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A taxonomic monograph of Ipomoea integrated across phylogenetic scales

Nature Plants volume 5, pages 1136–1144 (2019)Cite this article

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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.

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Fig. 1: Natural history collections facilitate biodiversity studies at a global scale.
Fig. 2: Integrating morphology and DNA in global taxonomic studies is key to utilizing the resources of natural history collections.
Fig. 3: Megadiverse plant groups demand a global approach.
Fig. 4: Rapid radiations in Ipomoea.
Fig. 5: Storage roots evolved multiple times independently in Ipomoea.
Fig. 6: Diversity within sweet potato predates agriculture.

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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.

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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).

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Author notes

  1. These authors contributed equally: Pablo Muñoz-Rodríguez, Tom Carruthers.

Authors and Affiliations

  1. Department of Plant Sciences, University of Oxford, Oxford, UK

    Pablo Muñoz-Rodríguez, Tom Carruthers, John R. I. Wood, Bethany R. M. Williams, Alex Sumadijaya, Denis Filer, Steven Kelly & Robert W. Scotland

  2. Royal Botanic Gardens, Kew, Richmond, UK

    John R. I. Wood

  3. Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR, USA

    Kevin Weitemier

  4. Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR, USA

    Brent Kronmiller

  5. Royal Botanic Garden Edinburgh, Edinburgh, UK

    Zoë Goodwin & David Harris

  6. International Potato Center, Lima, Peru

    Noelle L. Anglin

  7. French Family Science Center, Duke University, Durham, NC, USA

    Mark D. Rausher

  8. Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, USA

    Aaron Liston

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  1. Pablo Muñoz-Rodríguez
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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

Correspondence to Robert W. Scotland.

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The authors declare no competing interests.

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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.

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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.

Reporting Summary

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.

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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

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