Login | Register

Origin and evolution of the genus Piper in Peninsular India


Origin and evolution of the genus Piper in Peninsular India

Sen, Sandeep, Dayanandan, Selvadurai, Davis, Thomson, Ganesan, Rengaian, Jagadish, M.R., Mathew, P.J. and Ravikanth, Gudasalamani (2019) Origin and evolution of the genus Piper in Peninsular India. Molecular Phylogenetics and Evolution . ISSN 10557903 (In Press)

Text (in press, accepted manuscript) (application/pdf)
Origin-and-evolution-of-the-genus-Piper-in-P_2019_Molecular-Phylogenetics-an.pdf - Accepted Version
Available under License Creative Commons Attribution Non-commercial No Derivatives.

Official URL: http://dx.doi.org/10.1016/j.ympev.2019.05.033


The evolution of Peninsular Indian biodiversity has been a fascinating topic of research due to historical connections of this region to the ancient Gondwanaland. We investigated the phylogeny and historical biogeography of nearly all extant species of the genus Piper reported from the region to assess the biogeographical origins and test mechanisms of lineage diversification (dispersal, vicariance and in situ radiation) of this highly diverse genus of angiosperms commonly found in the understory of evergreen forests. The phylogeny of 21 species of Piper reported from Peninsular India was reconstructed for the first time, which included three new putative species from the Western Ghats. We used BEAST for the divergence time estimations (using three constraints), and ancestral range estimations were performed with the dated phylogenetic tree using BIOGEOBEARS. Divergence dating analysis revealed that the genus Piper originated during lower Cretaceous around 110Ma [95% highest posterior density (HPD): 116-105 Ma] and colonized Peninsular India five times independently, from Southeast Asia starting from the Oligocene. The two major dispersals into India occurred during the periods of 27.3Ma (95% HPD: 35.8 - 19.9.) and 15.5Ma (95% HPD: 24.9 - 7.11). This was followed by rapid radiations in some lineages with subsequent back dispersals to Southeast Asia. Our study indicates that dispersals from Southeast Asia led to the arrival of Piper to Indian subcontinent following the Indo-Eurasian collision. Members of Piper have colonized and diversified within the climatically stable habitats of Peninsular India. Furthermore, the present study provides evidence for the Miocene overland dispersal of Piper species to Africa from South Asia.

Divisions:Concordia University > Faculty of Arts and Science > Biology
Item Type:Article
Authors:Sen, Sandeep and Dayanandan, Selvadurai and Davis, Thomson and Ganesan, Rengaian and Jagadish, M.R. and Mathew, P.J. and Ravikanth, Gudasalamani
Journal or Publication:Molecular Phylogenetics and Evolution
Date:25 May 2019
  • International Association for Plant Taxonomy (IAPT, 2014)
  • Department of Biotechnology (DBT)
  • DST SERB (No EMR/2017/001269)
  • Canadian Commonwealth scholarship
  • NSERC Discovery Grant
Digital Object Identifier (DOI):10.1016/j.ympev.2019.05.033
Keywords:dispersal; shistorical biogeography; India–Asia collision; Piper; phylogeny; Western Ghats
ID Code:985469
Deposited By: MONIQUE LANE
Deposited On:06 Jun 2019 17:48
Last Modified:24 May 2020 00:00


I. Agarwal, K.P. Karanth A phylogeny of the only ground-dwelling radiation of Cyrtodactylus (Squamata, Gekkonidae): diversification of Geckoella across peninsular India and Sri Lanka Mol Phylogenet Evol., 82 (2015), pp. 193-199

I. Agarwal, A.M. Bauer, T.R. Jackman, K.P. Karanth Insights into Himalayan biogeography from geckos: A molecular phylogeny of Cyrtodactylus (Squamata: Gekkonidae) Mol Phylogenet Evol., 80 (2014), pp. 145-155

to Asia: plate tectonics, paleogeography and the biological connectivity of the Indian sub-continent from the Middle Jurassic through latest Eocene (166–35 Ma) Earth Sci. Rev., 88 (2008), pp. 145-166

Ajith Anand, Chaluvadi Srinivasa Rao A rapid in vitro propagation protocol for Piper barberi Gamble, a critically endangered plant In Vitro Cell.Dev.Biol.-Plant, 36 (1) (2000), pp. 61-64

R. Asmarayani Phylogenetic relationships in Malesian-Pacific Piper (Piperaceae) and their implications for systematics
Taxon., 67 (2018), pp. 693-724

K.N. Babu, R.R. Nair, G.K. Johnson, P.N. Ravindran Piper barberi Gamble- a re description of the species with a note on the karyotype J Spices aromatic Crop., 1 (1992), pp. 88-93

R. Bansal, K.P. Karanth Molecular phylogeny of Hemidactylus geckos (Squamata: Gekkonidae) of the Indian subcontinent reveals a unique Indian radiation and an Indian origin of Asian house geckos
Mol Phylogenet Evol., 57 (2010), pp. 459-465

S.D. Biju, F. Bossuyt New frog family from India reveals an ancient biogeographical link with the Seychelles Nature., 425 (2003), pp. 711-714

F. Bossuyt, M.C. Milinkovitch Amphibians as Indicators of Early Tertiary “Out-of-India” dispersal of vertebrates Science., 292 (2001), pp. 93-95

J.C. Briggs The biogeographic and tectonic history of India
J. Biogeogr., 30 (2003), pp. 381-388

Callejas, R., 2002. Micromorfologı́a de las semillas en el género Piper. Libro de Resúmenes Octavo Congreso latinoamericano y Segundo Colombiano de Botánica (ed. by J.O. Rangel, J. Aguirre and M.G. Andrade), 435 pp. Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Colombia

E. Conti, T. Eriksson, J. Schönenberger, K.J. Sytsma, D.A. Baum Early Tertiary out-of-India dispersal of Crypteroniaceae: evidence from phylogeny and molecular dating Evolution., 56 (2002), pp. 1931-1942

D. Darriba, G.L. Taboada, R. Doallo, D. Posadaj ModelTest 2: more models, new heuristics and parallel computing Nat. Methods., 9 (2012), p. 772

A. Datta-Roy, K.P. Karanth The Out-of-India hypothesis: What do molecules suggest? J. Biosci., 34 (2009), pp. 687-697

A. Datta-Roy, M. Singh, C. Srinivasulu, K.P. Karanth Phylogeny of the Asian Eutropis (Squamata: Scincidae) reveals an ‘into India’endemic Indian radiation Mol Phylogenet Evol., 63 (2012), pp. 817-824

S. Dayanandan, P.S. Ashton, S.M. Williams, R.B. Primack Phylogeny of the tropical tree family Dipterocarpaceae based on nucleotide sequences of the chloroplast rbcL gene Am J Bot., 86 (1999), pp. 1182-1190

A.J. Drummond, M.A. Suchard, D. Xie, A. Rambaut Bayesian phylogenetics with BEAUti and BEAST 1.7 Mol Biol Evol., 29 (2012), pp. 1969-1973

L.A. Dyer, A.D. Palmer (Eds.), Piper: a model genus for studies of phytochemistry, ecology, and evolution, Kluwer academic/Plenum publishers, New York(2004), pp. 117-134
D.J. Gower, I. Agarwal, K.P. Karanth, A. DattaRoy, V.B. Giri, M. Wilkinson, D.San Mauro The role of wet zone fragmentation in shaping biodiversity patterns in peninsular India: insights from the caecilian amphibian Gegeneophis J. Biogeogr., 43 (2016), pp. 1091-1102

L.J. Harmon, J.T. Weir, C.D. Brock, R.E. Glor, W. Challenger GEIGER: investigating evolutionary radiations Bioinformatics., 24 (2008), pp. 129-131

D.H. Huson, D. Bryant Application of phylogenetic networks in evolutionary studies Mol Biol Evol., 23 (2006), pp. 254-267

M.A. Jaramillo, R. Callejas, C. Davidson, J.F. Smith, A.C. Stevens, E.J. Tepe A phylogeny of the tropical genus Piper using ITS and the chloroplast intron psbJ–petA Syst Botany., 33 (2008), pp. 647-660

J. Joshi, P. Karanth Did southern Western Ghats of peninsular India serve as a refugia for its endemic biota during the Cretaceous volcanism? Ecol. Evol., 10 (2013), pp. 3275-3282

Joshi, J., & Edgecombe, G. D., 2019. Evolutionary biogeography of the centipede genus Ethmostigmus from Peninsular India: testing an ancient vicariance hypothesis for Old World tropical diversity. BMC Evol Biol.19.

K.P. Karanth An island called India: phylogenetic patterns across multiple taxonomic groups reveal endemic radiations
Curr Sci., 108 (2015), pp. 1847-1851

K. Katoh, D.M. Standley MAFFT multiple sequence alignment software version 7: improvements in performance and usability Mol Biol Evol., 30 (2013), pp. 772-780

S. Klaus, R.J. Morley, M. Plath, Y.P. Zhang, J.T. Li Biotic interchange between the Indian subcontinent and mainland Asia through time
Nat. Commun., 7 (2016), p. 12132

F. Koehler, M. Glaubrecht Out of Asia and into India: on the molecular phylogeny and biogeography of the endemic freshwater gastropod Paracrostoma Cossmann, 1900 (Caenogastropoda: Pachychilidae) Biol J Linnean Soc., 91 (2007), pp. 627-651

M.J. Landis, N.J. Matzke, B.R. Moore, J.P. Huelsenbeck Bayesian analysis of biogeography when the number of areas is large Syst Biol., 62 (2013), pp. 789-804

M.S. Mani Biogeography in India Surya Publications, Dehra Dun, India (1995)

Mani, M.S., 1974. Biogeography of Peninsula, In: Ecology and biogeography in India (The Hague: Dr W Junk Publishers) pp 614-646.

C. Martínez, M.R. Carvalho, S. Madriñán, C.A. Jaramillo A Late Cretaceous Piper (Piperaceae) from Colombia and diversification patterns for the genus Am J Bot., 102 (2015), pp. 273-289

N.J. Matzke Founder-event speciation in BioGeoBEARS package dramatically improves likelihoods and alters parameter inference in Dispersal-Extinction-Cladogenesis (DEC) analyses Front Biogeogr., 4 (2012), p. 210

Matzke, N. J., 2013. BioGeoBEARS: Biogeography with Bayesian (and Likelihood) evolutionary analysis in R scripts. Retrieved from http://cran.r-project.or/web/packages/BioGeoBEARS/ (last accessed 20 December 2017)

I. Metcalfe Gondwana dispersion and Asian accretion: tectonic and palaeogeographic evolution of eastern Tethys J. Asian Earth Sci., 66 (2013), pp. 1-33

Miller, M.A., Pfeiffer, W., Schwartz, T., 2010. Creating the CIPRES science gateway for inference of large phylogenetic trees. In Institute of Electrical and Electronics Engineers (Ed.), Proceedings of the gateway computing environments workshop (GCE) (pp.1-8). New Orleans, LA: IEEE Xplore

Y.F. Molina-Henao, A.L. Guerrero- Chacòn, M.A. Jaramillo Ecological and geographic dimensions of diversification in Piper subgenus Ottonia: A Lineage of Neo tropoical rain forest shrubs Syst Botany., 41 (2016), pp. 253-262

R.J. Morley Origin and evolution of tropical rain forests John Wiley & Sons (2000)

P.K. Mukherjee Nomenclatural notes on Piper Linn. (Piperaceae) from India II Phytotaxa., 338 (2018), pp. 17-32

J. Murienne Testing biodiversity hypothesis in New Caledonia using phylogenetics J. Biogeogr., 36 (2009), pp. 1433-1434

Y. Najman, E. Appel, M. Boudagher Fadel, P. Bown, A. Carter, E. Garzanti, R. Parrish Timing of India Asia collision: Geological, biostratigraphic, and palaeomagnetic constraints Journal of Geophysical Research: Solid Earth., 115 (B12) (2010)

L. Nauheimer, P.C. Boyce, S.S. Renner Giant taro and its relatives: a phylogeny of the large genus Alocasia (Araceae) sheds light on Miocene floristic exchange in the Malesian region
Mol Phylogenet Evol., 63 (2012), pp. 43-51

J. Naumann, K. Salomo, J.P. Der, E.K. Wafula, J.F. Bolin, E. Maass, S.Wanke Single-copy nuclear genes place haustorial Hydnoraceae within Piperales and reveal a Cretaceous origin of multiple parasitic angiosperm lineages PLoS One, 8 (11) (2013), p. e79204

E. Paradis, J. Claude, K. Strimmer APE: analyses of phylogenetics and evolution in R language Bioinformatics., 20 (2004), pp. 289-290

O.A. Pérez-Escobar, M. Gottschiling, G. Chomicki, F.L. Condamine, B.B. Klitgård, E. Pansarin, G. Gerlach Andean mountain building did not preclude dispersal of lowland epiphytic orchids in the Neotropics Sci Rep., 7 (2017), p. 4919

M. Popp, A. Gizaw, S. Nemomissa, J. Suda, C. Brochmann Colonization and diversification in the African ‘sky islands’ by Eurasian Lychnis L. (Caryophyllaceae) J. Biogeogr., 35 (2008), pp. 1016-1029

V. Prasad, A. Farooqui, S.K.M. Tripathi, R. Garg, B. Thakur Evidence of Late Palaeocene-Early Eocene equatorial rain forest refugia in southern Western Ghats India. J. Biosci., 34 (2009), pp. 777-797

R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. Available at http://www.R-project.org/ last accessed March 2017.
Google Scholar
Rambaut, 2016
Rambaut, A. 2016. Figtree, a graphical viewer of phylogenetic trees. Retrieved from http://tree.bio.ed.ac.uk/software/figtree (accessed 20 December 2017)

Rambaut, A., Drummond, A.J., 2010. LogCombiner version 1.6.1 [computer program] http://beast.bio.ed.ac.uk.

Rambaut, A., Drummond A.J., Xie, D., Baele, G., & Suchard, M.A., 2018. Tracer v1.7, Available from http://tree.bio.ed.ac.uk/software/trace

Ravindran, P. N. (Ed.)., 2003. Black pepper: Piper nigrum. CRC Press.

R.H. Ree, I. Sanmartín Conceptual and statistical problems with the DEC+ J model of founder-event speciation and its comparison with DEC via model selection J. Biogeogr., 45 (2018), pp. 741-749

R.H. Ree, S.A. Smith Lagrange: software for likelihood analysis of geographic range evolution Syst Biol., 57 (2008), pp. 4-14

L.H. Rieseberg, D.E. Soltis Phylogenetic consequences of cytoplasmic gene flow in plants Evol. Trends Plants., 5 (1991), pp. 65-84

C.M. Roersch Piper umbellatum L.: a comparative cross-cultural analysis of its medicinal uses and an ethnopharmacological evaluation J Ethnopharmacol., 131 (2010), pp. 522-537

F. Ronquist Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography Syst Biol., 46 (1997), pp. 195-203

F. Ronquist, M. Teslenko, P. Van Der Mark, D.L. Ayres, A. Darling, S.Höhna, J.P. Huelsenbeck MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space Syst Biol., 61 (2012), pp. 539-542

F. Rutschmann, T. Eriksson, J. Schönenberger, E. Conti Did Crypteroniaceae really disperse out of India? molecular dating evidence from rbc L, ndh F, and rpl 16 intron sequences
Int J Plant Sci., 165 (2004), pp. S69-S83

K. Salomo, J.F. Smith, T.S. Feild, M.S. Samain, L. Bond, C. Davidson, S.Wanke The emergence of earliest angiosperms may be earlier than fossil evidence indicates Syst. Bot., 42 (2017), pp. 607-619

J.R. Sambrook, D. Russell Molecular cloning: a laboratory manual
Q Rev Biol., 76 (2001), pp. 348-349

B. Samanth, D.M. Mohabey Playnoflora from Deccan volcano-sedimentary sequence (Cretaceous-Palaeogene transition) of central India: Implications for spatio-temporal correlation J. Biosci., 34 (2009), pp. 811-823

M.J. Sanderson Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach Mol Biol Evol., 19 (2002), pp. 101-109

S. Sen, A. Gode, S. Ramanujam, G. Ravikanth, N.A. Aravind Modeling the impact of climate change on wild Piper nigrum (Black Pepper) in Western Ghats, India using ecological niche models
J. Plant Res., 129 (2016), pp. 1033-1040

J.F. Smith, A.C. Stevens, E.J. Tepe, S. Davidson Placing the origin of two species- rich genera in the late Cretaceous with later species divergence in the tertiary: a phylogenetic, biogeographic and molecular dating analysis of Piper and Peperomia (Piperaceae)
Plant Syst Evol., 275 (2008), p. 9

A. Stamatakis RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
Bioinformatics., 22 (2006), pp. 2688-2690

A. Stamatakis, P. Hoover, J. Rougemont A rapid bootstrap algorithm for the RAxML web servers Syst Biol., 57 (2008), pp. 758-771

S. Surveswaran, M.Y. Kamble, S.R. Yadav, M. Sun Molecular phylogeny of Ceropegia (Asclepiadoideae, Apocynaceae) of Indian Western Ghats Plant Syst Evol., 281 (2009), pp. 51-63

C.U. Ulloa, P. Acevedo-Rodríguez, S. Beck, M.J. Belgrano, R. Bernal, P.E.Berry, P.M. Jørgensen An integrated assessment of the vascular plant species of the Americas
Science., 358 (2017), pp. 1614-1617

I. Van Bocxlaer, S.D. Biju, S.P. Loader, F. Bossuyt Toad radiation reveals into-India dispersal as a source of endemism in the Western Ghats-Sri Lanka biodiversity hotspot BMC Evol Biol., 9 (2009), p. 131

S. Wanke, M.A. Jaramillo, T. Borsch, M.S. Samain, D. Quandt, C. Neinhuis Evolution of Piperales -matK gene and trnK intron sequence data reveal lineage specific resolution contrast Mol Phylogenet Evol., 42 (2007), pp. 477-497

T.C. Whitmore An introduction to tropical rain forests
(2nd edn.), Oxford University Press, Oxford (1998)
Yu et al., 2014
X.Q. Yu, M. Maki, B.T. Drew, A.J. Paton, H.W. Li, J.L. Zhao, J. Li Phylogeny and historical biogeography of Isodon (Lamiaceae): Rapid radiation in south-west China and Miocene overland dispersal into Africa
Mol Phylogenet Evol., 77 (2014), pp. 183-194

Y.M. Yuan, S. Wohlhauser, M. Möller, J. Klackenberg, M.W. Callmander, P.Küpfer Phylogeny and biogeography of Exacum (Gentianaceae): a disjunctive distribution in the Indian Ocean Basin resulted from long distance dispersal and extensive radiation Syst Biol., 54 (2005), pp. 21-34

L. Zhou, Y.C. Su, D.C. Thomas, R.M.K. Saunders ‘Out of Africa’ dispersal of tropical floras during the Miocene climatic optimum: evidence from Uvaria (Annonaceae) J. Biogeogr., 39 (2012), pp. 322-335
All items in Spectrum are protected by copyright, with all rights reserved. The use of items is governed by Spectrum's terms of access.

Repository Staff Only: item control page

Downloads per month over past year

Research related to the current document (at the CORE website)
- Research related to the current document (at the CORE website)
Back to top Back to top