Close

A phylogenomic analysis of Nepenthes (Nepenthaceae)

Bruce Murphy, Félix Forest, Timothy Barraclough, James Rosindell, Sidonie Bellot, Robyn Cowan, Michal Golos, Matthew Jebb, Martin Cheek

Preprint posted on 24 June 2019 https://www.biorxiv.org/content/10.1101/680488v1

Article now published in Molecular Phylogenetics and Evolution at http://dx.doi.org/10.1016/j.ympev.2019.106668

Untangling the Asian pitcher plants’ complex tree of life using large-scale phylogenomic analysis

Selected by Edi Sudianto

Background

Nepenthes (common name: Asian pitcher plant) is a genus of carnivorous plants that has modified its leaves to form a pitcher-like structure (Fig. 1). The pitcher is attached to the leaf blade by a tendril. The structure is usually filled with fluids that may attract, capture, and digest their animal prey (1). Some Nepenthes species have been known to acquire their nutrients from other sources, such as leaf litter (2) and animal feces from tree shrews (3), rats (4), and bats (5). Their pitcher is also known to host several symbiotic species, such as mosquito larvae (6).

Figure 1. Examples of Nepenthes species found in Sabah, Malaysia. Adapted from (7).

 

It is estimated that there are 160–180 extant Nepenthes species in the world (8), mostly found in the rainforests of Southeast Asia. Yet, their phylogenetic relationships and species delimitation are poorly understood. Previous studies have been usually limited in the number of samples and loci. In this preprint, the authors used high throughput sequencing to capture 353 nuclear loci of 151 described or putative Nepenthes species and build the most comprehensive Nepenthes phylogeny to date using multiple matrices.

 

Key findings

The relationships of five Western outlying Nepenthes species are resolved

Based on their phylogenomic trees, the authors consistently found the Western outlying species as the earliest diverging clades in the Nepenthes phylogeny. In particular, they found N. pervillei (from Seychelles) as the sole sister of all other Nepenthes (Fig. 2). Two species from Madagascar, N. masaolensis and N. madagascarensis, were resolved as the sister to the clade containing Asian Nepenthes. Asian Nepenthes can be further distinguished into South and Southeast Asian clades. N. danseri from Waigeo Island in West Papua is indicated as the sister to remaining Southeast Asian species. The phylogenetic trees produced in this study confirmed the order of these five Western outlying species and N. danseri, which were controversial in previous studies. This result also supports the out-of-Africa hypothesis, which posits that Nepenthes is of African origin and it reached Asia when the Indian plate broke off from Madagascar in the late Cretaceous period (9).

Figure 2. Cladogram summarizing the phylogenetic relationships among two major Nepenthes clades and six other Nepenthes species (N. danseri, N. khasiana, N. distillatoria, N. masaolensis, N. madagascarensis, and N. pervillei). Sey. Is., Seychelles Island; Mad. Is., Madagascar Island; S. Asia, South Asia; S.E. Asia, South East Asia.

 

Southeast Asian Nepenthes diversified into two major clades

Southeast Asia, as the center of Nepenthes diversity, holds ca. 95% of all known Nepenthes species (7). Other than the six above-mentioned species, the Southeast Asian Nepenthes were always recovered as two sister clades in this study (Fig. 2). Common and lowland species are retained as Clade 1, along with several high altitudinal species from Sulawesi and Papua. Meanwhile, Clade 2 contains some of the most geographically defined clades from Sumatra-Java, Indochina, Peninsular Malaysia, Mindanao, and Palawan. Bornean, Sulawesian, and Papuan species were not as clearly distinguished as other regions; they were found both within Clade 1 and Clade 2. Together, these results indicate that most Nepenthes species have been resolved into well-supported clades and the phylogeny presented here could serve as a guide to understanding the evolution of Nepenthes lineages, especially for geographically-delimited clades.

 

Non-monophyly of several Nepenthes species

In this study, the authors also included multiple samples of widespread species in the analyses to account for different populations. It turns out that several species, including N. maxima, N. tentaculata, N. hamata, N. rafflesiana, and N. mirabilis, were recovered as paraphyletic – suggesting that some accessions in these taxa may be a misnomer. The recognition of non-monophyletic species as one species may also indicate cryptic species, i.e. morphologically identical but actually distinct species, in Nepenthes. However, we should also consider the possibility of systematic errors, such as the lack of strong support in individual gene trees and phylogenetic noises, as the cause for non-monophyly of these taxa.

 

Why I like this preprint

This preprint provides the first large-scale analysis for almost all of the known Nepenthes species using a huge number of loci, resulting in a high-resolution Nepenthes phylogeny. The authors not only resolved some controversial placements across the Nepenthes tree of life, but also clearly identified geographically-delimited clades from Sumatra-Java, Indochina, Peninsular Malaysia, Mindanao, and Palawan. Identification of paraphyletic Nepenthes species in this study also shows potential unknown cryptic taxa that warrant further study. These findings would form the basis for a better understanding of evolutionary processes and taxonomic classification in Nepenthes. Additionally, this preprint also demonstrated the applicability of a recently developed Angiosperms-353 probe kit in species-level systematics.

 

Future directions and questions

  • With the availability of high-resolution phylogeny for such a large number of Nepenthes taxa, would it be possible to include estimation of divergence time in the analysis? Estimation of divergence time would allow us to deduce the timings of Nepenthes diversification and dispersal, especially in Southeast Asia.
  • Are there any geological history events that may further support the biogeographical distribution and diversification of Nepenthes in Southeast Asia?

 

References

  1. Thorogood CJ, Bauer U, Hiscock SJ. (2018). Convergent and divergent evolution in carnivorous pitcher plant traps. New Phytol. 217(3): 1035–1041.
  2. Moran JA, Clarke CM, Hawkins BJ. (2003). From carnivore to detrivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria. Int J Plant Sci. 164(4): 635–639.
  3. Clarke CM, Bauer U, Lee CC, Tuen AA, Rembold K, Moran JA. (2009). Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biol Lett. 5(5): 632–635.
  4. Greenwood M, Clarke C, Lee CC, Gunsalam A, Clarke RH. (2011). A unique resource mutualism between the giant Bornean pitcher plant, Nepenthes rajah, and members of a small mammal community. PLOS ONE 6(6): e21114.
  5. Schöner MG, Schöner CR, Ermisch R, Puechmaille SJ, Grafe TU, Tan MC, Kerth G. (2017). Stabilization of a bat-pitcher plant mutualism. Sci Rep. 7: 13170.
  6. Tsukamoto M. (1989). Two new mosquito species from a pitcher plant of Mt. Kinabalu, Sabah, Malaysia: Culex rajah and Toxorhynchites rajah (Diptera: Culicidae). Japan J Trop Med Hyg. 17(3): 215–228.
  7. van der Ent A, Sumail S, Clarke C. (2015). Habitat differentiation of obligate ultramafic Nepenthes endemic to Mount Kinabalu and Mount Tambuyukon (Sabah, Malaysia). Plant Ecol. 216(6): 789–807.
  8. Clarke CM, Schlauer J, Robinson AS. (2018). Species of carnivorous plants. In: Ellison A, Adamec L (Eds.), Carnivorous plants: Physiology, Ecology, and Evolution. Oxford University Press, Oxford, pp. 411–413.
  9. Biswal DK, Debnath M, Konhar R, Yanthan S, Tandon P. (2018). Phylogeny and biogeography of carnivorous plant family Nepenthaceae with reference to the Indian pitcher plat Nepenthes khasiana reveals an Indian subcontinent origin of Nepenthes colonization in South East Asia during Miocene Epoch. Front Ecol Evol. 6: 108.

Tags: carnivorous plants, diversity, nepenthes, phylogeny, pitcher plants, plant

Posted on: 27 July 2019

doi: https://doi.org/10.1242/prelights.12481

Read preprint (No Ratings Yet)

Have your say

Your email address will not be published. Required fields are marked *

This site uses Akismet to reduce spam. Learn how your comment data is processed.

Sign up to customise the site to your preferences and to receive alerts

Register here

preLists in the evolutionary biology category:

‘In preprints’ from Development 2022-2023

A list of the preprints featured in Development's 'In preprints' articles between 2022-2023

 



List by Alex Eve, Katherine Brown

preLights peer support – preprints of interest

This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.

 



List by preLights peer support

EMBO | EMBL Symposium: The organism and its environment

This preList contains preprints discussed during the 'EMBO | EMBL Symposium: The organism and its environment', organised at EMBL Heidelberg, Germany (May 2023).

 



List by Girish Kale

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)

A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.

 



List by Alex Eve

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.

 



List by Ana Dorrego-Rivas

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

ECFG15 – Fungal biology

Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome

 



List by Hiral Shah

COVID-19 / SARS-CoV-2 preprints

List of important preprints dealing with the ongoing coronavirus outbreak. See http://covidpreprints.com for additional resources and timeline, and https://connect.biorxiv.org/relate/content/181 for full list of bioRxiv and medRxiv preprints on this topic

 



List by Dey Lab, Zhang-He Goh

1

SDB 78th Annual Meeting 2019

A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.

 



List by Alex Eve

Pattern formation during development

The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.

 



List by Alexa Sadier

Also in the genomics category:

preLights peer support – preprints of interest

This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.

 



List by preLights peer support

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

Semmelweis Symposium 2022: 40th anniversary of international medical education at Semmelweis University

This preList contains preprints discussed during the 'Semmelweis Symposium 2022' (7-9 November), organised around the 40th anniversary of international medical education at Semmelweis University covering a wide range of topics.

 



List by Nándor Lipták

20th “Genetics Workshops in Hungary”, Szeged (25th, September)

In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf

 



List by Nándor Lipták

EMBL Conference: From functional genomics to systems biology

Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020

 



List by Jesus Victorino

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

Zebrafish immunology

A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.

 



List by Shikha Nayar
Close