Challenges of comprehensive taxon sampling in comparative biology: Wrestling with rosids

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Challenges of comprehensive taxon sampling in comparative biology: Wrestling with rosids
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Folk, R.A., M. Sun, S.A. Smith, P.S. Soltis, R.P. Guralnick, and D.E. Soltis. 2018. Challenges of comprehensive taxon sampling in comparative biology: Wrestling with rosids. American Journal of Botany 105: 433–444. Invited review, special Tree of Life issue.
Folk, Ryan
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Using phylogenetic approaches to test hypotheses on a large scale, in terms of both species sampling and associated species traits and occurrence data—and doing this with rigor despite all the attendant challenges—is critical for addressing many broad questions in evolution and ecology. However, application of such approaches to empirical systems is hampered by a lingering series of theoretical and practical bottlenecks. The community is still wrestling with the challenges of how to develop species‐level, comprehensively sampled phylogenies and associated geographic and phenotypic resources that enable global‐scale analyses. We illustrate difficulties and opportunities using the rosids as a case study, arguing that assembly of biodiversity data that is scale‐appropriate—and therefore comprehensive and global in scope—is required to test global‐scale hypotheses. Synthesizing comprehensive biodiversity data sets in clades such as the rosids will be key to understanding the origin and present‐day evolutionary and ecological dynamics of the angiosperms.
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1 American Journal of Botany 105(3): 1, 2018; 2018 The Authors. American Journal of Botany is published by Wiley Periodicals, Inc. on behalf of the Botanical Society of America. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Although systematists have established a robust phylogenetic framework for angiosperms, the march to the tips has proceeded at a considerably slower pace. Uncovering the basic framework of the angiosperm branch of the tree of life was a challenging, decadeslong process (Chase etal., 1993; Soltis etal., 1997, 1999, 2000, 2011; Qiu etal., 1999; Ruhfel etal., 2014; Wickett etal., 2014), but, due to the sheer size of the angiosperm clade (~220,000,000 spp., reviewed by Scotland and Wortley, 2003), two even greater challenges will be (1) producing a comprehensive understanding of specieslevel relationships across owering plants and (2) pairing this tree with phenotypic traits and geographic data. Even the bestsampled angiosperm clades have specieslevel coverage only slightly better than 30% (e.g., Saxifragales, 2400 species; Soltis etal., 2013; de Casas etal., 2016), with sampling typically resulting from piecemeal, focused, and typically smallscale case studies. While studies of small exemplar clades are important for many questions in comparative biology, they neither intend to test, nor are capable of testing, the broadest evolutionary questions across flowering plants as a whole. While still uncommon, recent investigations have used thousands or tens of thousands of taxa (e.g., Jetz etal., 2012a; Zanne etal., 2014; Werner etal., 2014; Faurby and Svenning, 2015). Tetrapods may provide the best example of progress on dense taxon sampling. Initial trees for this comparatively small clade (~35,000 species; unpublished data from the VertLife project;, with dense coverage of extant species based on standard phylogenetic markers, are nearing completion. Comprehensive synthetic trees based on backbone phylogenies, as well as some deeply sampled supermatrices, have existed for several years in birds and other tetrapod groups (Jetz, etal., 2012a; see also citations in Title and Rabosky, 2017).INVITED SPECIAL ARTICLEFor the Special Issue: Using and Navigating the Plant Tree of LifeChallenges of comprehensive taxon sampling in comparative biology: Wrestling with rosidsRyan A. Folk1,5, Miao Sun1, Pamela S. Soltis1,3, Stephen A. Smith2, Douglas E. Soltis1,3,4, and Robert P. Guralnick1RESEARCH ARTICLEManuscript received 16 August 2017; revision accepted 19December 2017.1 Florida Museum of Natural History, Gainesville, FL 32611, USA2 Department of Ecology and Evolutionary Biology,University of Michigan, Ann Arbor, MI 48109, USA3 Genetics Institute,University of Florida, Gainesville, FL 32610, USA4 Department of Biology,University of Florida, Gainesville, FL 32611, USA5 Author for correspondence (e-mail: Citation : Folk, R. A., M. Sun, P. S. Soltis, S. A. Smith, D. E. Soltis, and R. P. Guralnick. 2018. Challenges of comprehensive taxon sampling in comparative biology: Wrestling with rosids. American Journal of Botany 105(3): 1. doi:10.1002/ajb2.1059 ABSTRACT Using phylogenetic approaches to test hypotheses on a large scale, in terms of both species sampling and associated species traits and occurrence dataand doing this with rigor despite all the attendant challengesis critical for addressing many broad questions in evolution and ecology. However, application of such approaches to empirical systems is hampered by a lingering series of theoretical and practical bottlenecks. The community is still wrestling with the challenges of how to develop specieslevel, comprehensively sampled phylogenies and associated geographic and phenotypic resources that enable globalscale analyses. We illustrate diculties and opportunities using the rosids as a case study, arguing that assembly of biodiversity data that is scaleappropriateand therefore comprehensive and global in scopeis required to test globalscale hypotheses. Synthesizing comprehensive biodiversity data sets in clades such as the rosids will be key to understanding the origin and presentday evolutionary and ecological dynamics of the angiosperms. KEY WORDS comparative methods; data layers; phylogeny; Rosidae; rosids; scientic infrastructure.


2 American Journal of Botanye use of comprehensive taxon samplingup to and including complete coverageis central to future progress in answering key questions in evolution and ecology framed at broad scales. Despite promise, progress in building comprehensive, broadscale phylogenies and their associated data layers (i.e., biologically relevant taxonlevel data linked to tips in a phylogenetic tree, such as phenotypic traits and occurrence records) for testing hypotheses has been limited by diverse challenges, such as incomplete phylogenetic coverage, lack of associated and accessible data layers, and a lack of available infrastructure to disseminate phenotypic and geographic data in ways that facilitate integration with phylogenetic information. Collating such largescale data sets is not trivial; thus, a set of factors converges to render macroevolutionary studies on vast scales as increasingly tractable, yet tantalizingly out of reach for many researchers. e fact that so many globalscale analyses (e.g., Jetz etal., 2012a) have focused on the rich data available for vertebrates (e.g., VertNet,; FishBase,; AmphibiaWeb, demonstrates how building linked biodiversity community resources spurs transformative research (for example, enabling assessment of drivers of diver sication that may include phenotypic traits, geographic range, and ecological niche occupancy, among other candidates). Extending the technical and social approaches for developing such resources to other clades would lower barriers to performing macroscale compar ative analyses in other groups. While the overall state of knowledge in the angiosperms generally lags well behind similar eorts in other groups (e.g., vertebrates, a more tractable target at perhaps one tenth the diversity of owering plants), there are angiosperm subclades well suited for realizing the vision of comprehensively assembling the largescale picture of evolution of terrestrial ecosystems. What are the ingredients for lowering this barrier in owering plants? Here we provide an example of a subclade within the angiosperms that exemplies the value of broadscale approaches, the rosids (Rosidae sensu Cantino etal. 2007). Rosids are a major angiosperm clade, with ~90,000 species (Sun etal., 2016; M. Sun etal., unpublished) representing 22% of all angiosperms (assuming 400,000 species of angiosperms)with properties that make this clade ideal for realizing the vision of globalscale hypothesis testing through a synthesis of biodiversity data. In this paper, we ask: What are the grand challenge questions that could be addressed if a robust comparative frameworka wellresolved phylogeny linked with phenotypic and geographic datawere developed? is contribution is organized as a series of questions: 1. Why rosids? What is the case for building an exemplary compar ative data set for this or any other large clade of life? 2. What challenges persist in building large-scale trees and trait layers despite progress to date, and how can these challenges be addressed? 3. Why use comprehensive approaches to analyze large clades of life? What motivations underlie large-scale analyses in ecology and evolution? ROSIDS: AN EXEMPLAR CLADE FOR THE ANGIOSPERMS Rosids, which capture many of the evolutionary and ecological dynamics of angiosperms as a whole, are ideal as a case study for demonstrating datadriven arguments behind building comparative resources in the owering plants. Rosids exhibit substantial diver sity in morphology, habit, reproductive strategy, and life history, and hence occupy a substantial portion of the phenotypic and ecological space that characterizes angiosperms as a whole. Nearcomplete phylogenetic and trait coverage would permit elucidation of the tempo and mode of global diversication of this large, ecologically dominant clade, enabling comparative analyses with other major lineages of life, and eventually global assessment and synthesis of the evolution of terrestrial landscapes. Because the rosid clade and its associated biomes constitute a major driver of terrestrial biodiversity, predicting future biodiversity patterns for rosids based on historical diversication may likewise be key to understanding the future of other terrestrial clades of life. In short, the rosid clade provides the opportunity to link our understanding of biodiversity from the past to both present and future. We proceed by outlining key properties of the clade and how these exemplify the prerequisites for building any largescale comparative system.PaleoperspectivesRosids have a particularly good fossil record. Many families are well known for their detailed fossil histories (e.g., Fabaceae, Juglandaceae, Betulaceae, Fagaceae); overall, all major subclades (Fig.1), have welldocumented fossils (Manchester, 1988,1989,1992, 1994a, b, 2001; Crepet and Nixon, 1989; CevallosFerriz and Stockey, 1991; Herendeen etal., 1992; Pigg etal., 1993; Boucher etal., 2003; Endress and Friis, 2006; Manchester etal., 2006, 2012; DeVore and Pigg, 2007; Burge and Manchester, 2008; Wing etal., 2009; EstradaRuiz and MartnezCabrera, 2011; Herrera etal., 2012, 2014; Gandolfo etal., 2011; Han etal., 2016; Jud etal., 2016; LarsonJohnson, 2016; Wang etal., 2013; Xing etal., 2014). is rich record provides a superb opportunity for integration of the fossil record with modern diversity and a critical resource for novel approaches for timecalibrating the rosid phylogeny (e.g., Gavryushkina etal., 2017). e rosid clade originated in the Early to Late Cretaceous (115 93 million years ago [Ma]), followed by rapid diversication of two major subclades, the Fabidae and Malvidae crown groups, about 112 to 91 Ma and 109 to 83 Ma, respectively (Wang etal., 2009; Bell etal., 2010). e rosid clade is further divided into clades recognized as 17 orders and 135 families (APG IV, 2016; Fig.).Rosids and terrestrial biome dynamicsUnderstanding rosid evolution also means characterizing the origin and diversity of major biomes. e radiation of the rosids represents the presumably rapid rise of angiospermdominated forests and associated codiversication events that profoundly shaped much of current terrestrial biodiversity (Wang etal., 2009; Boyce etal., 2010). Among major clades in the land plants, perhaps only the grasses and conifers (both smaller clades that are better under stood phylogenetically than rosids) could also lay claim to building biomes covering large sections of the globe. e megadiverse rosid clade is home to most dominant forest trees (e.g., Betulaceae [alder, birch], Casuarinaceae [Australian pine], Fabaceae [legumes], Fagaceae [oak], Juglandaceae [walnut, hickory], Moraceae [g], Salicaceae [willow], Ulmaceae [elm], Rutaceae [citrus], Meliaceae (mahogany), Sapindaceae [maple, buckeye], Malvaceae [linden], Dipterocarpaceae [dipterocarps], and Myrtaceae [eucalypts]). Rosid herbs and shrubs are also prominent components of arctic/alpine and temperate oras (e.g., Salicaceae, Rosaceae, Brassicaceae)


2018, Volume 105 Folk et al.Wrestling with the rosids 3 FIGURE1. Upper panel: Summary tree for ~19,000 rosid species (four loci; Sun et al., 2016); the legend matches branch colors to recognized orders. Lower panel: Photographs of representatives of 10 familiar orders; symbols follow colors in the upper panel legend.


4 American Journal of Botany and comprise aquatics (e.g., Podostemaceae), desert plants (e.g., Euphorbiaceae), and parasites (e.g., Rafflesia). Rosiddominated forests changed the terrestrial landscape, and this biomeshaping clade has been responsible for the concomitant diversication of other clades (e.g., ants, beetles, amphibians, and other animals; fungi; liverworts, ferns) that inhabit these forests. Accumulating evidence shows that other terrestrial lineages quite literally evolved and diversied in the shadow of rosiddominated angiospermous forests (Farrell, 1998; Wilf, 2000; Algeo etal., 2001; Schneider etal., 2004; Moreau etal., 2006; BinindaEmonds etal., 2007; Roelants etal., 2007; Hibbett and Matheny, 2009; Wang etal., 2009; Watkins and Cardelus, 2012; Moreau and Bell, 2013; Feldberg etal., 2014).Applied dimensionsRosids exhibit spectacular diversity in biological processes that may be responsible for the many practical uses of members of the clade. Foremost among these are symbioses with nitrogenxing bacteria in legumes and nine other families, the phylogenetic distribution of which is remarkably concentrated in one clade, the nitrogenxing clade (Soltis etal., 1995; Werner etal., 2014; Li etal., 2015). is symbiosis has enabled many members to thrive in resourcepoor soils; thus, the functional genomics of this symbiosis is of great interest for crop improvement (Stokstad, 2016). Rosids also exhibit diverse phytochemistry, providing potent biochemical defense mechanisms, such as glucosinolate production in Brassicales (Rodman etal., 1998; Edger etal., 2015). is chemical diversity is also associated with the many economic uses of members of Brassicaceae. e plant model Arabidopsis thaliana (Brassicaceae) is in the rosid clade; many other rosids are also genetic models with sequenced genomes, e.g., Brassica rapa also of Brassicaceae (Brassica rapa Genome Sequencing Project Consortium, 2011) and several legumes (Sato etal., 2008; Schmutz etal., 2010, 2014; Young etal., 2011; Varshney etal., 2012, 2013). CHALLENGES IN THE ROSIDSState of the artDespite the ecological and economic importance of rosids, aer decades of data accumulation, our knowledge of the clade remains remarkably limited along any metric. Rosids thus not only serve as a case study for the possibilities of largescale biodiversity research, but also reveal the constraints on this research due to limitations in basic biodiversity knowledge. is knowledge gap is character istic of nearly all large clades across the Tree of Life with the possible exception of vertebrates. Shedding a quantitative light on these disparities is critical to raising awareness about how little we truly know about global biodiversity and identifying priorities for future eorts in owering plants. Mapping DNA sequence availability onto a supertree estimate of the complete rosid clade (Fig.2, combining both phylogenetic and taxonomic knowledge from the Open Tree of Life; Hinchli etal., 2015) shows that current DNA sampling of rosids is highly biased toward subclades of economic interest and signicant temperate diversity (e.g., legumes). Groups with the worst representation (e.g., Malpighiales) have few economically impor tant members, yet are critical elements of tropical oras. Only a minority of rosid species,234 of 90,000, or 34%have sequence data of any kind in GenBank (https://www.ncbi.nlm.nih. gov/genbank/). Many of these sequences are microsatellites, ESTs, or other sequences with low species coverage and are not usable for phylogenetics. Even wellknown clades, such as Rosales (predominantly temperate), are poorly represented, with only 23% of species having usable DNA sequence data available (Table1). Only one small group, Fagales, surpasses 50% coverage. Curating the available DNA sequence data for supermatrix phylogenetic analyses (Sun etal., 2016) results in further loss of data, leaving approximately 21% of species across the rosids represented as phylogenetic tips. e pattern of incomplete and biased taxon sampling in the rosids (cf. Fig.2) is largely true of the angiosperms in general (see Fig.2 of Eiserhardt etal. [2018] in this issue). Most known species still have no DNA data at all (Drew, 2013; Hinchli etal., 2015); the vast majority of the owering plant branch of the tree of life remains dark.Phylogenetic biasLargescale phylogenetic eorts typically require integrating eorts and data sets from heterogeneous sources, including focused phylogenetic analyses, DNA barcoding data sets, genomic resources, and other data that were not purposebuilt for comprehensive specieslevel inference at global scales. e piecemeal assembly of data sets oen makes it dicult to control for uneven sampling of clades. A future need is the development of approaches to assess and correct phylogenetic bias in taxon sampling (either directly through improved sampling or indirectly through modeling taxon absence). In principle, phylogenetically even but incomplete sampling can be accounted for under many models if taxon sampling is unbiased (e.g., FitzJohn etal., 2009). Change in the overall shape of the tree due to biased sampling is not easily controlled for and will likely alter conclusions under models that make inferences from tree topology and branch lengths. As more researchers assemble largescale phylogenomic data sets, we see a need for identifying gaps in the coverage of the tree of life and of deploying this knowledge in sequencing eorts to ll these gaps and avoid duplication of eort (see also Eiserhardt etal., 2018, this issue). Although some generalpurpose loci have been developed for the angiosperms (e.g., LveillBourret etal., 2018 and the PAFTOL project; Eiserhardt etal., 2018, this issue), customdeveloped, oen nonoverlapping loci remain the norm (e.g., Weitemier etal., 2014; Mandel etal., 2014; Folk etal., 2015; Chamala etal., 2015; Schmickl etal., 2015), creating greater diculties for posthoc aggregation across these experiments.Spatial biasIn addition to building comprehensive phylogenetic hypotheses, an ongoing trend in comparative research has been the assembly of equally comprehensive and globally scaled data layers. Recent plant contributions in this spirit include Werner etal. (2014), Zanne etal. (2014), and Daz etal. (2016). For many clades of land plants, traits and geographic data are missing for most species in existing databases. is lack of coverage results partly from bias in the cumulative assembly of species trait and occurrence data over time, typically from aggregating a long series of smallscale or specialized projects and digitization eorts. Such data accumulation is highly correlated with sociological factors such as gross domestic


2018, Volume 105 Folk et al.Wrestling with the rosids 5 product, local funding sources, and distance to institutions per forming digitization (Amano and Sutherland, 2013; Meyer etal., 2015). One hallmark of spatial bias is an inverse latitudinal gradient clearly observable in the rosids (Fig.3A), where records are least heavily accumulated and species least completely represented in the tropics, some of the most biodiverse parts of the world for the rosids (Fig.3B). Because major rosid clades are not evenly distributed across the globe (e.g., Malpighiales and Rosales are associated, respectively, with tropical and temperate latitudes), spatial and phylogenetic bias are likely to interact. FIGURE2. Phylogeny of all rosids integrating taxonomic and phylogenetic knowledge (84,153 species, from the Open Tree of Life; Branch coloration represents ordinal taxonomy and matches the legend of Fig.1. Outer band: Species that either have (yellow) or lack (blue) phylogenetically usable data (usable based on taxa remaining after a series of ltering steps described by Sun et al., 2016), based on matching nomenclature with tips present in Sun et al. (2016) against the Open Tree topology (excluding Open Tree tips with labels for fossil taxa, indicating subspecic or hybrid status, etc.). Note how few taxa have data (yellow) and how phylogenetically uneven this data coverage is.


6 American Journal of Botany Spatial bias may propagate to downstream analyses that do not explicitly include spatial data, such as those focusing on potentially correlated traits and taxon coverage. Hence, spatial bias can occur at multiple levels of sampling; accumulation of phylogenetic tips, occurrences, and species traits are all inuenced by availability of material and digitization eorts. Most directly, spatial bias has an enormous impact on the spatial distribution of occurrence records, such that nearly any largescale clade in the tree of life has an occurrence density pattern matching closely that seen in the rosids (Fig.3A; compare with global mammal GBIF records: Boitani etal., 2011: g.2). is strong bias is partly due to historical dierences in collection eort. However, diering levels of investment in biodiversity digitization among countries also contribute to this unevenness, which is compounded by the tendency of digitization eorts to be locally focused initially, even for internationally representative collections (Amano and Sutherland, 2013; Meyer etal., 2015). As with phylogenetic bias, we see not only challenges but opportunities. It would be a major step toward enabling research if future eorts specically assigned digitization priorities on the basis of evidence for data gaps in current infrastructure. For most herbaria, it is not feasible in the immediate future to completely digitize all specimens, including georeferences, images, and other data. Targeting data gaps would provide an evidencebased method to direct digitization eorts and maximize downstream research impact.Linked dataLinking data sets such as those discussed above is critical for largescale inference (Parr et al., 2012). For instance, a common task is to subset a tree for the group of interest using a list of taxon names. Linked data already have a roleproviding linkages between taxonomic concepts and a phylogeny. If unusual phylogenetic placements are observed, it might be necessary to retrieve either original voucher specimen photographs or original sequence data. Finally, using the name list, linkages could allow users to subset trait data from online repositories such as the TRY Plant Trait Database (; both unusual trait scores and the possibility of polymorphism would warrant consulting original specimen material using online herbaria. Central to these aims are stable identiers built around taxon concepts to facilitate linking of disparate data products. Links between genetic data, online her baria, and phylogenetic tips are typically not explicit and need to be laboriously sought manually, although some linkages, such as that between GenBank and iDigBio (, are cur rently being developed. For example, herbarium specimen records in iDigBio that serve as vouchers for GenBank sequences and have globally unique identiers on GenBank are linked to their associated DNA sequences; unfortunately, globally unique identiers are not consistently used or formatted properly (Guralnick etal., 2014), thwarting eorts to link most data directly. Community consensus is lacking about minimal reporting standards for integrative research programs that include multiple data types. Minimally, we recommend that these projects should contain unique sample identiers (e.g., GUIDs) as part of data deposition in standard dataspecic repositories (e.g., GenBank and SRA; Unambiguous identier practices will enable future researchers to scrape metadata for recognizable identiers and retrieve matching information gener ated downstream from those samples, such as sequences, modeled geographic distributions, and other data and knowledge products.Name reconciliationReconciling conicting taxon identiers is unavoidable for any project that attempts to accrue multispecies data from diverse sources yet remains a core challenge of largescale biology (Patterson etal., 2010). Many largescale databases have their own internal taxonomy (e.g., GBIF; GenBank; Open Tree, https://, and standalone name products also exist (e.g., e Plant List,; Tropicos, http:// ese taxonomies sometimes represent conicting taxonomic opinions and oen are incomplete and partially TABLE1. Sampling statistics for DNA data (GenBank, and occurrence data (GBIF, for orders of rosids. Order GenBank DNA data GBIF occurrence data % Species sampled % Genera sampled Species with no records Species with records Species with records Brassicales 38.4 92.7 19.5 55.7 35.9 Celastrales 20.4 73.4 29.4 57.3 36.0 Crossosomatales 36.4 100.0 53.7 74.2 56.1 Cucurbitales 36.8 96.9 45.2 48.4 24.5 Fabales 27.8 88.6 25.1 68.6 46.1 Fagales 50.9 100.0 11.0 97.2 68.5 Geraniales 36.4 100.0 10.7 61.4 36.8 Huerteales 29.2 100.0 53.2 16.7 12.5 Malpighiales 23.9 83.1 24.6 58.0 35.4 Malvales 21.9 76.0 30.8 50.3 30.9 Myrtales 11.5 69.2 23.4 70.7 47.6 Oxalidales 10.5 75.0 26.5 56.0 32.0 Picramniales 10.2 66.7 46.0 57.1 38.8 Rosales 22.8 87.0 15.3 73.3 48.7 Sapindales 21.0 73.7 31.5 62.1 40.2 Vitales 13.6 64.3 52.8 50.7 28.5 Zygophyllales 20.3 75.0 33.4 67.5 45.5Notes: DNA taxon numbers were estimated by collating sequences for standard phylogenetic markers: LEAFY, NIA (nitrate reductase), ITS, ETS, 18S, 26S, atpA, atpB, atpF, rbcL, trnL, matK, ndhF, ndhA, rpl16, rps16, ycf1 ycf2 psbA-trnH spacer, petB-petD spacer, trnC-pet1N spacer, trnS-trnG spacer, trnY-trnT spacer, atpB-rbcL spacer, trnL-trnF intergenic spacer, trnT-trnL intergenic spacer. Denominators for percentage calculations come from total species estimates in Stevens (2001 onward).


2018, Volume 105 Folk et al.Wrestling with the rosids 7 out of date. Taxonomic mismatch results in major discrepancies in accepted genera, total species number, and other important metrics that inform sampling, analysis, and synthesis. e availability of community reconciliation services (Boyle etal., 2013) is an impor tant step toward resolving these issues, at least for providing current assessments of valid taxon names. A muchneeded area of growth is the improvement of existing databases by digitizing and incorporating major, yet largely inaccessible, natural history literature (below). While necessary for building the framework of online taxonomies, a static, centralized approach to the name reconciliation problem (generally the approach used to date) will lack permanency given the continual ux of taxon delimitation (Lepage etal., 2014), meaning that a resource that is updatable, preferably by the community and in close to real time, will be critical to improving resources beyond those available to date.Expert and algorithmic range productsA rich heritage of geographic range products is available for tetrapods, resulting from massive data digitization that has enabled comprehensive macroecological analyses and conservationoriented decisionmaking (Jetz etal., 2012a, b; Meyer etal., 2015). In addition to purely expertdrawn range maps, automated approaches based on point occurrences have also been developed recently (e.g., Merow etal., 2016, 2017), oering the potential for generating geographic range products in clades where few ranges have been FIGURE3. (A) Global distribution of occurrence records for species in the rosid clade with at least 30 occurrence records in GBIF (https://www.gbif. org/; downloaded October 2015; 6,085,341 records), plotted on an elevation data set from R package raster. (B) Countrywise species richness, colorcoded by a Jenks natural breaks classication. Species counts used country DarwinCore elds from both georeferenced and ungeoreferenced records, aggregating GBIF data with an unpublished data set of Amazonian records. The distribution of records is largely characteristic of any globally distrib uted clade, revealing more about global digitization eort than geographic range dynamics, while species richness estimates from available data for the rosids are close to a priori expectations. Projection for both maps is EPSG:4326.


8 American Journal of Botany expertassessed. Range data are complementary to betterknown occurrence record data, as range data have the potential to coarsely assess true species absence rather than pseudoabsence (Jetz etal., 2012a). Range products are not only useful for direct empirical analyses, but also for quality control of occurrence records for other research (Jetz etal., 2012b). Occurrence data sets too large to curate entirely by hand can be automatically checked against expertderived range maps using a spatial join to remove data points likely to be incorrect. ese maps typically require expert involvement to produce credible estimates and are themselves hypotheses open to reinterpretation with new reports of species detection (or lack thereof).Digitization of legacy natural history dataEnormous eort has been made in increasing access to data in biological collections (e.g., VertNet, iDigBio, and GBIF). e availability of these resources has facilitated growth in macroperspectives in ecology and evolution; the vast number of papers using repositories of occurrence records (nearly 6000 according to, 2017) illustrates how natural history data drive progress in biodiversity science. Despite this eort, literature containing natural history data in plants remain untapped resources that are as rich as specimen data. Rather than direct point observations, literature sources represent expertassessed consensus values for geographic range (see above) and phenotype, as well as a consensus taxonomic product for a given region in the form of accepted taxa. For largescale digitization strategies, largescale oras are ideal data sources. ese oras typically comprise comprehensive treatments of a specic area of the globe, covering information such as accepted species lists, partial synonymies, wholeplant trait data, coarsescale geographic range descriptors at the country, state, or other regional level, and variable additional features including chromosome number and invasive status. Regional taxonomic treatments are rich data sets; products of broad utility that can be developed from these treatments include (1) improved taxon name resolution, which could be combined with existing name databases for an improved consensus product; (2) coarsescale range maps such as are available for vertebrates, typically of political regions, for inferences of range evolution, invasive species status, or quality assessment of occurrence data and spatial bias; and (3) very large morphological matrices. eFloras, such as the Flora of North America (Flora of North America Editorial Committee, 1993 onward) and Flora of China (Wu etal., 1994 onward; Brach and Song, 2008), represent lowhanging fruit for data mining. e text in these eorts does not identify descriptors (e.g., morphological terms do not have explicit metadata), so that indirect text scraping strategies are needed to match descriptors among taxa. While text scraping requires considerable eort, the payo is substantial for obtaining organismal information for hundreds or thousands of phylogenetic tips. Some recent eorts (e.g., Flora of Tropical West Africa; https://archive. org/details/FloraOfWestTropi00hutc) are partially semantically tagged, so that subblocks of text, such as a traitrelated text block, can be obtained for further processing. Unfortunately, few other ora projects are so accessible. Although this is changing, e.g., for Flora Malesiana (Nooteboom etal. 2010 onwards) and Flora of New Zealand (Breitwieser etal. 2010 onwards), many recent and ongoing oras are not available online. Addressing these gaps in ora production would facilitate signicant progress towards the vision of illuminating the dark parts of the tree of life, going beyond simply populating the tree with tip taxa by adding geographic and trait data layers with the assistance of partially automated approaches (Burleigh etal., 2013; Liu etal., 2015; Cui etal., 2016; Endara etal. 2018). WHY USE COMPREHENSIVE APPROACHES? An obvious rst step in performing largescale analyses is identifying the motivation for what may be a costly and laborintensive enterprise spanning years from planning to fruition. Why ll in the dark parts of the tree, for rosids or any other clade, if we already understand higherlevel relationships? Why indeed go big in phylogenetics? Why not go small many times in succession on small subclades and ultimately sum these wellworked case studies up to the ecological and evolutionary whole? Discussion on this point is important because basic questions have been raised about the inherent value of large phylogenies for testing hypotheses in evolution and ecology (Donoghue and Edwards, 2014).Exemplar cladeWith respect to the rosids or any other group, the choice of taxon for addressing largescale hypotheses should be evidencebased and targeted toward nding groups appropriate in scale and properties for a given research question. Explicitly or implicitly, much recent work in phylogenetics sets its aims more broadly than infer ences solely constrained to the group of interest, such that the use of comprehensive approaches has contributed insights for decades in evolution and ecology (see an early review by Pagel, 1999). As has long been the case for small clades, largescale phylogenetic research should explicitly provide reasons for studying exemplar clades embodying the prerequisites for understanding particular evolutionary or ecological dynamics. We use exemplar clade to denote a monophyletic group that captures generalizable ecological and evolutionary processes for the purpose of analytical inference. An exemplar clade (= model clade; e.g., Chanderbali etal., 2016) thus serves as a biodiversity model in a phylogenetic framework, with the aim of inference placed more broadly than the group under concern. Selection of a study group should not be based primarily on data availability, a criterion that would likely only exacerbate existing knowledge gaps and phylogenetic biases in future investigationsaway from what are already dark parts of the tree of life. If the aim is to study generalizable principles and processes across the angiosperms, or in other parts of the tree of life, developing large exemplar clades as community resources puts globalscale research into reach, the conclusions of which will be reciprocally enhanced as other comprehensive comparative data sets are developed.A tale of two approachese comparative method has as its goal the testing of hypotheses using multispecies samples in a phylogenetic framework (Felsenstein, 1985). Recently, a dichotomy has been proposed, identifying what may be complementary or conicting alternative approaches to such macroevolutionary questions (Donoghue and Edwards, 2014). One could either (1) use an integrative, largescale approach to test hypotheses in a single framework (e.g., Meredith etal., 2011; Jetz


2018, Volume 105 Folk et al.Wrestling with the rosids 9 etal., 2012a; Zanne etal., 2014), or (2) accrue a large number of smallscale, wellcharacterized clades, which investigators would follow by a qualitative synthetic review (e.g., Soltis etal., 2006; Donoghue and Edwards, 2014) or quantitative metaanalyses (e.g., Mayrose etal., 2011) to test the same largescale hypotheses. Largescale studies have been criticized by some based in part on three largely accurate observations: (1) robust and comprehensive clade and trait sampling is very challenging to achieve on large scales, (2) identifying appropriate evolutionary models is dicult, in that a sample representing a long timespan is likely to capture a large number of evolutionary dynamics, and (3) individual instances substantiating broad patterns are anonymized and massaged out of the message of many such studies. ese issues are more easily overcome if taxonomic sampling is intentionally placed within modest limits. Despite these concerns, the scale of systematics research is steadily increasing, through improved sampling of both taxa and loci, generating phylogenetic matrices that are growing both taller and wider. e same growth is true for trait and occurrence data sets that accompany phylogenetic matrices. But a community trend does not constitute justication ipso facto; it is reasonable that the choice of a largescale analytical approach should be accompanied by compelling reasons for being large, as we have outlined above. Likewise, are there also risks for intentionally small, wellcircumscribed scales in biodiversity science?Emergent processesPerhaps the most immediate problem of integrating over large numbers of small case studies is the potential for consistently failing to recover patterns that inherently cannot appear in small data sets. is problem concerns analytical scale: how do we build data sets appropriate for the phylogenetic and temporal scales at which we are testing hypotheses? We argue that biodiversity questions posed globally across large taxonomic groups require sampling that is appropriate to global scales of inference. Synthesizing knowledge in this way across large expanses of space and time will consistently compel the analysis of large data sets. e use of small clades to answer questions at large scales leads to data sets that are well char acterized but restricted in their sampling of biological diversity. We identify conditions below where such sampling scales could obscure emergent signals and impact hypothesis testing. One core issue is statistical power. For inference of diversication and other approaches that use highly parameterized models, branches and their lengths are the data points. Hence, fairly large phylogenies, on the order of hundreds to thousands of taxa under idealized simulated conditions (e.g., diversication: Davis etal., 2013; Rabosky and Huang, 2016; phylogenetic correlation: Ackerly, 2009) are required to have sucient sensitivity to detect shis in diversication with high power. It is expected, therefore, that an intentionally taxonlimited approach will consistently underestimate the number of diversication shis and the occurrence of characterassociated diversication patterns. Although no quantitative studies have been performed to assess the eects of taxonomic scope beyond statistical power, we expect that the number of signicant evolutionary patterns extractable from phylogenetic data will be consistently and articially truncated by focusing on small case studies. Such a truncation is likely for the simple reason that such patterns may be present in subclades but without the context of broader sampling that would make them detectable. Estimation error increases with increasingly deep trees (Salisbury and Kim, 2001), and even within a given tree, estimation error is expected to increase as estimated nodes approach the root (Garland etal., 1999), leading to unequal error in ancestral state reconstruction across a tree. If a particular ancestral state is of interest, it is possible that removing taxa could result in smaller estimated uncertainty by incompletely sampling evolutionary transitions (Heath etal., 2008a), thus underestimating trait evolutionary rates and decreasing the magnitude of estimated error (e.g., the condence interval, cf. Garland etal., 1999). Hence, a smaller reported uncertainty does not necessarily imply that the true error of such an estimate has actually decreased due to sampling scheme alone. Building data sets appropriate to the scale of questions posedfor globalscale analyses, this oen means including data for as many extant species as possible, maximizing the information behind our inferences and the estimated uncertainty thereofis therefore preferable. e detection of some processes may fundamentally require large phylogenies, irrespective of statistical power. is problem is subtler, in that it cannot be easily measured or controlled for by per forming statistical power studies or extending models to account for potential data set biases. Such a problem is likely to occur in instances where deeplevel patterns in highly diverse clades (e.g., the root of major angiosperm clades) are the object of inference, but where inferences are sensitive to taxon sampling. is situation could appear in ancestral state reconstruction, where a deeplevel node is of interest, but the polarity of ancestral states is impacted by a complex distribution of states in descendant extant taxa. Some of the risks of poor taxon sampling in this case include incomplete sampling of evolutionary transitions in the clade of interest (Heath etal., 2008a) and warping of overall tree shape by dropping taxa (Heath etal., 2008b). ese concerns cannot both be addressed in small test cases (in this case, sets of trees with limited taxon sampling at deep levels) if the relevant information for accurately distinguishing among possible ancestral states is not present in the data, irrespective of our ability to detect it. Simulation studies have shown increased estimation error as proportional taxon coverage decreases (Salisbury and Kim, 2001; Litsios and Salamin, 2012; but see Li etal., 2008). A nal issue with a solely smallscale focus, raised by Beaulieu and OMeara (2018, this issue), is ascertainment bias. e choice of idealized smallscale clades to understand broadscale patterns oen resulting in a focus on groups showing especially frequent shis in a biological traitmay result in overemphasis of unusual outlier taxa unrepresentative of overall variation patterns. Hence, largescale biodiversity studies are needed to complement and contextualize focused cladelevel studies. Likewise, as we have suggested for the rosids, the suitability of an exemplar clade is a testable assumption that can be directly assessed by asking how well a focal clade crosssections broader diversity patterns. Issues of both statistical power and levels of inference imply that questions exist that are uniquely suited to purposeful attempts at comprehensive taxon sampling, such that focusing solely on small, wellcharacterized case studies is neither always sucient nor invariably necessary. Approaches in biodiversity science that use small study clades will continue to be relevant, particularly for understanding recentscale evolutionary processes. By contrast, the application of such sampling schemes to global questions poses risks, possibly resulting in data sets with high condence in individual data points but restricted and possibly biased coverage of the biodiversity that


10 American Journal of Botany underlies many biological processes. Comprehensive phylogenetic approaches that span deeptime and global geographic scales are urgently needed for the kinds of grand challenges which the comparative approach to biology is poised to address, due not simply to an obsession with larger and more resolved data sets (Hahn and Nakhleh, 2016), but to their central necessity for answering questions on deeptime and global scales in highly diverse clades.Ways forwardIn our view, largeand smallscale approaches are complementary. Some questions are best addressed with small clades. Increasingly, however, phylogenetic eort is devoted to asking questions in evolution and ecology that require large trees and comprehensive taxon sampling (e.g., global patterns of diversication, deeptime ancestral state reconstruction and biogeography, correlated evolution of characters, community phylogenetics), oen in a modelbased or otherwise explicitly quantitative framework (e.g., Smith and Donoghue, 2008; Smith and Beaulieu, 2009). We argue that the need remains for largescale, comprehensive approaches that are appropriate to address questions of major importance. We stress that focused case studies on small clades remain crucial for addressing certain specic questions and serve as an impor tant element of building comparative data sets. Nonetheless, despite substantial progress in many domains, 30 years of eort on small focal clades in molecular systematics have resulted in uneven and incomplete coverage of rosids in particular, and angiosperm diver sity as a whole, suggesting this approach alone may not suce to eventually synthesize biodiversity knowledge across the owering plants. Targeted and coordinated, largescale sampling eorts at the community level are needed to complement these eorts and directly address data and knowledge gaps that have continually per sisted despite intense eorts by individual researchers. Rather than continually aggregating upward in scope from focused data sets to create incomplete and biased larger sets, we can do more to collect comprehensive biodiversity data broadly for future users to disaggregate downward for focused work. CONCLUSIONS Much progress has been made in understanding deeplevel relationships in the angiosperms (Chase etal., 1993; Qiu etal., 1999; Soltis etal., 1999, 2011) with largescale sequencing projects (e.g., 1KP, Matasci etal., 2014) resulting in robust backbone resolution (Wickett etal., 2014) and community consensus taxonomic products (APG IV, 2016). Current eorts in plant systematics beyond the backbone have largely remained centered on localized taxonomic sampling eorts, with less consideration of how to develop more comprehensive, communitybased, synthetic investigations or of whether such goals are feasible without purposeful largescale generation of phylogenetic data to ll in gaps. Yet, it is just these kinds of eorts that can provide the most critical insights and applications in biology, particularly those posed at global or deeptime scales. e eort to develop such synthetic analyses is still enormous, and bottlenecks are multidimensional. We make the case for an evidencebased assessment as we build comprehensive community resources for phylogenetically informed hypothesis testing, with a focus on exemplary, hyperdiverse clades such as the rosids. Such resources, to maximize enabled research, should comprehensively sample phylogenetic tips and linked phenotypic and geographic data as a community priority. is approach is complementary to focal studies on smaller clades, which may address signicant problems but on dierent phylogenetic and temporal scales; both can help with goals geared towards broadscale synthesis. However, we believe that purposebuilt comprehensive phylogenies covering global scales and ancient radiations are valuable resources that, when linked to other biodiversity data and knowledge products, will be an impetus for transformative research. ACKNOWLEDGEMENTS e authors benetted from workshops supported by the Open Tree of Life ( and FuturePhy (https:// projects for discussions on building community resources. B. iers granted access to unpublished Amazonia records for our species richness estimates. M. Gitzendanner assisted with GenBank gap analyses. E. Edwards and an anonymous reviewer are thanked for comments on an earlier dra of this manuscript. is paper was supported in part by NSF (DBI1523667 to R.A.F.; DBI1458640 to D.E.S. and P.S.S.; DBI1458466 to S.A. Smith; DEB1442280 to P.S.S. and D.E.S.). LITERATURE CITEDAckerly, D. D. 2009. Taxon sampling, correlated evolution, and independent contrasts. Evolution 54: 1480. Algeo, T.J., S.E. Scheckler, and J.B. Maynard. 2001. Eects of the Middle to Late Devonian spread of vascular land plants on weathering regimes, marine biotas, and global climate. In Gensel, P. G. and D. E. [eds.]. Plants invade the land: evolutionary and environmental perspectives, 213. 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