Abstract
Nothapodytes (Icacinaceae) is a genus of seven to eleven evergreen or deciduous tree species distributed in tropical Asia from India to Japan. Nothapodytes nimmoniana sensu lato is the most widespread species of the genus, being reported sporadically throughout South Asia, Southeast Asia, Taiwan, and Japan’s southwest islands. Nothapodytes amamianus was recently described from Amami-oshima, Japan, the northeastern edge of this widespread species’ range. However, the phylogenetic distinction between these two species has yet to be explored. Here we present an analysis of molecular species delimitation to test the morphology-based taxonomic hypothesis currently used to differentiate the two species. The results clearly show that N. nimmoniana sensu lato comprises two species, one in India and the other in Taiwan and Japan, including N. amamianus, requiring a reassessment of the morphological traits hitherto used to define the former and distinguish it from the latter in East Asia. Based on the taxonomic history of the taxa and rules of nomenclature, the name N. nimmoniana is retained for the former. We propose a new combination, N. insularis, for the latter. Longitudinal intraspecific geographic structure is highlighted as an apparent indicator of further hidden diversity in India’s Western Ghats.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The datasets generated during and/or analyzed during the current study are available in GenBank and TreeBASE Web (TB2:S27743).
Code availability
Not applicable.
References
Bouckaert RR, Heled J, Kühnert D, Vaughan TG, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLOS Comput Biol 10:e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Byng JW, Bernardini B, Joseph JA, Chase MW, Utteridge TMA (2014) Phylogenetic relationships of Icacinaceae s.s. focusing on the vining genera. Bot J Linn Soc 176:277–294. https://doi.org/10.1111/boj.12205
Chang CE (1993) Icacinaceae. In Huang TC, Huang CF, Li ZY, Lo HC, Ohashi H, Shen CF, Wang CJ (eds), Flora of Taiwan, 2nd ed, vol. III. Committee of Flora of Taiwan, Taipei, pp 674–679
National Plant Specimen Resource Center (2021) Chinese Virtual Herbarium. Available at: http://www.cvh.org.cn/. Accessed 16 Jan 2021
Davis CD, Anderson WR, Donoghue MJ (2001) Phylogeny of Malpighiaceae: evidence from chloroplast ndhF and trnL-F nucleotide sequences. Amer J Bot 88:1830–1846. https://doi.org/10.2307/3558360
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214–222. https://doi.org/10.1186/1471-2148-7-214
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLOS Biol 4:e88. https://doi.org/10.1371/journal.pbio.0040088
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Flouri T, Jiao X, Rannala B, Yang Z (2018) Species tree inference with BPP using genomic sequences and the multispecies coalescent. Molec Biol Evol 35:2585–2593. https://doi.org/10.1093/molbev/msy147
Fujita MK, Leaché AD, Burbrink FT, McGuire JA, Moritz C (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends Ecol Evol 27:480–488. https://doi.org/10.1016/j.tree.2012.04.012
GBIF Secretariat (2019) GBIF Backbone Taxonomy. Checklist dataset https://doi.org/10.15468/39omei accessed via GBIF.org on 2021-01-11
Graham J (1839) A catalogue of the plants growing in Bombay and its vicinity. Government Press, Bombay
Hatusima S (1956) New and noteworthy plants from the Ryukyu Islands and Formosa. Sci Bull Agric Div Univ Ryukyus 3:19–33
Hatusima S, Amano T (1994) Flora of the Ryukyus, south of Amami Island. The Biological Society of Okinawa, Naha
Howard RA (1942) Studies of the Icacinaceae, II. Humirianthera, Leretia, Mappia, and Nothapodytes, valid genera of the Icacineae. J Arnold Arbor 23:55–78
Ito Y, Tanaka N, Barfod AS, Bogner J, Li J, Yano O, Gale SW (2019) Molecular phylogenetic species delimitation in the aquatic genus Ottelia (Hydrocharitaceae) reveals cryptic diversity within a widespread species. J Pl Res 132:335–344. https://doi.org/10.1007/s10265-019-01109-7
Johnson LA, Soltis DE (1994) MatK sequences and phylogenetic reconstruction in Saxifragaceae s. str. Syst Bot 19:143–156
Jones GL, Aydin Z, Oxelman B (2015) DISSECT: an assignment-free Bayesian discovery method for species delimitation under the multispecies coalescent. Bioinformatics 31:991–998. https://doi.org/10.1093/bioinformatics/btu770
Jones GL (2017) Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. J Math Biol 74:447–467. https://doi.org/10.1007/s00285-016-1034-0
Kareem AVK, Rajasekharan PE, Mini S, Kumar VT (2011) Genetic diversity and structure of the threatened anti-cancerous plant Nothapodytes nimmoniana as revealed by ISSR analysis. Pl Genet Resources 9:506–514. https://doi.org/10.1017/S1479262111000803
Kårehed J (2001) Multiple origin of the tropical forest tree family Icacinaceae. Amer J Bot 88:2259–2274. https://doi.org/10.2307/3558388
Kato H, Oginuma K, Gu Z, Hammel B, Tobe H (1998) Phylogenetic relationships of Betulaceae based on matK sequences with particular reference to the position Ostryopsis. Acta Phyototax Geobot 49:89–97
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molec Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Kornhall P, Heidari N, Bremer B (2001) Selagineae and Munuleeae, two tribes or one? Phylogenetic studies in the Scrophulariaceae. Pl Syst Evol 1228:199–218. https://doi.org/10.1007/s006060170029
Kozlov A, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable, and user-friendly tool for maximum-likelihood phylogenetic inference. Bioinformatics 35:4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Li ZZ, Ngarega BK, Lehtonen S, Gichira AW, Karichu MJ, Wang QF, Chen JM (2020) Cryptic diversity within the African aquatic plant Ottelia ulvifolia (Hydrocharitaceae) revealed by population genetic and phylogenetic analyses. J Pl Res 133:373–381. https://doi.org/10.1007/s10265-020-01175-2
Mabberley DJ (1980) A re-examination of the “Indian Catalogues” with particular reference to Hortus Malabaricus. In: Manilal KS (ed), Botany and History of Hortus Malabaricus. Oxford & IBH Publ. Co., New Delhi, pp 80–110
Matsumura J (1901) Notulæ ad Plantas Asiaticas Orientales (Continued from p. 41.). Bot Mag Tokyo 15:53–58
Miers J (1852) On some genera of the Icacinaceae. Ann Mag Nat Hist, Ser 2 9: 387–399.
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop (GCE), 14 Nov 2010, New Orleans, pp 1–8. http://www.phylo.org/sub_sections/portal/cite.php
Nagamasu H, Kato M (2004) Nothapodytes amamianus (Icacinaceae), a new species from the Ryukyu Islands. Acta Phytotax Geobot 55:75–78
Nylander JAA (2002) MrModeltest. Ver. 1.0. Program distributed by the author. Department of Systematic Zoology, Uppsala University, Uppsala. Retrieved from https://www.ebc.uu.se/systzoo/staf/nylander.html
Olmstead RG, Sweere JA (1994) Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae. Syst Biol 43:467–481. https://doi.org/10.1093/sysbio/43.4.467
Ooi K, Endo Y, Yokoyama J, Murakami N (1995) Useful primer designs to amplify DNA fragments of the plastid gene matK from angiosperm plants. J Jap Bot 70:328–331
Pelser PB, Barcelona JF, Nickrent DL (eds) (2011 onwards.) Co's Digital Flora of the Philippines. Available at: www.philippineplants.org
Peng H, Howard RA (2008) Icacinaceae. In: Wu C-Y, Raven PH, Hong D-Y (eds) Flora of China, vol. 11. Science Press. Beijing & Missouri Botanical Garden Press, St. Louis, pp 505–514
Potgieter MJ, Duno R (2016) Icacinaceae. In: Kadereit JW and Bittrich V (eds.) Flowering Plants. Eudicots, The Families and Genera of Vascular Plants 14. Springer, pp 239–256. https://doi.org/10.1007/978-3-319-28534-4_21
R Core Team (2018) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available at: https://www.R-project.org
Rambaut A (2009) FigTree, version 1.3.1. Computer program distributed by the author. Available at: http://www.treebioedacuk/software/figtree. Accessed 13 Dec 2019
Rambaut A, Suchard MA, Xie W, Drummond AJ (2014) Tracer. ver. 1.6. Available at: http://beast.bio.ed.ac.uk/Tracer
Rannala B (2015) The art and science of species delimitation. Curr Zool 61:846–853. https://doi.org/10.1093/czoolo/61.5.846
Rannala B, Yang Z (2003) Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164:1645–1656
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efcient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
Shivaprakash KN, Ramesha BT, Uma Shaanker R, Dayanandan S, Ravikanth G (2014) Genetic structure, diversity and long term viability of a medicinal plant, Nothapodytes nimmoniana Graham. (Icacinaceae), in protected and non-protected areas in the Western Ghats biodiversity hotspot. PLOS ONE 9:e112769. https://doi.org/10.1371/journal.pone.0112769
Sleumer H (1940) Beiträge zur Kenntnis der Icacinaceen und Peripterygiaceen. Notizbl Bot Gart Berlin-Dahlem 15:228–257
Sleumer H (1969) Materials towards the knowledge of the Icacinaceae of Asia, Malesia, and adjacent areas. Blumea 17:181–264
Sleumer H (1971) Icacinaceae. Fl Males Ser I 7:1–87
Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771. https://doi.org/10.1080/10635150802429642
Stuessy TF (2009) Plant Taxonomy: The Systematic Evaluation of Comparative Data, 2nd edn. Columbia University Press, New York
Stull GW, Duno de Stefano R, Soltis DE, Soltis PS (2015) Resolving basal lamiid phylogeny and the circumscription of Icacinaceae with a plastome-scale data set. Amer J Bot 102:1794–1813. https://doi.org/10.3732/ajb.1500298
Swofford DL (2002) PAUP: Phylogenetic analysis using parsimony (and other methods), ver. 40b10. Sinauer Associates, Sunderland
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109. https://doi.org/10.1007/BF00037152
Turland NJ, Wiersema JH, Barrie FR, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Kusber WH, Li DZ, Marhold K, May TW, McNeill J, Monro AM, Prado J, Price MJ, Smith GF (2018) International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code). Regnum Vegetabile 159. Koeltz Botanical Books, Glashütten
White TJ (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols, a Guide to Methods and Applications. Academic Press Inc., San Diego, pp 315–322
Yang Z (2015) The BPP program for species tree estimation and species delimitation. Curr Zool 61:854–865. https://doi.org/10.1093/czoolo/61.5.854
Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Molec Biol Evol 14:717–724
Yang Z, Rannala B (2010) Bayesian species delimitation using multilocus sequence data. Proc Natl Acad Sci USA 107:9264–9269. https://doi.org/10.1073/pnas.0913022107
Yang Z, Rannala B (2014) Unguided species delimitation using DNA sequence data from multiple loci. Molec Biol Evol 31:3125–3135. https://doi.org/10.1093/molbev/msu279
Acknowledgments
The authors thank Nb. Tanaka (TNS), J. Murata (TI), A. Naiki (Okinawa), and T. Yahara and A. Nagahama (FU) for providing materials or assistance in the field, S. Gale (KFBG) for improving an earlier draft of the manuscript, and S. Higashimukai (Osaka) for help with DNA sequencing. This research was partly supported by the University of the Ryukyus Research Project Promotion Grant (Strategic Research Grant) (No. 17SP01302) and partly supported by the Environment Research and Technology Development Fund (JPMEERF20204003) of the Environmental Restoration and Conservation Agency of Japan.
Funding
This study was funded by the University of the Ryukyus Research Project Promotion Grant (Strategic Research Grant) (No. 17SP01302) and the Environment Research and Technology Development Fund (JPMEERF20204003).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Handling editor: Hiroshi Kudoh.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
606_2021_1797_MOESM1_ESM.pdf
Online Resource 1. The summarized differences in Nothapodytes in clustering based on Stacey and BPP analyses outputs. Numbers of samples are shown in parentheses.
606_2021_1797_MOESM2_ESM.pdf
Online Resource 2. Summary of infra-and inter-specific similarity scores for Nothapodytes species based on Stacey analysis.
Information on electronic supplementary material
Information on electronic supplementary material
Online Resource 1. The summarized differences in Nothapodytes in clustering based on Stacey and BPP analyses outputs. Numbers of samples are shown in parentheses.
Online Resource 2. Summary of infra-and inter-specific similarity scores for Nothapodytes species based on Stacey analysis.
Rights and permissions
About this article
Cite this article
Ito, Y., Yadav, S.R., Chang, Y.S. et al. Molecular species delimitation reveals underestimated diversity in the tree genus Nothapodytes (Icacinaceae). Plant Syst Evol 308, 3 (2022). https://doi.org/10.1007/s00606-021-01797-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-021-01797-6