Phylogenetic relationship
With extensive taxon and gene sampling, this study retrieves a well-supported topology for most clades, although some subclades within the genera Taxillus and Scurrula exhibit weak support (Fig. 1). Our results demonstrate that the subtribe Scurrulinae is non-monophyletic, with one species, Taxillus wiensii, nested within the African Loranthaceae cldade. Phyllodesmis is strongly supported as sister to the two genera, Taxillus and Scurrula. Morphological characters are useful to support relationships within the subtribe, particularly the glabrous young stems and leaves can distinguish Phyllodesmis from Taxillus and Scurrula (Fig. 2A, B). Taxillus wiensii clade characterized by bract shape, flower part number, flower pedicel (Fig. 3B, C, D), while, the clade of Taxillus and Scurrula characterized by bract length (Fig. 4A). Our character optimizations suggest that the two genera Taxillus and Scurrula are very similar in morphology, and they share ancestral morphological states of most characters. However, they have evolved differently in the shape of fruit and stigma (Fig. 4B, C). Based on our observation of specimens and fresh plants in the field, fruits of Scurrula are always pyriform or clavate sometimes, while those of Taxillus are usually ellipsoid, ovoid, or cylindrical.
Scurrula comprises around 50 species in China and Southeast Asia. Our phylogenetic analysis revealed unexpected relationships between the S. parasitica complex and the S. chingii complex (Fig. 1). S. parasitica was found to be a complex member in this study based on molecular data, with two varieties: S. parasitica var. parasitica and S. parasitica var. graciliflora. Our results demonstrated that S. parasitica var. parasitica and S. parasitica var. graciliflora are not monophyletic (Fig. 1). Moreover, S. parasitica var. graciliflora is distantly from S. parasitica in the molecular phylogenetic tree (Fig. 1), which can be easily distinguished from S. parasitica var. parasitica by its greenish-yellow corolla (versus red corolla in S. parasitica var. parasitica). Based on our findings, we suggest that S. parasitica var. graciliflora should be redefined as a separate species. A detailed treatment of this taxon will be provided in a future study.
Scurrula chingii is composed of two varieties: S. chingii var. yunnanensis and S. chingii var. chingii [8]. Both varieties are non-monophyletic by Liu et al. [5] and our study (Fig. 1). Although the position of S. chingii var. yunnanensis is uncertain in our phylogenetic tree, it is distant from S. chingii var. chingii as reported by Liu et al. [5]. Furthermore, S. chingii var. yunnanensis can be easily distinguished from S. chingii var. chingii based on several characteristics, including glabrous leaf blade surfaces (versus rusty red tomentose or glabrous abaxial surface in S. chingii var. chingii), shorter peduncle and floral axis less than 10 mm (vs. 10–25 mm in S. chingii var. chingii), and lanceolate corolla lobes (versus subspatulate lobes in S. chingii var. chingii). Additionally, Scurrula chingii var. yunnanensis is endemic to Yunnan (China), while S. chingii var. chingii is distributed in Guangxi, southern Yunnan (China), and northern Vietnam. Based on our results, S. chingii var. yunnanensis should be redefined to the species rank. The detail treatment will be provided in a future study.
Taxillus includes approximately 35 species from tropical Asia (India and Sri Lanka to China, Japan, Philippines, Borneo) and Africa (Kenya coast). Taxillus is generally characterized by low host specificity. Taxillus chinensis (DC.) Danser, a Malesian species, is widely distributed in west of Charles’s Line. On the other hand, T. wiensii Polhill, the only species of Taxillus in East Africa, has a narrow distribution limited to the Kenya coast.
Polhill and Wiens [7] suggested that although the morphology of T. wiensii is similar to the species of Taxillus in Sri Lanka, the flowers of T. wiensii appear different from the Asiatic species due to the erect and possibly spontaneously open corolla-lobes. Additionally, Polhill and Wiens [7] proposed that T. wiensii is more comparable to the African genera that have been segregated from sections of Taxillus based on flower characteristics, such as sect. Bakerella (Tieghem) Balle, sect. Remoti, and sect. Septulina. Furthermore, all species of Loranthaceae in continental Africa and Madagascar, except Socratina and one species of Septulina, can be distinguished by their flowers that open spontaneously with erect or spreading corolla-lobes, rather than explosively as in Taxillus. Bakerella is entirely glabrous, while Socratina is hairy, with a unique occurrence of fine indumentum on the inner face of the corolla-lobes. In terms of morphology, T. wiensii can be distinguished from the Asian Taxillus by its 5-merous (rather than 4 merous) flowers and bract shape (as shown in Fig. 3C). Our analyses of character optimizations indicate that T. wiensii and the Asian Taxillus have evolved differently in terms of flower and bract structure. It is difficult to improve the generic classification without detailed consideration of relationship between T. wiensii and the Asian Taxillus species [7]. Our molecular results indicate that T. wiensii is placed within African Loranthaceae and is clearly different from the Asian Taxillus (Fig. 1). Therefore, we strongly suggest that the African Taxillus should be recognized as a new genus, and we propose the name Afrotaxillus for this taxon.
Furthermore, our molecular analyses revealed that Taxillus limprichtii and its variety T. limprichtii var. longiflorus (Lecomte) H. S. Kiu do not form a monophyletic group. Therefore, we recommend that their taxonomic classification be reevaluated in future studies.
Phyllodesmis, comprised four species, was initially described by Tieghem [11]. However, subsequent research reduced this genus to a synonym of Taxillus, incorporating T. delavayi (Tieghem) Danser, T. kaempferi (Candolle) Danser, T. caloreas (Diels) Danser, and T. renii H.S. Kiu [8]. Our results support Phyllodesmis as a distinct clade from Taxillus and Scurrula with strong support (Fig. 1). Moreover, the Phyllodesmis clade includes only P. delavayi, a species that does not parasitize species of Pinaceae, unlike the remaining three species. Furthermore, Phyllodesmis can be easily distinguished from all other Taxillus members based on characteristics of leaves alternate (as apposed to opposite or subopposite), glabrous young branchlets (not densely stellately hairy), and both surfaces of leaves glabrous (not hairy on at least one surface) (Fig. 7). Thus, we suggest reinstating Phyllodesmis as a recognized genus, comprising only one species, P. delavayi.
Taxonomic treatment of Phyllodesmis
Phyllodesmis Tiegh. in Bull. Soc. Bot. France 42: 255. 1895 (Fig. 7)
Aerial parasite, small shrubs, glabrous. Leaves alternate, sometimes subopposite, pinnately veined. Inflorescences at leafless node, umbels 2–4-flowered; 1 bract subtending each flower, usually scale-like. Flowers bisexual, 4-merous, zygomorphic. Calyx ellipsoid or ovoid, rarely subglobose, base not attenuate, limb annular, entire or denticulate, persistent. Mature flower bud tubular, tip ellipsoid. Corolla sympetalous, slightly curved, basal portion ± inflated, split along 1 side at anthesis, lobes all reflexed toward the side away from the split, red, glabrous. Stamens inserted at base of corolla lobes; filaments short; anthers 4-loculed. Pollen grain trilobate or semilobate in polar view. Ovary 1-loculed; placentation basal. Style filiform, 4-angled; stigma usually capitate. Berry ellipsoid or ovoid, exocarp leathery, verrucose or granular, rarely smooth, pubescent or glabrous, base rounded.
Phyllodesmis delavayi Tieghem, Bull. Soc. Bot. France 42: 255. 1895. Taxillus delavayi (Tieghem) Danser, Verh. Kon. Ned. Akad. Wetensch., Afd. Natuurk., 29(6): 123. 1933. Type: China, Yunnan, Dali, Feb. 1887, Delavay 2620 (P!).
Morphology
—Aerial parasite, small shrubs ca. 0.5-1 m tall, glabrous. Branches gray-brown to blackish, often very minutely transversely wrinkled, young branchlets glabrous. Leaves alternate, sometimes subopposite, petiole 2–4 mm; leaf blade ovate, or elliptic to lanceolate, 3–6 × 1.3–2.5 cm, leathery, both surfaces glabrous, lateral veins 3 or 4 pairs, base cuneate, slightly decurrent, apex obtuse, adaxial surface of young leaf brown, especial leaf edge; abaxial surface green. Umbels solitary or 2 together, sometimes at leafless node, 2-7-flowered; peduncle 0–2 mm; bracts ovate, ca. 2 mm, glabrous, rarely long bearded at tip. Pedicel 5–15 mm. Calyx ellipsoid, ca. 2.5 mm, limb annular, entire or minutely 4-toothed. Mature bud 4–5 cm, tip ellipsoid, tip inside yellow. Corolla red, slightly curved, glabrous, lobes lanceolate, 3–9 mm, reflexed. Filaments short ca. 2 mm; anthers 1.5 mm. Ovary 1-loculed; placentation basal. Stigma capitate. Berry yellow or orange, ellipsoid, 8–10 × 3–4 mm, glabrous.
Phenology
—Flowering in Feb–May, fruiting in Apr–Sep.
Habitat
—Forests, mountain slopes; 1500–3000 m.
Conservation
—While not threatened as a species, and not listed under IUCN criteria, some populations of Phyllodesmis do require protection from over collection for medicinal use.
Distribution:—China: Yunnan, Guangxi, Sichuan, Xizang; Myanmar, and Vietnam: Lao Cai, Lai Chau.
Selected specimens examined:—VIETNAM: Lao Cai: Sapa district, San Sa Ho commune, Cat Cat village, October 2019, Van Du Nguyen, Hung Manh Nguyen, Xuan Thanh Trinh and Chi Toan Le DMTT38, DMTT39 (HN). CHINA: Sichuan: Dêrong County, Zigen, Jul 1981, Qinghai-Tibetan Expedition Team 1734 (PE); Shimian County, 1955, C.J. Xie 39892 (PE). Xizang: Zayü County, Shangchayu, Jul 1980, C.C. Ni et al. 740 (PE). Yunnan: Wenshan County, Mt. Laojun, April 1993, Y.M. Shui 1904 (PE); Dêqên County, Benzilan, July 1981, Qinghai-Tibetan Expedition Team 1864 (PE).
Historical biogeography of Scurrulinae
Asian origin of Scurrulinae
Our divergence time estimations for Scurrulinae are consistent with those from Magallón et al. [45], Grímsson et al. [26], and Liu et al. [5] (Table S5). The biogeographic analyses and divergence time estimations suggest that the stem group of Scurrulinae originated in Asia ca. 32.37 Ma during the Oligocene (node 3, Figs. 5, 6; Table 3), with a crown age dating back to 25.46 Ma (95% HPD: 19.54–31.58 Ma; node 4, Figs. 5, 6; Table 3). The Indian subcontinent began rifting from Australia-Antarctica ca. 136 Ma [44], and connected to mainland Asia ca. 44 Ma. Thus, the connection between India and Asia occurred much earlier than the origin of the Scurrulinae. According to Li et al. [46], the uplift of high mountains in Asia during the Oligocene-Miocene, combined with the southwest monsoon in Asia, probably provided ideal conditions for colonization and wide distribution of Scurrulinae. Additionally, short-distance dispersal in Asia is also important for domination or wide distribution of plants. Therefore, Asian Scurrulinae, including Indian Scurrulinae, likely originated in Asia and may have spread throughout the area by birds or small animals [47–49].
Our study confirms the findings of Liu et al. [5] that Asian Loranthaceae migrated from Australia in the late Eocene. Notably, despite several species of Scurrulinae being found in Malaysia, Indonesia, and the Philippines [4, 8, 9], which are geographically close to Australasia, there is no evidence of Scurrulinae dispersing from Asia to Australasia. While several Loranthaceae genera are common to both regions, including Lepeostegeres, Amylotheca, Decaisnina, Macrosolen, and Cecarria [5], our study, along with Liu et al. [5] suggests that all migration events from Asia to Australasia occurred before about 35 Ma, which is earlier than the origin of Scurrulinae. Thus, the Phyllodesmis, Taxillus and Scurrula of Scurrulinae may be endemic genera to Asia.
Liu et al. [5] proposed that within-area speciation events are more prevalent in most of the large clades that are endemic to single areas of Loranthaceae. They suggested that dispersal without “range contractions” was the main driver of range evolution, occurring more frequently than vicariance events. Our BSM results (Table S4) are consistent with Liu et al. [5] that within-area speciation events are the main factor in creating the Asian endemic group of Scurrulinae. Dispersal events have been considered as the most common factor for worldwide distributed plants, including Loranthaceae and Scurrulinae lineages [5, 41]. Our BSM indicates that the dispersal events of Scurrulinae occurred without “range contractions” or “founder events”, which is consistent with biogeographic history of the subtribe Scurrulinae (Fig. 6). After originating in Asia, Scurrulinae did not disperse to other regions. African Loranthaceae evolved from an Asian ancestor [5], and Taxillus wiensii originated in Africa from the African Loranthaceae ancestor. Short-distance dispersal events between proximal regions appear to have been frequent in the historical biogeography of Scurrulinae, and it may have been facilitated by the colonization or domination of Scurrulinae host plants in tropical forests.
Species of Loranthaceae are distributed worldwide [2, 4, 5, 8]. However, due to geographic distance, climate change, and special evolutionary direction, they are becoming endemic groups for each continent, resulting in fewer shared genera. Our resultssuggest that Scurrulinae originated and diverged in Asia during a period when rainforests dominated the continent [50] (Fig. 6). The members of this subtribe evolved and adapted to the living conditions in Asia, and the rapid climate changes, cooling, drying, and the progressive uplift of the high mountains in central Asia, especially during the late Pliocene and Pleistocene, might have promoted the diversification of Scurrulinae and prevented their dispersal to other continents. Our study does not recognize any migration of Scurrulinae to other continents since the early Oligocene, except for one species of Taxillus that originated in Africa.
African origin and diversification of “Afrotaxillus”
The present study supports that the placement of “Afrotaxillus wiensii” (Taxillus wiensii) within Africa Loranthaceae and its close relationship to Tapinanthus constrictiflorus (Figs. 1, 6). Biogeographic analyses indicate that “Afrotaxillus” originated and diversified in Africa (Fig. 6), and this genus is likely not part of Scurrulinae. Taxillus wiensii, formerly known as “Afrotaxillus wiensii” was considered as the only member of Taxillus in Africa, with dispersal from Asia to Africa proposed to explain its historical biogeography [5, 7]. However, this study confirms that the ancestor of “Afrotaxillus” is African Loranthaceae, and this genus likely evolved separately from Taxillus in Asia ca. 17 Ma (Figs. 5, 6). A similar situation was encountered in the genus Helixanthera, with Liu et al. [5] demonstrating differences between African and Asian Helixanthera and suggesting that African Helixanthera may be recognized as a distinct genus in the future studies.