Hiptage is an Asia-endemic genus of Malpighiaceae currently placed in the tetrapteroid clade, representing one of the seven inter-continent dispersions from New to Old World. A molecular phylogeny based on sequences of the internal transcribed spacer (ITS) region was recovered for the first time for the genus. Our results showed that the most recent common ancestor of Hiptage probably originated in the South Indo-China Peninsula and diversified in this region. Based on phylogenetic evidence and relevant morphological traits, we propose a new species; Hiptage incurvatum is characterised by mericarps with arcuate anterior lateral wings, two large glands on the dorsal sepals, and small glands on the remaining sepals. The new species is from Mt. Cangshan, Dali City (25°35'N, 100°02'E) in North Yunnan, Southwest China and is notable for its occurrence at high altitude, 1400 m (the highest distribution currently known for the genus). The implications of this unusual species for the dispersal and evolution of the genus are discussed.

Asia, Hiptage incurvatum, Malpighiales, taxonomy, tetrapteroid clade

Hiptage Gaertn. is a genus of Malpighiaceae currently comprising ca. 40 species (Anderson et al. 2006; Chen and Funston 2008; Ren 2015; Yang et al. 2018). Its species typically grow as woody lianas in the margins of evergreen and seasonal rainforests, in river valleys, or on limestone hills of South and Southeast Asia (Sirirugsa 1991; Srivastava 1992; Chen and Funston 2008). The genus is characterised by its many-flowered thyrse bearing mirror-image flowers with nectar secreting sepal glands, and a single mericarp per flower bearing three lateral wings (Anderson et al. 2006; Ren et al. 2013; Zhang et al. 2016). Mirror-image flowers are a sexual polymorphism in which the style is deflected away from the floral axis, resulting in mirror images between the left-styled flower and right-styled flowers, facilitating cross-pollination (Jesson and Barrett 2002; Ren et al. 2013). Currently, the genus is placed in the tetrapteroid clade, one of the ten major lineages recovered for Malpighiaceae by Davis and Anderson (2010). Hiptage was represented in that phylogeny by six species and recovered as sister to Flabellariopsis R.Wilczek, an African endemic, and together both genera form a poorly supported clade, sister to the Neotropical genus Carolus W.R.Anderson (Davis and Anderson 2010). However, the monophyly of Hiptage has never been properly tested by the inclusion of its type species (Jacobs 1955; Davis and Anderson 2010; Zhang et al. 2016).

During recent field studies addressing the pollination ecology of Hiptage in North Yunnan, two populations of an unusual morphotype of Hiptage benghalensis were discovered near Pingpo Town, in Mount Cangshan near Dali City. After molecular and morphological analyses, based on the nuclear internal transcribed spacer (ITS) region and on the comparison of living and herbarium specimens (including type specimens of all currently accepted names in the genus), we concluded that these abovementioned populations represent an undescribed species of Hiptage. We present a molecular phylogeny sampling 17 of 39 species of Hiptage, including a discussion on the systematics and biogeography of the genus, besides the formal description of the new species and an updated key for the genus in China.

For the 17 Hiptage species, we obtained 36 sequences of ITS in total. Source information and the GenBank accession numbers of the new sequences are listed in Table 1. The dataset had an aligned length of 691 base pairs (bp), containing 128 parsimony-informative characters.

In the ITS tree (Fig. 1) Hiptage was recovered as monophyletic, strongly supported (PP/BS=1/100) by both analyses, with H. stellulifera from Vietnam as the first diverging lineage in the genus. The remaining species of Hiptage sampled formed two separate clades, although with weak support (PP/BS=0.64/52). Most species of Hiptage show reflexed petals (red line), with all species bearing erect petals (i.e., H. lucida, H. bullata, and H. minor) being recovered on a single clade, suggesting a single origin of erect petals in the genus (Fig. 1). The four specimens of the proposed new species, H. incurvatum, coalesced in a clade with strong support (PP/BS=1/100%) (Fig. 1). This clade was recovered in a polytomy, the H. multiflora + H. tianyangensis clade, from Guangxi Province, and the widespread H. benghalensis clade, from Southwest China and Indo-China Peninsula (Fig. 1). Relationships among these four species are mostly poorly supported (PP/BS=0.73/-) with the exception of the strongly supported H. multiflora + H. tianyangensis clade (PP/BS=1/98).

Figure 1. 

Molecular phylogeny for 17 species of Hiptage and two Neotropical outgroups based on ITS sequences. Bayesian posterior probability (PP) and MP bootstrap values (BS) are showed above branches as PP/BS (only shown if BS > 50%). H. incurvatum was shown in grey. The red, blue, black clades indicate reflexed petals, erect petals, and unknown, respectively. Inserted photos indicate petal-reflexed flowers (red branches) and petal-plat flowers (blue branches). Black branches represent the unclear mode.

Taxonomy

Hiptage incurvatum K.Tan & M.X.Ren, sp. nov.

urn:lsid:ipni.org:names:77203327-1

Figs 2, 3

Type

China. Yunnan Province: Pingpo Town, Mt. Cangshan, Dali City, 25°35'N, 100°02'E, 1400 m altitude. 31 Mar 2019, K. Tan and M.X. Ren 2019033110 (holotype: HUTB!, isotypes: HUTB!, KUN!)

Diagnosis

Similar to H. tianyangensis in ovate leaf shape, suborbicular petals; but differing from this species by sepal glands twice big as H. tianyangensis (vs. sepal gland, ~ 3 × 1 mm), the elevation ca. 400 m (vs. 1379–1724 m), the short inflorescence 1–4 cm (vs. 4–10 cm).

Description

Woody lianas; stems 20–30 (–200) mm diam. Branches round, lenticels white or greenish, tomentose to glabrous, with white to grey hairs. Leaves opposite; stipules absent; petioles ca 0.5 cm long, round, tomentose, with white hairs, eglandular; leaf blades 6–12 × 2.5–4.5 cm, elliptic, base cuneate, margin plane, apex attenuate, both surfaces sericeous, 10–16-glandular dots abaxially near margin, lateral veins 5–8 pairs, prominent on both surfaces. Thyrses, solitary, axillary or terminal; main axis 4–10 cm long, tomentose, with white hairs; peduncles 1.5–2.5 cm long, tomentose; bracteoles inserted below the apex of peduncles, 0.3–0.5 cm long, lanceolate. Flowers with pedicels 1.5–2.5 cm long, sericeous, with white hairs; sepals 5, ca. 0.5 cm long, elliptic to oblong, margin slightly revolute, apex rounded, adaxial surface glabrescent, abaxial surface white tomentose; glands 4 (–6), 0.5–3 × 0.5–1 mm, prominent, rounded, restricted to sepals, two large, basally fused glands on the dorsal sepals, remaining glands small and free; petals white to light pink, yellow at the base, ca. 1 × 0.8 cm, suborbicular, extremely reflexed, claws ca. 1 mm long. Stamens 10, filaments white or light yellow, free or basally fused, 7–13 mm long, glabrous; anthers ca. 0.5 × 0.3 cm, ovate, pubescent, with yellow hairs; pollen sacs dehiscing longitudinally. Ovary ca. 2 mm diam.; styles 1, light pink, ca. 13 mm long, curved upwards, deflected either to the left or right side, glabrous; stigma apical. Mericarps 3, each flower developing up to three mericarps, detaching from a pyramidal torus; individual mericarps three-winged (laterally placed in the nut), wings pink with greenish base, the posterior wing ca. 3.6 × 1.3 cm, ovoid, apex round or slightly lobed, with white or brown hairs; anterior lateral wings ca. 2.3 × 0.7 cm, lanceolate, arcuate back to the middle; nut ca. 0.2 cm, round or slight ovate, glabrous; areole ca. 0.3–0.6 cm, roughly triangular. Seeds angular-globose, ca. 3–5 mm, dark yellow or brown.

Figure 2. 

Hiptage incurvatum K.Tan & M.X.Ren, sp. nov. A, B habit C flowering branch D flower in frontal view E flower with petals removed in sideview F flower with petals removed in dorsal view showing two large glands on the dorsal sepals) G flowers in sideview H detached petals I young leaf in adaxial view J young samaras K mature samaras L leaf branch in adaxial view. Photos A–C by M. X. Ren, J, K by H. L. Zheng and D–I, L by K. Tan.

Figure 3. 

Line drawing of Hiptage incurvatum K.Tan & M.X.Ren, sp. nov. A flowering branches B flower (in sideview) C sepals showing two large glands on the dorsal sepals and small glands on the remaining sepals D samara in dorsal view, showing the curved lateral wings E samara in sideview. Drawings by Ya-Jing Zhang based on K. Tan and M.X. Ren 2019033109 (HUTB).

Additional specimens examined (paratypes)

China. Yunnan Province: Pingpo Town, Mt. Cangshan, Dali City. 31 Mar 2019, K. Tan and M.X. Ren 2019033109 (HUTB), K. Tan and M.X. Ren 2019033108 (KUN).

Phenology

Flowering from April to May, and fruiting in May.

Distribution and habitat

Hiptage incurvatum is only known from two localities near Mt. Cangshan, Pingpo Town, Dali City, North Yunnan, growing on soil slopes or forest margins and river valleys, at 1400–1700 m. In China, a total of 13 species of Hiptage now have been recorded, 10 of which, including the new species, are endemic to the country (Chen and Funston 2008; Ren 2015; Yang et al. 2018).

Figure 4. 

Distribution map of the new species Hiptage incurvatum and the other 12 species of the genus known in China and nearby regions.

Etymology

The specific epithet reflects the arcuate and curved anterior lateral wings of the three-winged samara.

Vernacular name

Chinese: 弯翅风筝果 (wān chì fēng zhēng gǔo). The name ‘wān chì’ means arcuate wing, ‘fēng zhēng gǔo’ is the Chinese name of Hiptage.

Conservation status

The only two known populations of Hiptage incurvatum are in Pingpo Town of Dali City, in a river valley near Mt. Cangshan. These two populations have about 50 individuals in total along the woodland margins or slopes of the valley near a road. Very limited information is known about the new species. Therefore, H. incurvatum can be treated as Near Threatened (NT, close to being at high risk of extinction in the near future under the criterion [B1ab(iii) + 2ab (iii)] according to the IUCN Red List criteria (IUCN 2013).

Notes

The new species can be clearly identified from three similar species (H. benghalensis, H. multiflora, H. tianyangensis) from the following traits. Leaf: H. incurvatum (ovate, 6–12 × 2.5–4.5 cm) is smaller than all the three species, i.e. H. tianyangensis (ovate, 7–12× 3–5.5 cm), H. multiflora (oblong, 12–13 × 5–5.5 cm), H. benghalensis (elliptic, 9–18 × 3–7cm). Petal color: H. incurvatum (white with light pink), H. tianyangensis (white), H. multiflora (pink), H. benghalensis (white with yellow on the vexillum). Calyx glands: H. incurvatum (2 large and fused at the lower part, not decurrent to the pedicel; sometimes 2 or 4 smaller glands can be seen on other sepals), H. tianyangensis (2, small, clearly isolated, not decurrent to the pedicel), H. multiflora (1, large, not decurrent to the pedicel), H. benghalensis (1, very large, 1/2 adnate to the pedicel).

We provide here the first well-sampled phylogenetic study for the Asian endemic Hiptage, although this phylogeny is based on a single marker and most clades are not highly supported. Hiptage is one of the largest Old-World genera of Malpighiaceae, being adapted to various habitats such as forest edges, river valleys and limestone hills in Asia (Sirirugsa 1991; Ren 2015; Yang et al. 2018). Our phylogenetic tree shows that two species from South Vietnam and Thailand (i.e. H. stellulifera and H. detergens) were recovered as basal groups, suggesting the genus might have evolved at the southern part of Indo-China Peninsula (Fig. 1).

Based on the phylogeny tree, the most widespread species in the genus, H. benghalensis, might have appeared late in the evolution of the genus, although we are not providing divergence time estimates. H. benghalensis is well-known for its extremely reflexed petals and single oversized calyx gland secreting nectar, attracting both pollinators and herbivory-defending ants (Ren et al. 2013). Such floral syndromes indicate generalized pollination by pollen-collecting bees (Ren et al. 2013; Qian et al. 2016), which can explain the widespread distribution of H. benghalensis. Moreover, both our data and the results of Davis and Anderson (2010) demonstrated the polyphyly in H. benghalensis (Fig. 1), suggesting this most widespread species might be treated as two taxa. Further studies are still needed to properly address this question with more extensive sampling.The petal shape and calyx glands are diagnostic traits of the family Malpighiaceae, being used for species identification and taxonomic study (Niedenzu 1924; Anderson et al. 2006; Chen and Funston 2008; Ren 2015). The phylogeny indicates that reflexed petals may be common in both basal and nested clades, and flat petals probably evolved only once (Fig. 1). Normally there are ten oil secreting calyx glands in Neotropical Malpighiaceae, with two glands on each sepal (Anderson et al. 2006). In Hiptage, however, most species show a single calyx gland, but secreting nectar instead of oil (Ren et al. 2013). In the basal H. stellulifera, five calyx glands were found (i.e., each sepal shows a single gland) (Hô 1992). Therefore, one of the evolutionary trends in Hiptage appears to be the numeric reduction of calyx glands (Anderson et al. 2006; Ren et al. 2013; Ren 2015).

The multiple accessions of the proposed new species were recovered as a strongly supported clade (Fig. 1), separated from closely related taxa by weak molecular, but several morphological traits (Fig. 2). Specifically, the new species is distinctive in having two large glands on the dorsal sepals and two small glands on the remaining sepals (Figs 2E–F, 3C). Interestingly, the lower parts of the two large glands are fused (Figs 2F, 3C), indicating a possible explanation for the evolution of the single oversized calyx gland in H. benghalensis (Anderson et al. 2006; Ren et al. 2013). The similar evolutionary trend was also found in the Paleotropical genus Acridocarpus (Malpighiaceae) (Guesdon et al. 2019), in which the adjacent sepal glands show different degrees of fusion in several species and the single sepal gland in some species shows sagittate-acute shape, shared secretory tissues and vascular bundles, providing strong evidence of the fusion of two glands on adjacent anterior sepals (Vogel 1990; Guesdon et al. 2019).

Molecular data showed that H. incurvatum is closely related to H. tianyangensis, H. multiflora and H. benghalensis. These species, however, differ significantly in habitat type, and in calyx gland and mericarp morphology (see Key). The new species grows along a river valley at very high latitudes (>1300 m) in North Yunnan, while H. multiflora and H. tianyangensis normally grow at the top of limestone mountains in Guangxi and H. benghalensis is widespread in Asia in forest margins and riversides (Anderson et al. 2006; Ren 2015).

The most distinctive trait in the new species is the arcuate anterior lateral wings of the three-winged mericarp (Figs 2J–K, 3D). Winged mericarps are an adaption for wind dispersal of fruits (Tan et al. 2018) and the striking diversity of winged mericarps types in Malpighiaceae indicates that this morphology played a role in long-distance dispersals and speciation (Davis et al. 2001, 2002; Qian and Ren 2016; Tan et al. 2018). Pingpo Town is located at the northern edge of the distribution range of the genus Hiptage. The surrounding mountains and gorges form a unique isolated habitat, which might be the main reason for the evolution and maintenance of the new species.

We presented the first well-sampled phylogeny of Hiptage, based on the ITS region, suggesting that the southern part of Indo-China Peninsula may be the area of origin of the genus. It also indicates that the erect petals have probably evolved only once in the genus. The number of calyx glands in Hiptage seems to have decreased during the genus evolutionary history. And specimens from Mt. Cangshan in North Yunnan were treated as a new species due to forming a highly supported clade in our phylogenetic study and being morphologically distinct from all accepted species in Hiptage.

We are grateful to Ding Song and Min Li for providing locality information and all reviewers (Augusto Francener, Kenneth Wurdack, Rafael Felipe de Almeida, Ricarda Riina and Wen-Heng Zhang) for their insightful comments. This study was financially supported by the Innovative Team Program of Hainan Natural Science Foundation (2018CXTD334), National Natural Science Foundation of China (31670230) and Postgraduate Innovative Grant of Hainan Province (Hyb2016-06).