Abstract
Taxonomic monographs have the potential to make a unique contribution to the understanding of global biodiversity. However, such studies, now rare, are often considered too daunting to undertake within a realistic time frame, especially as the world’s collections have doubled in size in recent times. Here, we report a global-scale monographic study of morning glories (Ipomoea) that integrated DNA barcodes and high-throughput sequencing with the morphological study of herbarium specimens. Our approach overhauled the taxonomy of this megadiverse group, described 63 new species and uncovered significant increases in net diversification rates comparable to the most iconic evolutionary radiations in the plant kingdom. Finally, we show that more than 60 species of Ipomoea, including sweet potato, independently evolved storage roots in pre-human times, indicating that the storage root is not solely a product of human domestication but a trait that predisposed the species for cultivation. This study demonstrates how the world’s natural history collections can contribute to global challenges in the Anthropocene.
Similar content being viewed by others
Data availability
Passport data for all specimens included in the molecular studies presented in this paper are available in Supplementary Data File 2. Additional records and information for the collections included in this study and for specimens added subsequently are available through the project website (https://herbaria.plants.ox.ac.uk/bol/ipomoea). DNA barcode sequences are available through GenBank and genome assemblies are available through the Oxford Repository Archive (https://doi.org/10.5287/bodleian:kepgnxzeK). Illumina raw reads are available through the Sequence Read Archive (BioProject PRJNA453382). Alignment files and other materials are available from the corresponding author upon request.
References
Brownsey, P. The Banks and Solander collections—a benchmark for understanding the New Zealand flora. J. R. Soc. N. Z. 42, 131–137 (2012).
Mabberley, D. J. Jupiter botanicus: Robert Brown of the British Museum 1st edn (Lubrecht & Cramer Ltd, 1985).
Goodwin, Z. A., Harris, D. J., Filer, D., Wood, J. R. I. & Scotland, R. W. Widespread mistaken identity in tropical plant collections. Curr. Biol. 25, R1066–R1067 (2015).
The Science and Technology Committee Systematics and Taxonomy in Crisis (Authority of the House of Lords, 2008).
Riedel, A., Sagata, K., Suhardjono, Y. R., Tänzler, R. & Balke, M. Integrative taxonomy on the fast track - towards more sustainability in biodiversity research. Front. Zool. 10, 15 (2013).
Bradley, R. D., Bradley, L. C., Garner, H. J. & Baker, R. J. Assessing the value of natural history collections and addressing issues regarding long-term growth and care. BioScience 64, 1150–1158 (2014).
Plant Conservation Report. A Review of Progress in Implementing the Global Strategy for Plant Conservation (GSPC) (Convention on Biological Diversity, 2009).
Feeley, K. J. & Silman, M. R. The data void in modeling current and future distributions of tropical species. Glob. Change Biol. 17, 626–630 (2011).
Scotland, R. W. & Wood, J. R. I. Accelerating the pace of taxonomy. Trends Ecol. Evol. 27, 415–416 (2012).
Bisby, F. A., Shimura, J., Ruggiero, M., Edwards, J. & Haeuser, C. Taxonomy, at the click of a mouse. Nature 418, 367–367 (2002).
Joppa, L. N., Roberts, D. L. & Pimm, S. L. The population ecology and social behaviour of taxonomists. Trends Ecol. Evol. 26, 551–553 (2011).
Bacher, S. Still not enough taxonomists: reply to Joppa et al. Trends Ecol. Evol. 27, 65–66 (2012).
Wheeler, Q. D. et al. Mapping the biosphere: exploring species to understand the origin, organization and sustainability of biodiversity. Syst. Biodivers. 10, 1–20 (2012).
Costello, M. J., May, R. M. & Stork, N. E. Can we name Earth’s species before they go extinct? Science 339, 413–416 (2013).
Bebber, D. P., Wood, J. R. I., Barker, C. & Scotland, R. W. Author inflation masks global capacity for species discovery in flowering plants. New Phytol. 201, 700–706 (2014).
Wortley, A. H. & Scotland, R. W. Synonymy, sampling and seed plant numbers. TAXON 53, 478–480 (2004).
Tautz, D., Arctander, P., Minelli, A., Thomas, R. H. & Vogler, A. P. DNA points the way ahead in taxonomy. Nature 418, 479–479 (2002).
Tautz, D., Arctander, P., Minelli, A., Thomas, R. H. & Vogler, A. P. A plea for DNA taxonomy. Trends Ecol. Evol. 18, 70–74 (2003).
Chase, M. W. et al. Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann. Missouri Bot. Gard. 80, 528–580 (1993).
The Angiosperm Phylogeny Group An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot. J. Linn. Soc. 141, 399–436 (2003).
Hollingsworth, P. M., Li, D.-Z., van der Bank, M. & Twyford, A. D. Telling plant species apart with DNA: from barcodes to genomes. Phil. Trans. R. Soc. B 371, 20150338 (2016).
CBOL Plant Working Group et al. A DNA barcode for land plants. Proc. Natl Acad. Sci. USA 106, 12794–12797 (2009).
Weitemier, K. et al. Hyb-Seq: combining target enrichment and genome skimming for plant phylogenomics. Appl. Plant Sci. 2, 1400042 (2014).
Frodin, D. G. History and concepts of big plant genera. TAXON 53, 753–776 (2004).
Wood, J. et al. A foundation monograph of Convolvulus L. (Convolvulaceae). PhytoKeys 51, 1–282 (2015).
Doyle, J. J. Gene trees and species trees: molecular systematics as one-character taxonomy. Syst. Bot. 17, 144 (1992).
Muñoz-Rodríguez, P. et al. Reconciling conflicting phylogenies in the origin of sweet potato and dispersal to Polynesia. Curr. Biol. 28, 1246–1256 (2018).
Baldwin, B. G. Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae. Mol. Phylogenet. Evol. 1, 3–16 (1992).
Álvarez, I. & Wendel, J. F. Ribosomal ITS sequences and plant phylogenetic inference. Mol. Phylogenet. Evol. 29, 417–434 (2003).
Feliner, G. N. & Rosselló, J. A. Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Mol. Phylogenet. Evol. 44, 911–919 (2007).
Miller, R. E., Rausher, M. D. & Manos, P. S. Phylogenetic systematics of Ipomoea (Convolvulaceae) based on ITS and Waxy sequences. Syst. Bot. 24, 209–227 (1999).
Huang, J., Corke, H. & Sun, M. Highly polymorphic AFLP markers as a complementary tool to ITS sequences in assessing genetic diversity and phylogenetic relationships of sweetpotato (Ipomoea batatas (L.) Lam.) and its wild relatives. Genet. Resour. Crop Evol. 49, 541–550 (2002).
Roullier, C. et al. Disentangling the origins of cultivated sweet potato (Ipomoea batatas (L.) Lam.). PLoS ONE 8, e62707 (2013).
De Queiroz, K. Species concepts and species delimitation. Syst. Biol. 56, 879–886 (2007).
Wood, J. R. I., Bianchini, R. S. & Fuentes, A. F. in Catálogo de las Plantas Vasculares de Bolivia (eds Jorgensen, P. M. et al.) 520–531 (Missouri Botanical Garden Press, 2015).
Wood, J. R. I. et al. Ipomoea (Convolvulaceae) in Bolivia. Kew Bull. 70, 31 (2015).
Wood, J. R. I., Martinez Ugarteche, M. T., Muñoz-Rodríguez, P. & Scotland, R. W. Additional notes on Ipomoea (Convolvulaceae) in Bolivia. Kew Bull. 73, 57 (2018).
Wood, J. R. I., Muñoz-Rodríguez, P., Williams, B. R. M. & Scotland, R. W. A foundation monograph of Ipomoea (Convolvulaceae) in the New World. Phytokeys (in the press).
Wood, J. R. I., de Arrúa, R. D., de Rojas, G. D. & Scotland, R. W. Two overlooked species of Ipomoea L. (Convolvulaceae) from Paraguay. Kew Bull. 71, 25 (2016).
Wood, J. R. I., Urbanetz, C. & Scotland, R. W. Ipomoea pantanalensis, a new species of Ipomoea L. (Convolvulaceae) from the Pantanal, Brazil. Kew Bull. 71, 6 (2016).
Wood, J. R. I. & Scotland, R. W. Notes on Ipomoea L. (Convolvulaceae) in Cuba and neighbouring islands with a checklist of species found in Cuba. Kew Bull. 72, 45 (2017).
Wood, J. R. I. & Scotland, R. W. Misapplied names, synonyms and new species of Ipomoea (Convolvulaceae) from South America. Kew Bull. 72, 9 (2017).
Wood, J. R. I. & Scotland, R. W. Notes on Ipomoea (Convolvulaceae) from the Amazonian periphery. Kew Bull. 72, 10 (2017).
Wood, J. R. I., Muñoz-Rodríguez, P., Degen, R. & Scotland, R. W. New species of Ipomoea (Convolvulaceae) from South America. PhytoKeys 88, 1–38 (2017).
Wood, J. R. I., Buril, M. T. & Scotland, R. W. Remarkable disjunctions in Ipomoea species (Convolvulaceae) from NE Brazil and Central America and their taxonomic implications. Kew Bull. 72, 44 (2017).
Wood, J. R. I., Vasconcelos, L. V., Simão-Bianchini, R. & Scotland, R. W. New species of Ipomoea (Convolvulaceae) from Bahia. Kew Bull. 72, 8 (2017).
Wilkin, P. A morphological cladistic analysis of the Ipomoeeae (Convolvulaceae). Kew Bull. 54, 853–876 (1999).
Beerling, D. J. & Osborne, C. P. The origin of the savanna biome. Glob. Change Biol. 12, 2023–2031 (2006).
Scheiter, S. et al. Fire and fire-adapted vegetation promoted C4 expansion in the late Miocene. New Phytol. 195, 653–666 (2012).
Baldwin, B. G. & Sanderson, M. J. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl Acad. Sci. USA 95, 9402–9406 (1998).
Hughes, C. & Eastwood, R. Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc. Natl Acad. Sci. USA 103, 10334–10339 (2006).
Givnish, T. J. et al. Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae). Proc. R. Soc. B 276, 407–416 (2009).
Koenen, E. J. M. et al. Exploring the tempo of species diversification in legumes. South Afr. J. Bot. 89, 19–30 (2013).
Zhang, D., Cervantes, J., Huamán, Z., Carey, E. & Ghislain, M. Assessing genetic diversity of sweet potato (Ipomoea batatas (L.) Lam.) cultivars from tropical America using AFLP. Genet. Resour. Crop Evol. 47, 659–665 (2000).
Roullier, C., Kambouo, R., Paofa, J., McKey, D. & Lebot, V. On the origin of sweet potato (Ipomoea batatas (L.) Lam.) genetic diversity in New Guinea, a secondary centre of diversity. Heredity 110, 594–604 (2013).
Yang, J. et al. Haplotype-resolved sweet potato genome traces back its hexaploidization history. Nat. Plants 3, 696–703 (2017).
Wu, S. et al. Genome sequences of two diploid wild relatives of cultivated sweetpotato reveal targets for genetic improvement. Nat. Commun. 9, 4580 (2018).
Austin, D. F. The Ipomoea batatas complex-I. Taxonomy. Bull. Torrey Bot. Club 105, 114–129 (1978).
Harris, D. J. & Wortley, A. H. Monograph of Aframomum (Zingiberaceae) (The American Society of Plant Taxonomists, 2018).
Drew, L. W. Are we losing the science of taxonomy? As need grows, numbers and training are failing to keep up. BioScience 61, 942–946 (2011).
Thiers, B. Index Herbariorum: A Global Directory of Public Herbaria and Associated Staff (New York Botanical Garden’s Virtual Herbarium, 2018).
Katoh, K. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).
Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).
Bruen, T. C. A simple and robust statistical test for detecting the presence of recombination. Genetics 172, 2665–2681 (2005).
Sanderson, M. J. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19, 101–109 (2002).
Smith, S. A. & O’Meara, B. C. treePL: divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics 28, 2689–2690 (2012).
Hohna, S. et al. RevBayes: Bayesian phylogenetic inference using graphical models and an interactive model-specification language. Syst. Biol. 65, 726–736 (2016).
Rabosky, D. L. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9, e89543 (2014).
Acknowledgements
We acknowledge the financial support of The Leverhulme Trust for our Ipomoea Foundation Monograph project and the University of Oxford through The John Fell Fund for travel and sequencing costs. P.M.-R. was funded by a BBSRC scholarship granted through the Interdisciplinary Bioscience DTP Programme and by the University of Oxford Global Challenges Research Fund; he also received additional funding from a Santander Travel Award and from the Synthesys project (FR-TAF-6575). J.R.I.W. received travel awards from the Synthesis project to visit Paris (FR-TAF), Madrid (ES-TAF) and Stockholm (SE-TAF) and B.R.M.W. received a Synthesis travel award to visit Leiden (NF-TAF). R.W.S. and P.M.-R. acknowledge funding from the BBSRC GCRF-IAA fund (BB/GCRF-IAA/16 and BB/GCRF-IAA/17/16). T.C. was funded by a NERC scholarship granted through the Environmental Research DTP Programme. We thank all herbarium curators for granting access to their collections. We thank T. Wells for his comments on the genomic analyses. We also thank all colleagues who contributed to this project through fieldwork and continuous discussion (see the list in Supplementary Information, Section 7).
Author information
Authors and Affiliations
Contributions
Conceptualization, supervision and project administration was performed by R.W.S. Funding acquisition was performed by R.W.S., J.R.I.W., P.M.-R. and T.C. Methodology was defined by R.W.S., J.R.I.W., A.L., S.K., K.W., B.K., D.H., D.F., P.M.-R. and T.C. Resources were obtained by J.R.I.W., B.R.M.W., P.M.-R., A.S., Z.G., N.L.A. and M.D.R. Formal analysis and investigation were performed by P.M.-R., T.C. and J.R.I.W. Writing of the original draft was performed by P.M.-R., R.W.S., T.C. and J.R.I.W., and writing and review of the final draft was performed by all authors. Visualization and image design was performed by P.M.-R.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Peer review information Nature Plants thanks Matt Lavin, Quentin Wheeler and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data
Extended Data Fig. 1 DNA barcode sequences used and statistics.
3,035 DNA barcode sequences were obtained from herbarium specimens spanning the last two and a half centuries. 88.5% specimens were collected in the last 50 years and 22 samples came from pre-20th century collections.
Extended Data Fig. 2 Use of ITS phylogeny in the taxonomic process.
We used the ITS phylogeny of Ipomoea as a single taxonomic character. a, We inferred a ML tree that included, when possible, multiple accessions of each putative species and interpreted it in three distinct ways, monophyly of accessions, non-monophyly and distantly related, non-monophyly but closely related. b, accessions of a given species are monophyletic (black triangles). Also, two existing species (I. piurensis and I. acanthocarpa) that we considered conspecific formed a clade of accessions that are intermingled (dashed-line green box), confirming our hypothesis. c, accessions of a given species are non-monophyletic and appear in very different parts of the Ipomoea phylogeny. In the example shown, our hypothesis based on morphology was a monophyletic I. squamosa but the ITS tree split the specimens, with some forming a clade in clade D and others forming a clade in clade A which is very distantly related to clade D. In such cases, we re-examined the morphology and usually found a mis-identified specimen(s). In other cases, specimens were similar on herbarium sheets but could be distinguished on closer inspection. In this case, the ITS tree alerted us to re-examine and have a closer look at specimens and subsequently describe the new species I. cryptica. d–e, in some parts of the ITS phylogeny there was a lack of resolution, with only a small number of subclades recognised and generally lacking support. Here we show an example with the clade including sweet potato. In such cases, we did not follow the ITS phylogeny but relied on morphology and genomic data when available. This decision was based on the fact that f, genomic phylogenies for the sweet potato clade demonstrate that nearly all species are monophyletic.
Extended Data Fig. 3 Summary genomic phylogenies of Ipomoea.
Summary phylogeny of Ipomoea inferred from A) 605 putative single-copy nuclear coding regions using Astral-II and B) whole chloroplast genomes using Maximum Likelihood showing the main clades identified in the genus. See Supplementary Discussion, Phylogeny of Ipomoea. Complete phylogenies in Supplementary data files 3–7.
Extended Data Fig. 4 Patterns of diversification-rate-variation in nuclear time-calibrated phylogenies inferred with smoothing values that differ from the optimum.
The coloured tree in each sub-figure represents the pattern of diversification-rate-variation with the highest posterior probability and the posterior probability is shown in the top left corner of each sub-figure. If present, alternative patterns of diversification-rate-variation that have a posterior probability of greater than 0.05 are indicated with coloured arrows, with the position of the arrow indicating the position of the diversification rate shift. Arrows with the same colour indicate a single set of diversification rate shifts that have a specific posterior probability (indicated next to one arrow for each colour). a) A single rate shift at the origin of the diverse South America and Central American clades has a posterior probability of 0.98. b) A single rate shift at the origin of the diverse South America and Central American clades has a posterior probability of 0.98. c) A single rate shift at the origin of the diverse South America and Central American clades has a posterior probability of 0.98.
Extended Data Fig. 5 Patterns of diversification-rate-variation in the chloroplast time-calibrated phylogeny inferred with the optimum smoothing value.
The coloured tree, posterior probabilities, and coloured arrows are indicated according to the same conventions as Extended Data Fig. 4. A single rate increase near the origin of the diverse South American clade has a posterior probability of 0.8. Two alternative patterns of diversification-rate-variation, where there are rate increases on immediately ancestral branches, have posterior probabilities of 0.11 and 0.058.
Extended Data Fig. 6 Patterns of diversification-rate-variation in chloroplast time-calibrated phylogenies inferred with smoothing values that differ from the optimum.
The coloured trees, posterior probabilities, and coloured arrows are indicated according to the same conventions as Extended Data Fig. 4. a) A model with no discrete rate shifts has a posterior probability of 0.54. Two alternative patterns of diversification-rate-variation, where there are rate increases near the origin of the diverse South American clade, have posterior probabilities of 0.34 and 0.058 respectively. b) A single rate shift near the origin of the diverse South American clade has a posterior probability of 0.51. An alternative pattern of diversification-rate-variation, where there is a rate increase on immediately ancestral branch, has a posterior probability of 0.088. c) A single rate shift at the origin of the diverse South American clade has a posterior probability of 0.81. An alternative pattern of diversification-rate-variation, where there is a rate increase on an immediately ancestral branch, has a posterior probability of 0.11.
Extended Data Fig. 7 Biome occupancy and growth habit of sampled taxa for the clades with elevated speciation rates.
A section of the time-calibrated phylogeny shown in Fig. 4, for which elevated speciation rates were inferred. Biome occupancy and growth habit of sampled taxa are indicated. This indicates that there are likely to have been multiple shifts into and out of fire-adapted cerrado-type habitats, and multiple shifts between different growth forms amongst recently diverged taxa.
Supplementary information
Supplementary Information
Supplementary Methods, Supplementary Discussion, Supplementary Tables and Supplementary References.
Supplementary Data 1
GBIF data of Ipomoea.
Supplementary Data 2
Passport data of all accessions used in this study.
Supplementary Data 3
ITS phylogeny of Ipomoea.
Supplementary Data 4
Nuclear phylogeny of Ipomoea inferred from gene trees using the coalescent.
Supplementary Data 5
Nuclear phylogeny of Ipomoea inferred from concatenated alignments.
Supplementary Data 6
Chloroplast phylogeny of Ipomoea inferred using Bayesian inference.
Supplementary Data 7
Chloroplast phylogeny of Ipomoea inferred using maximum likelihood.
Supplementary Data 8
Chloroplast phylogeny of Ipomoea inferred using parsimony.
Supplementary Data 9
Chloroplast phylogeny used to estimate diversity existing within the crop.
Supplementary Data 10
Nuclear phylogeny used to estimate diversity existing within the crop.
Rights and permissions
About this article
Cite this article
Muñoz-Rodríguez, P., Carruthers, T., Wood, J.R.I. et al. A taxonomic monograph of Ipomoea integrated across phylogenetic scales. Nat. Plants 5, 1136–1144 (2019). https://doi.org/10.1038/s41477-019-0535-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41477-019-0535-4
- Springer Nature Limited
This article is cited by
-
A Review of Taxonomic Concepts and Species Delimitation in Cycadales
The Botanical Review (2024)
-
Pressed for space
Nature Plants (2023)
-
Influence of incompatible pollen grains on the reproductive success of Ipomoea asarifolia (Desr.) Roem. & Schult. (Convolvulaceae) in Restinga, RN, Brazil
Brazilian Journal of Botany (2023)
-
Plant taxonomic species and their role in the workflow of integrative species delimitation
Kew Bulletin (2022)
-
Reduction of Blinkworthia (Convolvulaceae) based on multilocus phylogenetic reconstruction and resurrection of a species from synonymy revealed by phenetic analyses
Kew Bulletin (2022)