Sindora × changiensis L.M.Choo, Loo, W.F.Ang & K.Er is a new hybrid from the subfamily Detarioideae in Fabaceae. This is the first reported instance of natural hybridisation in Sindora. Based on population genetics analyses using ddRAD and morphological observations, this taxon represents a fertile hybrid between Sindora coriacea and Sindora echinocalyx. This new hybrid is so far only known to occur naturally from Changi at the north-eastern coast of Singapore. It has pods that are sparsely spiny. This is intermediate between the smooth, non-spiny pods of S. coriacea, and the densely spiny pods of S. echinocalyx. The calyx is smooth and unarmed, resembling S. coriacea. Last but not least, the ovary is entirely pubescent, different from S. coriacea and S. echinocalyx. The ovary of S. coriacea has a glabrous patch in the middle, while that of S. echinocalyx has minute spines protruding from the dense pubescence. A taxonomic description and an updated key to the Sindora of Singapore and Peninsular Malaysia are also provided.

Caesalpinioideae, Changi, ddRAD, new hybrid, Sindora coriacea, Sindora echinocalyx

Sindora Miq. is a genus of the legume family (Fabaceae: Detarioideae) and consists of 20–22 species. It has a paleotropical distribution, with one species from West Central Africa, and the rest from Asia, which are distributed from Southern China to Southeast Asia, and to as far west as the Philippines (de Wit 1949; Chen et al. 2010; Choo and Ngo 2020). The genus can be easily recognised in the field by its characteristic pods, often with spines originating from modified glands, and dark-coloured seeds with a large yellow or reddish-brown aril of about the same size as the seed itself (de Wit 1949; Sosef 1993).

Previous work on Sindora in Singapore and Peninsular Malaysia reported five native species to the region, i.e. Sindora coriacea (Baker) Prain, Sindora echinocalyx Prain, Sindora siamensis Teijsm. ex Miq., Sindora velutina Baker, Sindora wallichii Benth. (Choo and Ngo 2020). Of these, four species, Sindora coriacea, S. echinocalyx, S. velutina and S. wallichii are present in both Singapore and Peninsular Malaysia, while S. siamensis is found only in northern Peninsular Malaysia, Thailand, Cambodia, Laos and Vietnam, and is only present as a cultivated tree in Singapore. In Singapore, the four native species can be found in the remaining patches of primary and mature secondary rainforest. S. coriacea and S. wallichii are relatively more abundant than S. velutina and S. echinocalyx, which are comparatively rarer in the wild in Singapore. S. velutina is found only in the primary rainforest at Bukit Timah Nature Reserve, while S. echinocalyx may be more associated with hillsides and coastal areas (Choo and Ngo 2020). Recent field observations of mature Sindora trees in Singapore revealed a particular 27 m-tall mature tree from Changi at the north-eastern coast of the island, which could not be satisfactorily identified to species using the taxonomic key in Choo and Ngo (2020).

From a combination of population genetics and morphological evidence, we found that this particular tree represents a natural hybrid between Sindora coriacea and Sindora echinocalyx, and is the first recorded instance of hybridisation in Sindora. We describe this new hybrid as Sindora × changiensis L.M.Choo, Loo, W.F.Ang & K.Er, and further explain the characteristics that distinguish this new hybrid from its parent species.

Sindora × changiensis is the first recorded instance of natural hybridisation in the genus Sindora, and is currently known to be endemic to Singapore. Both of the parent species, S. coriacea and S. echinocalyx, are native to Singapore. S. echinocalyx is known to occur in coastal hills and heath forests in Peninsular Malaysia (Saw 2010) and had been recorded in Changi in the past based on an herbarium specimen (Bakar s.n., Year 1893, Changi, SING[SING0044593]). In addition, S. coriacea is a native of lowland rainforests in Singapore (Chong et al. 2009; Choo and Ngo 2020). Located at the north-eastern coast of Singapore, Changi was known to be dominated by lowland rainforest and was previously designated as a forest reserve in 1884, before it was largely cleared by the British to make way for military barracks and an airbase from 1927 to 1941 (Probert 1965; Corlett 1992). However, there are presently still a few large trees of lowland rainforest species in Changi, which are remnants of the original rainforest vegetation, such as Shorea gibbosa, Dipterocarpus sublamellatus and Gluta malayana. Based on early aerial photographs of the site in 1946 and 1950, it showed that the mature Sindora × changiensis tree was part of a remnant rainforest patch that was retained as part of the grounds of the existing bungalow (503 Cranwell Road) that served as the residence of senior British military officers based at Changi (National Archives of Singapore records) (Fig. 6). Carbon dating also estimated that the tree is at least approximately 226 to 364 years old, further suggesting that the tree was naturally occurring in-situ and could not have been planted (National Parks Board, unpublished data).

Figure 6. 

Aerial photo of the Changi area from various years showing Sindora × changiensis circled in yellow A aerial photo on 17 Feb 1946, which is the earliest archival aerial photo of the Changi area, showing the tree as part of the rainforest remnant B aerial photo on 14 Jul 1950, showing the erection of the Cranwell bungalows to the left and right of the tree C aerial photo on 5 Mar 1963 D present day aerial photo showing the tree. (Images: A–C aerial photographs by the British Royal Air Force between 1940 to 1970s, from a collection held by the National Archives of Singapore. Crown copyright, reproduced in part D imagery 2021 Maxar Technologies, Map data 2021 Google).

This hybrid individual was observed to have been pollinated by the giant honey bee (Apis dorsata). These bees are known to be able to transfer pollen over sizeable distances, and have also been inferred to facilitate pollen dispersal of another leguminous tree species, Koompassia malaccensis, between rainforest patches across a distance of more than 2.5 km within the urban landscape of Singapore (Noreen and Webb 2013; Noreen et al. 2016). Given that these bees are likely to be pollinators of other Sindora species, it is therefore possible that this hybrid could have come about by the transfer of pollen between S. coriacea and S. echinocalyx trees at Changi in the past.

In both the Neighbour-Net (Fig. 1) and STRUCTURE analyses (Fig. 2), the proportion of S. coriacea in the genetic composition of the mature hybrid tree (Sind019) is higher than that of S. echinocalyx. This might suggest that S. coriacea is the maternal parent, which contributes both plastid and nuclear genetic material to the hybrid (Greiner et al. 2015). Another possibility is that the hybrid tree or its seedlings (Sind006, Sind 017) could be backcrossed to S. coriacea, which could explain the larger genetic contribution of S. coriacea to the hybrid. However, further studies including the sequencing of the chloroplast genome and the sampling of more hybrid offspring will be necessary to ascertain this.

This hybrid is fertile, with extensive flowering and fruit set happening once a year (Fig. 3), based on field observations from August 2020 to September 2021. The hybrid characters are also stable, as an offspring of the hybrid tree which was planted in 2001 has also been observed to produce fruits with a similarly sparse distribution of spines (Choo SING2021-677, 17 Sep 2021, outside Changi Chapel & Museum, SING). While this is unusual as hybrids often have lower fitness and are usually sterile (Ashton 1969; Hopkins 2013; reviewed in Schley et al. 2020), natural Shorea hybrids in the rainforest of Singapore have been documented to be fecund (Kamiya et al. 2011). The growth rates and survivability of S. curtisii × S. leprosula seedlings were also found to be comparable to the parent species, albeit with slightly slower growth rate than S. leprosula, suggesting similar fitness to that of parent species in the rainforest environment (Kenzo et al. 2016, 2019). There have also been suggestions that environmental disturbance could potentially result in less favourable conditions for parental species and give rise to conditions that favour natural hybrids, with implications for conservation (Levin et al. 1996; Rieseberg and Carney 1998). This could have enabled Sindora × changiensis to establish and persist over time, even as its habitat changed drastically from a primary rainforest to an urban environment. More research could be done to further examine the mechanisms giving rise to this fertile hybrid, including the possibility of backcrossing with its parent species, as well as the effects of this on the evolutionary trajectory and the genetic diversity of Sindora in rainforest patches within anthropogenic landscapes.

The authors would like to thank the Singapore Land Authority for granting access to the site at 503 Cranwell Road, and Abigail Leong, Arthur Ng, Jonathan Lam, Koh Yong Kwang from the Streetscape Division, Yeo Chow Khoon from the Singapore Botanic Gardens of National Parks Board, Singapore (NParks) and Desmond Aw (TKB C-E Contractor Pte Ltd) for logistical support in sample collections in Changi. We would also like to thank Yap Ee Hean and Zestin Soh (NParks) for collecting and identifying the bees on the Cranwell Road tree. We are also grateful to Dr Matti Niissalo (NParks) and Dr Ngo Kang Min (Nanyang Technological University) for field work support for specimens collected from the Central Catchment Nature Reserve and Bukit Timah Nature Reserve. Dr Matti Niissalo and Dr Rowan Schley (University of Exeter) also provided advice on the molecular analyses. We would also like to thank Khoo-Woon Mui Hwang and Dr Gillian Khew (Singapore Botanic Gardens, NParks) for providing technical support and resources in the molecular lab. The authors are also grateful to the National Archives of Singapore for facilitating their research of the Changi area and for providing the aerial photographs for this paper. Dr Patrick Herendeen and Dr Jeremie Fant are also thanked for their constructive comments and suggestions which improved this manuscript.