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 Gray; Charlie 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

doi:10.1038/s41467-022-32637-x

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

Biological Sciences

Research output: Contribution to journal › Article › peer-review

1 Citation (Scopus)

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 language	English
Article number	5031
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-32637-x
Publication status	Published - 12 Sep 2022

Keywords

Genetic Speciation
Genomics
Phylogeny
Syzygium/genetics
Trees

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Low, Y. W., Rajaraman, S., Tomlin, C. M., Ahmad, J. A., Ardi, W. H., Armstrong, K., Athen, P., Berhaman, A., Bone, R. E., Cheek, M., Cho, N. R. W., Choo, L. M., Cowie, I. D., Crayn, D., Fleck, S. J., Ford, A. J., Forster, P. I., Girmansyah, D., Goyder, D. J., ... Albert, V. A. (2022). Genomic insights into rapid speciation within the world's largest tree genus Syzygium. Nature Communications, 13(1), [5031]. https://doi.org/10.1038/s41467-022-32637-x

Low, YW, Rajaraman, S, Tomlin, CM, Ahmad, JA, Ardi, WH, Armstrong, K, Athen, P, Berhaman, A, Bone, RE, Cheek, M, Cho, NRW, Choo, LM, Cowie, ID, Crayn, D, Fleck, SJ, Ford, AJ, Forster, PI, Girmansyah, D, Goyder, DJ, Gray, B, Heatubun, CD, Ibrahim, A, Ibrahim, B, Jayasinghe, HD, Kalat, MA, Kathriarachchi, HS, Kintamani, E, Koh, SL, Lai, JTK, Lee, SML, Leong, PKF, Lim, WH, Lum, SKY, Mahyuni, R, McDonald, WJF, Metali, F, Mustaqim, WA, Naiki, A, Ngo, KM, Niissalo, M, Ranasinghe, S, Repin, R, Rustiami, H, Simbiak, VI, Sukri, RS, Sunarti, S, Trethowan, LA, Trias-Blasi, A, Vasconcelos, TNC, Wanma, JF, Widodo, P, Wijesundara, DSA, Worboys, S, Yap, JW, Yong, KT, Khew, GSW, Salojärvi, J, Michael, TP, Middleton, DJ, Burslem, DFRP, Lindqvist, C, Lucas, EJ & Albert, VA 2022, 'Genomic insights into rapid speciation within the world's largest tree genus Syzygium', Nature Communications, vol. 13, no. 1, 5031. https://doi.org/10.1038/s41467-022-32637-x

@article{6daa02fc6dbb499389504900ec9c78be,

title = "Genomic insights into rapid speciation within the world's largest tree genus Syzygium",

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.",

keywords = "Genetic Speciation, Genomics, Phylogeny, Syzygium/genetics, Trees",

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

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{\textquoteright} 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 Assembl{\'e}e de la Province Nord and Assembl{\'e}e 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{\textquoteright}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.",

year = "2022",

month = sep,

day = "12",

doi = "10.1038/s41467-022-32637-x",

language = "English",

volume = "13",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

number = "1",

}

TY - JOUR

T1 - Genomic insights into rapid speciation within the world's largest tree genus Syzygium

AU - Low, Yee Wen

AU - Rajaraman, Sitaram

AU - Tomlin, Crystal M

AU - Ahmad, Joffre Ali

AU - Ardi, Wisnu H

AU - Armstrong, Kate

AU - Athen, Parusuraman

AU - Berhaman, Ahmad

AU - Bone, Ruth E

AU - Cheek, Martin

AU - Cho, Nicholas R W

AU - Choo, Le Min

AU - Cowie, Ian D

AU - Crayn, Darren

AU - Fleck, Steven J

AU - Ford, Andrew J

AU - Forster, Paul I

AU - Girmansyah, Deden

AU - Goyder, David J

AU - Gray, Bruce

AU - Heatubun, Charlie D

AU - Ibrahim, Ali

AU - Ibrahim, Bazilah

AU - Jayasinghe, Himesh D

AU - Kalat, Muhammad Ariffin

AU - Kathriarachchi, Hashendra S

AU - Kintamani, Endang

AU - Koh, Sin Lan

AU - Lai, Joseph T K

AU - Lee, Serena M L

AU - Leong, Paul K F

AU - Lim, Wei Hao

AU - Lum, Shawn K Y

AU - Mahyuni, Ridha

AU - McDonald, William J F

AU - Metali, Faizah

AU - Mustaqim, Wendy A

AU - Naiki, Akiyo

AU - Ngo, Kang Min

AU - Niissalo, Matti

AU - Ranasinghe, Subhani

AU - Repin, Rimi

AU - Rustiami, Himmah

AU - Simbiak, Victor I

AU - Sukri, Rahayu S

AU - Sunarti, Siti

AU - Trethowan, Liam A

AU - Trias-Blasi, Anna

AU - Vasconcelos, Thais N C

AU - Wanma, Jimmy F

AU - Widodo, Pudji

AU - Wijesundara, Douglas Siril A

AU - Worboys, Stuart

AU - Yap, Jing Wei

AU - Yong, Kien Thai

AU - Khew, Gillian S W

AU - Salojärvi, Jarkko

AU - Michael, Todd P

AU - Middleton, David J

AU - Burslem, David F R P

AU - Lindqvist, Charlotte

AU - Lucas, Eve J

AU - Albert, Victor A

N1 - 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.

PY - 2022/9/12

Y1 - 2022/9/12

N2 - 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.

AB - 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.

KW - Genetic Speciation

KW - Genomics

KW - Phylogeny

KW - Syzygium/genetics

KW - Trees

U2 - 10.1038/s41467-022-32637-x

DO - 10.1038/s41467-022-32637-x

M3 - Article

C2 - 36097018

VL - 13

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 5031

ER -

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

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