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

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

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

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.Peer reviewedPublisher PD

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

The relative importance of the mechanisms underlying species radiation remains unclear. Here, the authors combine reference genome assembly and population genetics analyses to show that neutral forces have contributed to the radiation of the most species-rich tree genus Syzygium. 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.Peer reviewe

Hanguana deflexa (Hanguanaceae), a new forest species from Sarawak, Borneo

Hanguana deflexa sp. nov. (Hanguanaceae) from Lawas district, Sarawak, Malaysia (northern Borneo) is described and illustrated, bringing the total number of species in Borneo to eight. The new species differs from all other recognized Hanguana species by a combination of flat leaf blade, deflexed infructescences, one-seeded dull red fruits with centrally positioned stigma and globose seed with wedge-shaped ostiole. Revised key for Bornean Hanguana species is presented

Data from: Persistence of long-distance, insect-mediated pollen movement for a tropical canopy tree species in remnant forest patches in an urban landscape

As deforestation and urbanization continue at rapid rates in tropical regions, urban forest patches are essential repositories of biodiversity. However, almost nothing is known about gene flow of forest-dependent tree species in urban landscapes. In this study, we investigated gene flow in the insect-pollinated, wind-dispersed tropical tree Koompassia malaccensis in and among three remnant forest patches in the urbanized landscape of Singapore. We genotyped the vast majority of adults (N=179) and a large number of recruits (N=2103) with 8 highly polymorphic microsatellite markers. Spatial genetic structure of the recruit and adult cohorts was significant, showing routine gene dispersal distances of ~100–400 m. Parentage analysis showed that 97% of recruits were within 100 m of their mother tree, and a high frequency of relatively short-distance pollen dispersal (median ~143–187 m). Despite routine seed and pollen dispersal distances of within a few hundred meters, interpatch gene flow occurred between all patches and was dominated by pollen movement: parentage analysis showed 76 pollen versus 2 seed interpatch dispersal events, and the seedling neighborhood model estimated ~1–6% seed immigration and ~21–46% pollen immigration rates, depending on patch. In addition, the smallest patch (containing five adult K. malaccensis trees) was entirely surrounded by >2.5 km of ‘impervious’ substrate, yet had the highest proportional pollen and seed immigration estimates of any patch. Hence, contrary to our hypothesis, insect-mediated gene flow persisted across an urban landscape, and several of our results also parallel key findings from insect-pollinated canopy trees sampled in mixed agricultural–forest landscapes

Hanguana Thailandica (Hanguanaceae): A new peat swamp forest species from Thailand

A new species of Hanguana (Hanguanaceae), H. thailandica, is described and illustrated from Trang province, Peninsular Thailand. This is the second Hanguana species recorded in Thailand, along with the widespread helophytic H. malayana. The species is morphologically similar to Hanguana exultans and H. nitens found in swamp forests habitats in southern Peninsular Malaysia and Singapore. The conservation status of this species is accessed as Endangered according to the IUCN Red List Category and Criteria

Whence came these plants most foul? Phylogenomics and biogeography of Lowiaceae (Zingiberales)

Lowiaceae (order Zingiberales) is a small family of forest herbs in Southeast Asia. All species belong to the genus Orchidantha. They are known for possessing orchid-like flowers that are smelly, apparently mimicking dead animals, feces, or mushrooms. Little is known of the biogeographic patterns or character evolution of the family. We sampled the family extensively, including many recently discovered species, and reconstructed the phylogeny of the family using HybSeq with Lowiaceae-specific RNA baits. Our phylogenetic reconstructions confirm that the family is most closely related to Strelitziaceae, and that species with dark, foul-smelling flowers form a grade in which a clade of species with paler flowers are embedded. The pale-flowered species produce a distinct odor, resembling edible mushrooms. Apart from a single species, the species from Borneo form a clade, and the same is true for Indochinese species. The remaining species form a more widespread clade. A biogeographic analysis shows that the distribution of Lowiaceae can explained by vicariance and gradual dispersal from a shared ancestral range of Borneo and Indochina. There is no evidence of long-distance dispersal, only a later extension in distribution to Peninsular Malaysia which coincides with the presence of a land bridge. Different directions of spread are possible, but none require long-distance dispersal. The results are consistent with the geological history of Southeast Asia. In particular, the relatively early isolation between Indochina and Borneo could be explained by the presence of a sea barrier that developed 10–15 MYA, and the continuous movement of plant species between Borneo and Peninsular Malaysia could be explained by a land bridge that existed until c. 5 MYA. The lack of an extensive land bridge with a suitable habitat may explain the absence of this genus from Sumatra and other Indonesian islands aside from Borneo. The strict reliance on a continuous habitat for the range expansion of Lowiaceae can be explained by their fruits and seeds, which lack obvious adaptations for long-distance dispersal. The inability to disperse to new areas may also explain why the extant species have very restricted distributions.National Parks BoardPublished versionGK, MN, and JL-Š were supported by the National Parks Board. OŠ was financially supported by the Ministry of Culture of the Czech Republic (nos. 00023272, DKRVO 4.II.c). EG was supported by the United States National Science Foundation (DBI award no. 1711391)

microsatellite markers, Koompassia malaccensis in Singapore

Microsatellite data (8 loci) for 179 adults and 2,013 recruits of the canopy tree Koompassia malaccensis from three primary forest patches within Singapore