Huaceae, followed by Celastrales are successive sisters to Malpighiales. Parasitic Rafflesiaceae, which produce the world's largest flowers, are confirmed as embedded within a paraphyletic Euphorbiaceae. Novel findings show a well-supported placement of Ctenolophonaceae with Erythroxylaceae + Rhizophoraceae, sister-group relationships of Bhesa + Centroplacus, and the exclusion of Medusandra from Malpighiales. New taxonomic circumscriptions include the addition of Bhesa to Centroplacaceae, Medusandra to Peridiscaceae (Saxifragales), Calophyllaceae applied to Clusiaceae subfamily Kielmeyeroideae, Peraceae applied to Euphorbiaceae subfamily Peroideae, and Huaceae included in Oxalidales.
Journal Article