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Research Article
Biogeography and evolution of Asian Gesneriaceae based on updated taxonomy
expand article infoKe Tan‡, Tao Lu‡, Ming-Xun Ren‡
‡ Hainan University, Haikou, China

Corresponding author: Ming-Xun Ren ( renmx@hainu.edu.cn )

Academic editor: Kang Ming
© 2020 Ke Tan, Tao Lu, Ming-Xun Ren.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Tan K, Lu T, Ren M-X (2020) Gesneriaceae in China and Vietnam: Perfection of taxonomy based on comprehensive morphological and molecular evidence. In: Shui Y-M, Chen W-H, Ren M-X, Wen F, Hong X, Qiu Z-J, Wei Y-G, Kang M (Eds) Taxonomy of Gesneriaceae in China and Vietnam. PhytoKeys 157: 7-26. https://doi.org/10.3897/phytokeys.157.34032
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Abstract

Based on an updated taxonomy of Gesneriaceae, the biogeography and evolution of the Asian Gesneriaceae are outlined and discussed. Most of the Asian Gesneriaceae belongs to Didymocarpoideae, except Titanotrichum was recently moved into Gesnerioideae. Most basal taxa of the Asian Gesneriaceae are found in the Indian subcontinent and Indo-China Peninsula, suggesting Didymocarpoideae might originate in these regions. Four species diversification centers were recognized, i.e. Sino-Vietnam regions, Malay Peninsula, North Borneo and Northwest Yunnan (Hengduan Mountains). The first three regions are dominated by limestone landscapes, while the Northwest Yunnan is well-known for its numerous deep gorges and high mountains. The places with at least 25% species are neoendemics (newly evolved and narrowly endemic) which were determined as evolutionary hotspots, including Hengduan Mountains, boundary areas of Yunnan-Guizhou-Guangxi in Southwest China, North Borneo, Pahang and Terengganu in Malay Peninsula, and mountainous areas in North Thailand, North Sulawesi Island. Finally, the underlying mechanisms for biogeographical patterns and species diversification of the Asian Gesneriaceae are discussed.

Keywords

Didymocarpoideae, endemic, species diversification, limestone landscape, monsoon, long-distance dispersal

Introduction

Gesneriaceae Rich. & Juss. ex. DC. is a middle-sized family, including about 150 genera and over 3400 species (Weber et al. 2013). Traditionally, the family was divided into two subfamilies, subfamily Cyrtandroideae Burnett (palaeotropical group, with superior ovary and two unequal cotyledons) and subfamily Gesnerioideae Burnett (neotropical group, with inferior ovary and two equal cotyledons) (Burtt 1998).

Based on recent molecular and morphological data, Weber et al. (2013) put forward a new classification system, consisting of three subfamilies: Sanangoideae Weber (monotypic genus, endemic to South America), Didymocarpoideae Arn. and Gesnerioideae Burnett. In this newest classification system, the monotype genus Titanotrichum Solereder in Asia (China and Japan) has been transferred to the subfamily Gesnerioideae, which was formerly treated as “New World Gesneriaceae” (Burtt 1998; Weber et al. 2013). However, Didymocarpoideae is still “Old World Gesneriaceae”, consisting of 67 genera and more than 2300 species (Möller et al. 2017, Xu et al. 2017).

Recently, many Asian Gesneriaceae taxa had experienced extensive revision for their systematic positions, such as Boea Commerson ex Lamarck (Puglisi and Middleton 2018), Microchirita (C.B.Clarke) Y.Z. Wang (Middleton 2018), Henckelia Spreng. (Middleton et al. 2013), Paraboea (C. B. Clarke) Ridley (Puglisi et al. 2016) and the enlarged genus Oreocharis Bentham (Möller et al. 2011, 2014; Chen et al. 2014). Furthermore, several genera were newly established, i.e. Billolivia D.J. Middleton (Middleton et al. 2014), Chayamaritia D.J. Middleton (Middleton et al. 2015), Middletonia D.J. Middleton (Puglisi et al. 2016; Puglisi and Middleton 2017), Rachunia D.J. Middleton (Middleton et al. 2018). Such significant revisions of so many genera call for an updated study about biogeography and evolution of the Asian Gesneriaceae.

In this paper, we collected the species locality data (coordinates) from GBIF (Global Biodiversity Information Facility, https://www.gbif.org/) for all the species of the Asian Gesneraiceae. The species diversity and systematic positions of all genera were determined according to the newest literatures (e.g. Möller et al. 2016a, b, 2017; Roalson and Roberts 2016; Puglisi and Middleton 2018). We used the software DIVA-GIS 7.5 to create a distribution map at 1° × 1° latitude/longitude grid resolution to reveal distribution patterns of species diversity and endemism. We also analyzed the distribution type of all the genera and identified evolutionary hotspots, i.e. the center of neoendemic species, which is determined when at least 25% of total species are locally endemic. Finally, we discussed the possible mechanisms, including both intrinsic and extrinsic factors, to explain the formation and maintenance of diversification and endemic centers of the Asian Gesneriaceae.

1 Distribution type

Based on Wu’s (1979, 1991) criterions and Li’s (1996) pioneer study on the geographical areal-types of the Asian Gesneriaceae, we identified the Asian Gesneriaceae as belonging to three areal types and 20 subtypes as below.

I. Pantropics

I1. Tropic Asia and tropic America disjuncted: Rhynchoglossum Blume.

I2. Tropic Asia to tropic Australia: Boea Comm. ex Lam., Cyrtandra J. R. Forster & G. Forster, Stauranthera Bentham, Rhynchotechum Blume.

I3. Tropic Asia to tropic Africa: Epithema Blume.

II. Tropical and subtropical Asia

II1. Widespread in tropical and subtropical Asia: Aeschynanthus Jack, Paraboea (C. B. Clarke) Ridley, Dorcoceras Bunge, Codonoboea Ridl., Didymostigma W. T. Wang, Henckelia Spreng., Didymocarpus Wallich.

II2. East India to Java: Boeica C. B. Clarke, Leptoboea Benth., Beccarinda Bentham, Microchirita, Middletonia D.J. Middleton.

II3. Indo-China Peninsula: Tetraphyllum C.B.Clarke, Deinostigma W.T.Wang & Z.Y.Li, Damrongia Kerr ex Craib, Kaisupeea B.L. Burtt, Tribounia D.J. Middleton ex M. Möller, Billolivia, Chayamaritia, Rachunia D.J. Middleton.

II4. North of Indo-China Peninsula: Pseudochirita W. T. Wang, Anna Pellegrin.

II5. Subtropic Asia (Southwest and South China): Primulina Hance, Whytockia W. W. Smith, Hemiboea C. B. Clarke, Glabrella M. Möller & W. H. Chen, Gyrocheilos W. T. Wang, Raphiocarpus Chun, Petrocodon Hance, Allostigma W. T. Wang, Allocheilos W. T. Wang, Gyrogyne W. T. Wang, Litostigma Y.G. Wei, Fang Wen & M. Möller.

II6. Malay Peninsula to Southwest China: Ornithoboea Parish ex C. B. Clarke.

II7. Hainan Island: Cathayanthe W. Y. Chun, Metapetrocosmea W. T. Wang.

II8. Sri Lanka and India: Championia Gardn., Jerdonia Wight.

II9. Malay Peninsula: Orchadocarpa Ridl., Emarhendia R. Kiew, A. Weber & B.L. Burtt, Senyumia R. Kiew, A. Weber & B.L. Burtt, Somrania D.J. Middleton, Spelaeanthus R. Kiew, A. Weber & B.L. Burtt.

II10. Malay Archipelago: Agalmyla Blume, Monophyllaea R. Br., Loxocarpus R. Br., Loxonia Jack, Didissandra C.B. Clarke, Liebigia, Ridleyandra A. Weber & B.L. Burtt.

II11. Borneo Island: Hexatheca C.B. Clarke.

III. North Temperate

III1. Widespread in East Asia: Oreocharis Bentham.

III2. Sino-Himalaya: Corallodiscus Batalin, Loxostigma C.B. Clarke.

III3. Sino-Japan: Conandron Sieb. & Zucc., Titanotrichum Solereder.

III4. Hengduan Mountains to Yunnan Plateau: Rhabdothamnopsis Hemsl.

III5. Hengduan Mountains to Central China: Briggsiopsis K. Y. Pan, Petrocosmea Oliver.

III6. Himalaya: Platystemma Wallich.

2 Geographical distribution patterns

Tropical and subtropical Asia are the distribution centers of the subfamily Didymocarpoideae, harbouring 85% genus and more than 90% species of Didymocarpoideae. Indo-China Peninsula and Southwest China (Figs 1, 2), which are dominated by limestone landscapes (Clements et al. 2006), are places notable for recording the highest species density (Fig. 1 and Fig. 3). According to the updated phylogeny of the Asian Gesneriaceae (Möller et al. 2016b, 2017; Xu et al. 2017), most basal taxa of the Didymocarpoideae, like Rhynchotechum and Corallodiscus (Fig. 3), occur at India and Indo-China Peninsula and the nearby regions such as Sino-Vietnam region and Southwest Yunnan. This suggests that modern Didymocarpoideae probably originated in these regions.

Figure 1. 

Geographical distribution patterns of the 10 genera of the Asian Gesneriaceae that experienced extensive changes in species compositions.

2.1 Diversification and endemic centers

Our data recognized four species diversification centers (places with highest values of species density), i.e. Sino-Vietnam Region including boundary areas of Guizhou-Yunnan-Guangxi in Southwest China, Northwest Yunnan (Hengduan Mountains), Malay Peninsula and North Borneo (Fig. 3). In a study focusing on China’s Gesneriaceae, Liu et al. (2017) found that richness of Gesneriaceae peaked in Southwest China, and Hengduan Mountains and boundary areas of Guizhou-Yunnan-Guangxi are the most significant hotspots of species diversity and endemism. Our results closely coincided with their findings.

Indo-China Peninsula turned out to be an extraordinary diversification center, harbouring several endemic genera Tribounia, Billolivia, Chayamaritia (Fig. 2). These genera are newly evolved and contain very few species (Fig. 4). The Indian subcontinent has the lowest value of species density, with only two endemic genera, i.e. Jerdonia and Championia (Sri Lanka). Boea was no longer widespread in tropic Asia and its endemic center appeared in Papua New Guinea and the Solomon Islands (Puglisi et al. 2016; Puglisi and Middleton 2018) (Fig. 2). Based on molecular data from Möller and Clark (2013) and Roalson and Roberts (2016), most locally endemic species such as in Aeschynanthus and Cyrtandra were newly evolved, i.e. neoendemics.

Figure 2. 

Distribution localities of 15 genera of the Asian Gesneriaceae that experienced extensive changes in species compositions.

Figure 3. 

Species distributions pattern of the Asian Gesneriaceae. Black circles indicate diversification centers with highest species richness and the red grids are the evolutionary hotspots (at least 25% species are neoendemics). The species distribution information is obtained from http://www.gbif.org. The map was drawn using DIVA-GIS7.5.

Figure 4. 

Genera phylogeny with geographical distribution pattern of the Asian Gesneriaceae. The number in the brackets is the species diversity of the genus. Phylogeny tree was redrawn based on Möller and Clark (2013), Middleton et al. (2015), Puglisi et al. (2016), Möller et al. (2016a), Middleton et al. (2018).

2.2 Evolutionary hotspots

We determined places where at least 25% species are local endemics as ‘evolutionary hotspots’. Six evolutionary hotspots were identified, i.e. Northwest Yunnan (Hengduan Mountains), boundary areas of Yunnan-Guizhou-Guangxi in Southwest China, mountains in North Thailand, Malay Peninsula, North Borneo, and North Sulawesi (Fig. 3). These evolutionary hotspots were distributed largely in the diversification centers (Fig. 3), similar to findings of Liu et al. (2017) in which Hengduan Mountains and boundary areas of Yunnan-Guizhou-Guangxi were recognized as two hotspots of species richness of Chinese Gesneriaceae.

The geography of these six evolutionary hotspots was the most complex area in tectonic history, formed by the interaction of Indian, Eurasian, Australian and Pacific Plates (Hall and Spakman 2015). Therefore, the highly fragmented islands and limestone landscapes in Southeast Asia probably facilitated speciation of the Asian Gesneriaceae, similar pattern found in Begonia (Chung et al. 2014) and Alocasia (Nauheimer et al. 2012).

3 Origin and Evolution of the Asian Gesneriaceae

Burtt (1998) proposed that Gesneriaceae is of southern hemisphere (Gondwana) origin, with the Gondwana broken down and dispersed all over the world. This hypothesis is based on Gesnerioideae spreading to South America via the Antarctic and Didymocarpoideae by migrating northwards, ‘dropping’ representatives in Africa and Madagascar and finally reaching the Eurasiatic continent and spreading from there to the Malay Archipelago and the Pacific. This hypothesis, however, faces difficulties both from the geological time scale and the molecular data. Perret et al. (2013) reconstructed the biogeography history and suggested an origin of this family in southern America during the late Cretaceous period. The Gondwana break-up, however, began at about 150 Ma (Hall and Spakman 2015). Woo et al. (2011) indicated that there were two independent long-distance dispersals or overland migrations from South America to Australasia via Antarctica, but how they entered Asia or Africa is still unclear. The molecular data from Möller et al. (2009) and Roalson and Roberts (2016) show that the most basal species were found on the Indian subcontinent, such as Jerdonia (mountains of SW India), Corallodiscus (Himalayas and China), Tetraphyllum, Leptoboea and Boeica (Himalayas and adjacent areas). Only Rhynchotechum, about 18 species, which is widespread from Himalayas to Malay Archipelago, and one other species, even reaches New Guinea. Furthermore, Boea was the only endemic genus at the east side of the Huxley’s Line. Therefore, the Asian Gesneriaceae may have originated from the Indian subcontinent and/or Indo-China Peninsula, then dispersed to the east and the north and finally reached Southeast Asia and East Asia.

An up-to-date phylogeny indicated that Didymocarpoideae and Gesnerioideae probably separated at about 74 Ma (Roalson and Roberts 2016), when the Indian Plate had been separated from Gondwana (Hall and Spakman 2015). We propose two hypotheses for the origin of Didymocarpoideae. One is in India, whereby the ancestor of Didymocarpoideae dispersed via the south of South America and Antarctica to India, until about 45 Ma when the Indian Plate collided with the Eurasia Plate and rapid speciation occurred. This is in accordance with Burtt’s (1998) “Out of India” hypothesis.

The new position of Titanotrichum in the Gesnerioideae (Wang et al. 2004) suggests a possible dispersal event from the New World to Asia. Perret et al. (2013) proposed that the ancestor of Titanotrichum might either disperse across Beringia from North America to East Asia or originate at East Asia. This genus is distinctive for small and numerous bulbils in the inflorescence, which evolved at about Miocene (Wang and Cronk 2003) and probably facilitated its long-distance dispersal.

The alternative hypothesis is that the Asian Gesneriaceae might follow the ‘Malpighiaceae Route’ via the ‘North Atlantic land bridge’ to Eurasia (Davis et al. 2002). However, currently very limited experimental studies focusing on this scenario have been carried out and we cannot speculate on details about this hypothesis. To test such a hypothesis, molecular biogeographic studies on a pantropical genus such as Epithema and Rhynchoglossum are needed to figure out their historical dispersal route(s) between tropical America, Africa and Asia.

4 Mechanisms for species diversification

4.1 Growth forms

According to Roalson and Roberts (2016), epiphytism and unifoliate growth are two important growth forms impacting on the diversification rate in Gesneriaceae, like Monophyllaea and a section of Streptocarpus Lindl. in the Old World. Epiphytes and non-epiphytes have the same speciation rate, but epiphytism has a much lower extinction rate (Roalson and Roberts 2016). This means that epiphytism per se is not the driving factor for speciation, it probably can lower the extinction rate or is associated with other traits that promoting speciation. For example, there is a strong correlation between the epiphytic habit and ornithocory (dispersal of seeds by birds) (Weber 2004). In orchids, epiphytism is also often correlated with CAM photosynthesis (Givnish et al. 2015), but in Gesneriaceae only the New World Codonanthe crassifolia was confirmed to have some CAM-like characteristics (Guralnick et al. 1986).

Unifoliate growth form strongly suggests that growth form positively influences speciation rate (Roalson and Roberts 2016). Previous work on Streptocarpus shows the evolution of growth forms, especially rosulate and unifoliate growth and they believed this was an adaptation for deep shade and unifoliate growth increasing diversification rate (Möller and Cronk 2001). Cyrtandra has, however, also undergone a significant increase in speciation rate, probably associated with other characteristics such as seeds’ dispersal mode.

4.2 Specialized pollination adaptations

Normally, most Gesneriaceae species exhibiting zygomorphic flowers are thought to be more specialised in pollination adaptation, since it restricts pollinator behaviour and can therefore increase pollination efficiency (Gong and Huang 2009; Ling et al. 2017). Wang et al. (2010) and Ling et al. (2017) proposed that actinomorphy probably is a derived trait in the Asian Gesneriaceae, which is associated with shifts in pollination strategies, such as nectar- to pollen-rewards and/or from specialist to generalist pollinators.

Most Asian Gesneriaceae has the fused anthers, normally anthers are united by pairs, such as Loxostigma and Anna (Weber 2004). In some species, all the four anthers are fused or adnated, such as Beccarinda and Stauranthera (Weber 2004). Anther fusion can assemble the anthers to the same position and facilitate all the anthers touching the same locality of the pollinator’s body, which can greatly enhance the precision of cross-pollination (Ren 2008; Ren and Tang 2010). Wang (1990) indicated that anthers fusion with all stamens in the flower is late evolved than anther fusion in pairs and show a relatively higher level of pollination efficiency and consequently probably facilitate species diversifications.

There is a highly specialized pollination mechanism in the Asian Gesneriaceae, i.e. mirror-image flowers (Gao et al. 2006; Lu et al. 2019). Mirror-image flowers can be found in five genera in the Asian Gesneriaceae, i.e. Paraboea (Gao et al. 2006), Ornithoboea, Didymocarpus, Rhabdothamnopsis, and Henckelia (Lu et al. 2019). Mirror-image flowers are a sexual polymorphism in which the style deflects either to the left or the right side of the floral axis (Jesson and Barrett 2002; Gao et al. 2006). Jesson and Barrett (2002, 2003) pointed out that mirror-image flowers can increase the precision of cross-pollen transfer and may play an important role in pollination isolation and speciation. Normally, mirror-image flowers have reciprocal deflecting stamen(s) to the other side as compared with the deflecting style (reciprocal mirror-image flowers), which greatly increases pollen transfer efficiency (Jesson and Barrett 2003; Ren et al. 2013), but most mirror-image flowers in the Asian Gesneriaceae are non-reciprocal, without a deflecting stamen (Lu et al. 2019). Such unusual floral syndromes indicate unusual pollination adaptations in these species, but are awaiting further study.

4.3 Fruit adaptations to long-distance dispersal

In angiosperms, fruits significantly increase adaptive ability to withstand harsh environments and facilitate seed dispersal (Weber 2004). Fruit trait probably is a key trait for the high speciation rate and widespread range of both Aeschynanthus and Cyrtandra (Roalson and Roberts 2016). The hair-like appendages of seed in Aeschynanthus provide a favourable surface area to mass ratio (Denduangboripant et al. 2001), adapting to wind dispersal.

In Cyrtandra and Rhynchotechum, soft-fleshy (a true berry) fruits facilitate their colonisation throughout the Southeast Asia islands and nearby Pacific islands via bird dispersals (Cronk et al. 2005; Liu et al. 2017), and numerous islands in this area then promoted the speciation of the genus.

4.4 Extrinsic (environmental) factors

Compared to other regions, Asia is mostly dominated by the monsoon climate. There are three main types of summer monsoons in Asia, i.e. East Asia Monsoon, South Asia Monsoon and North-west Pacific Ocean Monsoon (Jiang et al. 2017; Kong et al. 2017). These three monsoons interact at Southwest China and Indo-China Peninsula and bring a large quantity of warm and wet air, thus providing a precondition for tropical plants to exist and facilitate the long-distance dispersal of the propagules. Monsoons do not only facilitate the northwards spread of tropical plants, but also aggravate the isolation of local habitat via the alternate dry and rainy seasons (Jiang et al. 2017), which might be related with the formation of diversification centers and evolutionary hotspots in Southwest China and Sino-Vietnam regions (Wang et al. 2011). More specifically, temperature changes since the Last Glacial Maximum had stronger effects on richness of rare species (Kong et al. 2017; Liu et al. 2017) while richness of common species was determined largely by current temperature seasonality such as monsoon climate (Liu et al. 2017).

Many studies had pointed out that microhabitat isolation caused by various landscapes such as limestone is the main factor for speciation in the Asian Gesneriaceae (Wang 1990; Ren 2015; Liu et al. 2017; Shui and Chen 2017). Especially for the three diversification and endemic centers, i.e. Sino-Vietnam Region, Malay Peninsula, North Borneo, the local landscapes are characterised by the various types of limestone landscapes (Clements et al. 2006; de Bruyn et al. 2014). Northern Borneo and Malaysia Peninsular were separated by the South China Sea, but they were connected during the glacial period and acted as a “land bridge” for plant dispersal across Southeast Asia (Hall and Spakman 2015). Frequent alternation of transformation between sea and continent intensified speciation in this area (de Bruyn et al. 2014).

Southwest China has the largest continuous limestone areas in the world, which includes Guizhou, Yunnan, Guangxi provinces and the Sino-Vietnam region (Clements et al. 2006; Hou et al. 2010; Ren 2015; Kong et al. 2017). South Yunnan is not only rich in limestone landscapes, but also comprises a series of spectacular north-south trending ridges along three major rivers of Asia: the Salween, Mekong and Red River, which have formed many unique microhabitats and microclimates, such as dry and hot valleys in Yunnan (Jiang et al. 2017). These diverse landscapes, forming ‘microhabitat islands’, greatly facilitated plant speciation (Clements et al. 2006; Ren 2015). Clements et al. (2006) and Chung et al. (2014) also proposed that these kinds of limestone microhabitats were formed largely by the East Asian monsoon (Jiang et al. 2017).

Northwest Yunnan (Hengduan Mountains), located at the eastern fringe of the Tibetan Plateau, is widely recognised as a globally important biodiversity hotspot (Myers et al. 2000; Liu et al. 2017) and the cradle of new species with an extraordinarily high ratio of recently evolved endemic species (neoendemics) that resulted from the uplift of the Himalayas and surrounding mountains (López-Pujol et al. 2011). It is noteworthy that not only neoendemics of Gesneriaceae have been found here, but most of the basal taxa also appeared here (Möller et al. 2009; Möller and Clark 2013; Roalson and Roberts 2016). Such a distribution pattern may relate to the Asian Gesneriaceae migration route (Möller et al. 2009).

In conclusion, we have discussed the biogeographic and diversification patterns of the Asian Gesneriaceae, along with underlying mechanisms of the family’s dispersal, adaptation and evolution. The family is still undergoing quick diversification and is awaiting further detailed studies not only about ecological adaptations but also evo-devo examinations on relationships between micro- and macro-evolution. Molecular biogeographic studies on the typical pantropic taxa using updated techniques such as sequenced restriction-site associated DNA (Baird et al. 2008; Feng et al. 2017) are also suggested to explore the historical dispersal patterns and evolutionary diversification of the family from tropical America to Africa and Asia.

Table 1.
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List of present genera of Asian Gesneriaceae.

Gernus Distribution Habitat Species number Taxonomic status Reference
Subfamily Gesnerioideae
Tribe Titanotricheae
Titanotrichum E China (Fujian and Taiwan) and Japan Shaded areas in valleys; altitude 100–1200 m. 1 Placed in subfam. Gesnerioideae Perret et al. 2013; Weber et al. 2013
Subfamily Didymocarpoideae
Tribe Epithemateae
Epithema Central tropical Africa, India, Sri Lanka, Nepal, southern China and through Southeast Asia and Malesia to the Solomon Islands. Shaded limestone rocks or caves in valleys. 20 No change at genus level Bransgrove and Middleton 2015
Gyrogyne S China (Bose Xian, W Guangxi) Shaded waysides in hilly regions at low elevations. 1 Position in Epithemateae-Loxoniinae uncertain
Loxonia Southeast Asia (Sumatra, Malay Peninsula, Borneo, Java) Damp places and humid rocks in deep shade. 3 No change
Monophyllaea Throughout Sumatra to New Guinea and from S Thailand and Luzon to Java Limestone rocks, in shady forests, at cave entrances and below rocks. >40 No change Möller et al. 2016b
Rhynchoglossum From India and S China to New Guinea, but one species distributed in Central America (Mexico, Colombia, Venezuela) Wet and shady (preferably limestone) rocks, in forest or open, shady places; usually in the lowlands. 16 No change
Stauranthera from NE India and S China throughout Malaysia to New Guinea Wet rocks and damp places in lowland rain forest. 7 No change
Whytockia S China (Sichuan, Guangxi, Hunan, Hubei, Guizhou, Yunnan and Taiwan) Shaded and moist areas in valleys, shaded streamside rocks and stream banks, altitude 500–2200 m. 8 No change
Tribe Trichosporeae
Aeschynanthus From S China, N & S India throughout Malesia to New Guinea and the Solomon Islands Epiphytically on trees (rarely on rocks or bare soil), lowland or montane rain forest. ~185 Emended by inclusion of Micraeschynanthus
Agalmyla Malaysia (Sumatra, Malay Peninsula, Borneo, Java, Sulawesi, New Guinea) Lowland and montane rainforest, mostly climbers. 96 No change
Allocheilos S China (Guizhou, E Yunnan) Rocks in limestone hills, altitude ca. 1400 m. 2 No change
Allostigma S China Limestone pavements; altitude ca. 200 m. 1 No change
Anna China, N Vietnam Grassy slopes or forests, rock crevices in limestone hills. 4 No change
Beccarinda NE India, Burma, S China, Vietnam, Sumatra Probably growing on humid rocks. 8 No change
Billolivia E Vietnam (Lam Dong) Submontane tropical evergreen closed forest at 1550 m alt. 7 Re-established for five species of Cyrtandra Middleton et al. 2014
Boea Eastern Indonesia, Papua New Guinea, the Solomon Islands and Queensland (Australia) Limestone, moorstone and argillite montane cliffs or shady places under the forest, altitude 100–3300 m. 11 Redefined; Chinese spp. now in Dorcoceras and Damrongia Puglisi et al. 2016; Puglisi and Middleton 2018
Boeica Bhutan, S China, N & NE India, Myanmar, N Vietnam, NW Malaya Shady and damp places and on humid rocks in forests, altitude 200–1400 m. 14 No change Möller et al. 2017
Briggsiopsis S China (C & S Sichuan, NE Yunnan, Guizhou) Forests, at stream sides and on rocks in shady places, altitude 250–1500 m. 1 No change
Cathayanthe S China (Hainan) Rocks, in wet valleys and ravines; altitude ca. 1800 m. 1 No change
Championia Sri Lanka Undisturbed forest, in shady places and loose soil along stream beds. 1 No change
Chayamaritia Central and eastern Thailand, Laos. Evergreen and submontane forest in deep shade at 150–1200 m altitude. 2 Genus recently established Middleton et al. 2015
Codonoboea S Thailand and throughout Malesia, S Japan, E China and Taiwan Primary forest granite, sandstone and quartz derived soils or rocks. 120 New combination for particular species of Henckelia and Loxocarpus Kiew and Lim 2011; Weber et al. 2011a
Conandron E China, Taiwan region of China, S Japan Humid and wet rocks in forests, altitude 500–1300 m. 1 No change
Corallodiscus Bhutan, China, N & NE India, Nepal, Thailand Rocks and rock crevices within forests or above the forest line, from 700 to nearly 5000 m. 5 No change
Cyrtandra Nicobar Islands and S Thailand through Malesia include Taiwan region of China and the S Pacific to the Hawaiian Islands Lowland and montane rain forests. >800 No change
Damrongia China to Sumatra Limestone rocks, usually in shade. 11 Re-established for particular species of erstwhile Chirita; inclusion of Boea clarkeana and the Asian species described in Streptocarpus Weber et al. 2011a; Puglisi et al. 2016
Deinostigma Southern China and Vietnam. Forests rocks and along trails and roadsides in forested areas; altitude 650–1200 m. 7 Expanded to included several species previously ascribed to Primulina Möller et al. 2016a
Didissandra W Malesia (Sumatra, Malay Peninsula, Borneo, Java) Lowland and montane rain forests. 8 No change
Didymocarpus From N and NE India, Nepal and S China southwards to the Malay Peninsula and N Sumatra Damp (usually acid) rocks or earth banks, in forest or above the forest line, altitude (rarely) sea level to 3500 m. 98 Some spp. transferred to Petrocodon Weber et al, 2011b
Didymostigma SE China (Guangdong, Fujian, Guangxi) & Vietnam Forests rocks and along trails and roadsides in forested areas; altitude 650–1200 m. 3 No change
Dorcoceras China, Thailand, Cambodia, Vietnam, Philippines and Indonesia Shady and damp rocks along trails and roadsides in forests; 100–1500 m. 4 Re-established for particular (non-Australasian) species of Boea Puglisi et al. 2016
Emarhendia Malay Peninsula Damp limestone rocks, especially at cave entrances. 1 No change
Glabrella S China, Taiwan region of China Forests damp rocks and crevices of rocks; 600-1800 m. 3 New genus estblished for 3 spp. of Briggsia not to be included in Oreocharis or Loxostigma Möller et al. 2014; Wen et al. 2015a,b
Gyrocheilos S China (Guangxi, Guangdong, SE Guizhou), Vietnam Forests wet places, in valleys and on rocks beside streams; altitude 400–1600m. 5 No change
Hemiboea C & S China, Taiwan region of China, N Vietnam, S Japan, NE India Forests and at forest margins rock crevices by streams and wet, shady places in karst regions; altitude 80–2500 m. 34 Inclusion of Metabriggsia (2 spp.) Weber et al. 2011c
Henckelia India, S China, Indo-China Peninsula, Malay Peninsula Acidic soils and rocks but not on limestone. ~60 Redefined to include Chirita p. p. (excl. Microchirita and Primulina) and Hemiboepsis, and to exclude Codonoboea Weber et al. 2011a; Middleton et al. 2013
Hexatheca Borneo (W Kalimantan, Sarawak to Sabah) Sandstone or limestone rocks. 4 No change
Jerdonia India (Nilghiri and Anamally Hills) Rocks in mountains 1 No change
Kaisupeea Myanmar, Thailand, S Laos Wet rocks and rocks crevices along streams and waterfalls 3 No change
Leptoboea Bhutan, N and NE India, S China (Yunnan), Myanmar, Thailand Hills and mountains 2 No change
Liebigia Sumatra, Java and Bali Forest plants, also in disturbed forest, open places and forest margins, river banks etc.; probably growing in acid soil (limestone not recorded, but ecological information generally scanty) 12 Raised from Chirita sect. Liebigia to generic rank Weber et al. 2011a
Litostigma China (Guizhou, Yunnan) Wet limestone rocks and at the entrance to caves. 2 Genus recently established Wei et al. 2010
Loxocarpus S Thailand and E Malesia Primary forests, often on sloping ground, river banks or on damp rocks. 20 New combinations Middleton et al. 2013
Loxostigma S China (Sichuan, Yunnan, Guizhou, Guangxi), N Vietnam Damp, mossy rocks or on tree trunks in forests 11 Recently inclusion of caulescent Briggsia species Möller et al. 2014
Lysionotus From N India and Nepal eastwards through N Thailand, N Vietnam and S China to S Japan Epiphytically on trees in forest or on damp mossy rocks; 300–3100 m. 29 No change
Metapetrocosmea S China (Hainan) Forests and stream sides, altitude 300–700 m. 1 No change
Microchirita From the Western Ghats of India to the foothills of the Himalayas, through continental SE Asia to Sumatra, Borneo and Java Wet, light to moderately shady places at cliff bases, on cliff walls in crevices and cracks, or at cave entrances. 37 Raised from Chirita sect. Microchirita to generic rank Wang et al. 2011; Weber et al. 2011a; Middleton 2018
Middletonia India, Bangladesh, Bhutan, China, Burma, Thailand, Laos, Cambodia, Vietnam, Malaysia Limestone or granite 5 Genus recently established for four species of Paraboea Puglisi et al. 2016
Orchadocarpa Malay Peninsula (Main Range) Montane forests, on acid soil. 1 No change
Oreocharis China, Thailand, Vietnam, Myanmar, Bhutan, NE India, Japan Shady and damp rocks by streams, in valleys or in forests on slopes or cliffs, dry shaded rocks, altitude 200–3600 m. >120 Expanded to include Ancylostemon, Bournea, Briggsia, Dayaoshania, Deinocheilos, Isometrum, Opithandra, Paraisometrum, Thamnocharis and Tremacron; Inclusion offurther ten spp. of Briggsia Möller et al. 2011b; Möller et al. 2014; Chen et al. 2014
Ornithoboea From S China and Vietnam southwards to N Peninsular Malaysia Rocks, in shaded, humid places; some (possibly all) species confined to limestone. 16 No change Scott and Middleton 2014
Paraboea Bhutan, China, Indonesia, Malaysia, Myanmar, Philippines, Thailand, Vietnam Usually growing on limestone (rarely quartzitic) rocks, in forest or sun-exposed places, altitude 100–3200 m. 141 Expanded by inclusion of Phylloboea and Trisepalum; removal of four species and placement in the new genus Middletonia Puglisi et al. 2011; Puglisi et al. 2016
Petrocodon China, N Vietnam, NE Thailand Shady places on rocks cliffs and rocks crevices of limestone hills or in broad-leaved evergreen forests; altitude sea level to 3500 m. 33 Expanded to include Calcareoboea, Didymocarpus, Dolicholoma, Lagarosolen, Paralagarosolen, Tengia and Wentsaiboea p. p. (exclude type) Wang et al. 2011; Weber et al. 2011b
Petrocosmea NE India, S China, Myanmar, Thailand, S Vietnam Damp rocks and shaded cliffs in forest and above the forest line, altitude 500–3100 m. 49 No change
Platystemma Nepal, Bhutan, N India, SW China Shady and damp rocks in valleys or dry cliffs, altitude 2300–3200 m. 1 No change
Primulina Essentially southern half of China and Vietnam Limestone >190 Enormous expansion of the previously monotypic genus by inclusion of Chirita sect. Gibbosaccus, Chiritopsis, Deltocheilos, and Wentsaiboea Wang et al. 2011; Weber et al. 2011a
Pseudochirita S China (C & W Guangxi), Vietnam Forests on limestone hills. 1 No change
Rachunia Thailand, Kanchanaburi province, Thong Pha Phum district, Ban E Tong, near the Thai-Myanmar border at 900 m. Moist evergreen forest on a slope in shade. 1 Genus recently established Middleton et al. 2018
Raphiocarpus S China and N & C Vietnam Montane regions, in shady and damp places under forests, on slopes near streams or in rock crevices. 14 No change since Weber 2004, but changes to be expected
Rhabdothamnopsis S China Dense forests, at streamsides in forested areas and in thickets along roadsides, altitude 1600–2200(–4600) m. 1 No change
Rhynchotechum NE India, Nepal, Bhutan, SW & S China, SE Asia and Malesia to New Guinea Under broad-leaved forest in valley, shady places near the stream, on the rocks, distributed from coast to 2200 m. 16 No change
Ridleyandra Malay Peninsula and Borneo Lowland and (more frequently) montane rain forests. 31 No change Yunoh and Dzulkafly 2017
Senyumia Malay Peninsula (Pahang: Gunung Senyum and adjacent localities) Rock faces in damp limestone caves 1 No change
Somrania Peninsular Thailand limestone 2 Genus recently established Middleton and Triboun 2012
Spelaeanthus Malay Peninsula (Pahang), Batu Luas Damp rock faces, especially at the entrance to limestone caves. 1 No change
Tetraphyllum NE India, Bangladesh, Myanmar, Thailand Damp rocks in forest 3 No change
Tribounia Thailand Crevices of karst limestone in deciduous forest. 2 Genus recently established Middleton and Möller 2012

Acknowledgements

Financial support was provided by the Innovative Team Program of Hainan Natural Science Foundation (2018CXTD334), National Natural Science Foundation of China (31670230 and 41871041) and the Postgraduate Innovative Grant of Hainan Province (Hyb2016-06).

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