Genomic insights into rapid speciation within the world's largest tree genus Syzygium

Yee Wen Low, Sitaram Rajaraman, Crystal M Tomlin, Joffre Ali Ahmad, Wisnu H Ardi, Kate Armstrong, Parusuraman Athen, Ahmad Berhaman, Ruth E Bone, Martin Cheek, Nicholas R W Cho, Le Min Choo, Ian D Cowie, Darren Crayn, Steven J Fleck, Andrew J Ford, Paul I Forster, Deden Girmansyah, David J Goyder, Bruce GrayCharlie D Heatubun, Ali Ibrahim, Bazilah Ibrahim, Himesh D Jayasinghe, Muhammad Ariffin Kalat, Hashendra S Kathriarachchi, Endang Kintamani, Sin Lan Koh, Joseph T K Lai, Serena M L Lee, Paul K F Leong, Wei Hao Lim, Shawn K Y Lum, Ridha Mahyuni, William J F McDonald, Faizah Metali, Wendy A Mustaqim, Akiyo Naiki, Kang Min Ngo, Matti Niissalo, Subhani Ranasinghe, Rimi Repin, Himmah Rustiami, Victor I Simbiak, Rahayu S Sukri, Siti Sunarti, Liam A Trethowan, Anna Trias-Blasi, Thais N C Vasconcelos, Jimmy F Wanma, Pudji Widodo, Douglas Siril A Wijesundara, Stuart Worboys, Jing Wei Yap, Kien Thai Yong, Gillian S W Khew, Jarkko Salojärvi, Todd P Michael, David J Middleton, David F R P Burslem, Charlotte Lindqvist, Eve J Lucas, Victor A Albert

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Abstract

Species radiations, despite immense phenotypic variation, can be difficult to resolve phylogenetically when genetic change poorly matches the rapidity of diversification. Genomic potential furnished by palaeopolyploidy, and relative roles for adaptation, random drift and hybridisation in the apportionment of genetic variation, remain poorly understood factors. Here, we study these aspects in a model radiation, Syzygium, the most species-rich tree genus worldwide. Genomes of 182 distinct species and 58 unidentified taxa are compared against a chromosome-level reference genome of the sea apple, Syzygium grande. We show that while Syzygium shares an ancient genome doubling event with other Myrtales, little evidence exists for recent polyploidy events. Phylogenomics confirms that Syzygium originated in Australia-New Guinea and diversified in multiple migrations, eastward to the Pacific and westward to India and Africa, in bursts of speciation visible as poorly resolved branches on phylogenies. Furthermore, some sublineages demonstrate genomic clines that recapitulate cladogenetic events, suggesting that stepwise geographic speciation, a neutral process, has been important in Syzygium diversification.

Original languageEnglish
Article number5031
JournalNature Communications
Volume13
Issue number1
DOIs
Publication statusPublished - 12 Sept 2022

Bibliographical note

Acknowledgements
Y.W.L. was supported by a postgraduate scholarship research grant from the Ministry of National Development, Singapore awarded through the National Parks Board, Singapore (NParks; NParks’ Garden City Fund). Principal research funding from NParks and the School of Biological Sciences (SBS), Nanyang Technological University (NTU), Singapore, is acknowledged. We thank Peter Preiser, Associate Vice President for Biomedical and Life Sciences, for facilitating NTU support, and Kenneth Er, CEO of NParks, for facilitating research funding through that organisation. V.A.A. and C.L. were funded by SBS, NTU for a one-year research leave. V.A.A. and C.L. also acknowledge support from the United States National Science Foundation (grants 2030871 and 1854550, respectively). S.R. was supported by a postdoctoral research fellowship under the NTU Strategic Plant Programme. S.R. and N.R.W.C. acknowledge funding from NTU start-up and the Academy of Finland (decisions 318288, 319947) grants to J.S. Fieldwork conducted by Y.W.L. was supported by an Indonesian Government RISTEK research permit (Application ID: 1517217008) and an Access License from the Sabah State government [JKM/MBS.1000-2/2JLD.7(84)]. T.N.C.V. is grateful to the Assemblée de la Province Nord and Assemblée de la Province Sud (New Caledonia) for facilitating relevant collection permits. A.N. was partly supported by the Research Project Promotion Grant (Strategic Research Grant No. 17SP01302) from the University of the Ryukyus, and partly by the Environment Research and Technology Development Fund (JPMEERF20204003) from the Environmental Restoration and Conservation Agency of Japan. Fieldwork in Fiji conducted by R.B. was hosted and facilitated by Elina Nabubuniyaka-Young (The Pacific Community’s Centre for Pacific Crops and Trees, Fiji). We thank the NTU-Smithsonian Partnership for tree data obtained for the Bukit Timah Nature Reserve (BTNR) long-term forest dynamics plots. Administrative support provided by Mui Hwang Khoo-Woon and Peter Ang at the molecular laboratory of the Singapore Botanic Gardens (SBG) is acknowledged. Rosie Woods and Imalka Kahandawala (DNA and Tissue Bank, Royal Botanic Gardens, Kew) facilitated additional DNA samples. Daniel Thomas (SBG) and Yan Yu (Sichuan University) commented on biogeographical analyses. NovogeneAIT in Singapore is acknowledged for personalised sequencing service.

Data Availability Statement

The genome data generated in this study has been deposited in the NCBI database under accession code PRJNA803434 and BioSample ID SAMN29207412. The Syzygium grande genome assembly and annotation are also available on CoGe [https://genomevolution.org/coge/GenomeInfo.pl?gid=60239]. Processed data generated in this study and used for main text figures are provided in source data files. Additional processed data are available at Dryad [https://doi.org/10.5061/dryad.h18931zpw]. Source data are provided with this paper.

Keywords

  • Genetic Speciation
  • Genomics
  • Phylogeny
  • Syzygium/genetics
  • Trees

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