Open Access
Translator Disclaimer
23 March 2021 Artabotrys angustipetalus (Annonaceae), a new species from Thailand, including a plastid phylogeny and character evolutionary analyses of thorn occurrence in Artabotrys
Ekkaphon Photikwan, Anissara Damthongdee, Hathaichanok Jongsook, Tanawat Chaowasku
Author Affiliations +
Abstract

Artabotrys R. Br. is one of the larger genera of Annonaceae with over 100 species distributed throughout the palaeotropics plus northern Australia. Although the genus is morphologically very well circumscribed, species delimitation is quite problematic owing to overlapping morphological characteristics. In Thailand, 20 species of Artabotrys have been reported, including A. multiflorus C. E. C. Fisch. Detailed comparisons with the type specimen from Myanmar revealed that A. multiflorus occurring in Kanchanaburi Province of Thailand represents a new species herein described as A. angustipetalus Photikwan & Chaowasku. The new species differs from A. multiflorus by having fewer flowers per hook, linear (vs oblong to oblong-lanceolate) petals, acute (vs obtuse) petal apex, longer and narrower petals and fewer carpels per flower. A multi-locus plastid phylogeny including an accession of A. angustipetalus and 30 accessions of other species of Artabotrys has been reconstructed. The results uncover a well-supported clade consisting of thorn-bearing species of Artabotrys, with A. angustipetalus recovered outside this clade. To understand the evolution of thorns in Artabotrys, ancestral character-state reconstructions were carried out; this trait is inferred to have evolved only once in Artabotrys. The benefits of thorns in Artabotrys species are discussed and hypothesized.

Citation: Photikwan E., Damthongdee A., Jongsook H. & Chaowasku T. 2021: Artabotrys angustipetalus (Annonaceae), a new species from Thailand, including a plastid phylogeny and character evolutionary analyses of thorn occurrence in Artabotrys. – Willdenowia 51: 69–82.

Version of record first published online on 23 March 2021 ahead of inclusion in April 2021 issue.

Introduction

Artabotrys is one of the larger genera of Annonaceae, a pantropical family of flowering plants consisting of c. 2430 species (Couvreur & al. 2019) in 108 genera (Guo & al. 2017; Chaowasku & al. 2018a, 2018b; Xue & al. 2018; note that Friesodielsia Steenis and Schefferomitra Diels are synonymous, see Saunders & al. 2020; and Melodorum Lour. has been synonymized with Uvaria L., see Turner 2018). Artabotrys, with over 100 species distributed in tropical forests of Africa-Madagascar, Asia, New Guinea and Australia, has been classified in the tribe Xylopieae of the subfamily Annonoideae (Chatrou & al. 2012). Artabotrys is mainly characterized by (1) hooked peduncles and inflorescence axes, (2) inner petals that are generally constricted over the reproductive organs, (3) biovulate carpels, with basal placentation and (4) sessile to shortly stipitate monocarps (Keßler 1993; Chen & al. 2018; Chen & Eiadthong 2020). Species of Artabotrys develop a climbing habit with the help of hooked peduncles and inflorescence axes, but sometimes appear as straggling shrubs (e.g. in A. spinosus Craib; Chalermglin 2001; personal observations). Moreover, some species even possess thorns, a rare character in Annonaceae; these thorns are generally observable on the lower part of plants (Posluszny & Fisher 2000; Chalermglin 2001; Fisher & al. 2002; personal observations). The genus has been inferred to have originated in Africa and subsequently dispersed to Madagascar and to Asia-Australasia (Chen & al. 2019). The latter dispersal event has been inferred to have occurred during the Middle Miocene via overland migration across Arabia. The majority of species diversity is in Asia-Australasia instead of Africa-Madagascar, with c. 75 species vs c. 30 species, respectively (Chen & al. 2018).

Although, as a genus, Artabotrys is easily recognizable, species delimitation and identification are somewhat problematic (e.g. Turner 2009; Turner & Utteridge 2015; Chen & al. 2018). In Thailand, there are 20 species of Artabotrys reported, two of which have recently been described (Chen & Eiadthong 2020). However, based on personal observations, identification of some specimens is still unsatisfactory due to the morphological heterogeneity of certain species, e.g. A. harmandii Finet & Gagnep., A. siamensis Miq. and A. spinosus. In the course of identifying specimens for the inclusion in a molecular phylogeny in order to solve some species complexes in Thai Artabotrys as part of the first author's M.Sc. study, we came across specimens from southwestern Thailand identified as A. multiflorus C. E. C. Fisch. These collections do not match the type specimen of A. multiflorus well. Therefore, in this study, we re-assess the taxonomic status of such specimens by detailed morphological comparisons. A multi-locus plastid phylogeny is also reconstructed, incorporating, among others, an accession of A. cf. multiflorus and multiple accessions of the above-mentioned three species. In addition, as mentioned earlier, certain species of Artabotrys exhibit thorns, a feature that is exceptional in the family. Several questions regarding this remarkable trait arise, e.g. did it evolve only once? Consequently, character evolutionary analyses are performed to shed light on the evolution of thorns in Artabotrys, with discussion on their putative advantages.

Material and methods

Phylogenetic reconstructions

The ingroup consisted of Xylopieae: 31 accessions of Artabotrys and two species of Xylopia L. On the basis of plastid DNA data, both genera have been consistently retrieved as sister genera with strong support (e.g. Chatrou & al. 2012; Guo & al. 2017), although this relationship was not supported based on some nuclear DNA data (Couvreur & al. 2019). Outgroups were members of Du-guetieae (a species of Letestudoxa Pellegr. plus a species of Pseudartabotrys Pellegr.). Six plastid DNA regions (matK, ndhF and rbcL exons; trnL intron; psbA-trnH and trnL-trnF intergenic spacers) were included. Sequences of 18 accessions were newly generated in the present study. Appendix 1 shows voucher information and GenBank accession numbers.

DNA extraction, amplification and sequencing, including primer sequences, used in the present study followed Chaowasku & al. (2018a, 2018b, 2020). Sequences obtained were edited using the Staden package (Staden & al. 2000) and then aligned using the Multiple Sequence Comparison by Log-Expectation (MUSCLE; Edgar 2004) implemented in MEGA7 (Kumar & al. 2016). The alignments were subsequently checked manually and adjusted where necessary based on the similarity criterion (Simmons 2004). In some accessions there was an inversion of 15-stretch nucleotides in the psbA-trnH intergenic spacer and this was complementarily reversed to be alignable to the remaining sequences, following Pirie & al. (2006). In total, 5484 nucleotide characters were included. Indel characters were not included because only a few non-autapomorphic indel structures were present. Alignments are available in the Supplemental content online ( https://doi.org/10.3372/wi.51.51106).

Parsimony analysis was performed in TNT version 1.5 (Goloboff & Catalano 2016). All characters were equally weighted and unordered. Incongruence among regions was assessed by analysing each region individually to see if there was any significant topological conflict (e.g. Wiens 1998). Multiple most parsimonious trees were generated by a heuristic search of the combined data, with 9000 replicates of random sequence addition, saving 10 trees per replicate, and using the tree bisection and reconnection (TBR) branch-swapping algorithm. Clade support was assessed by symmetric resampling (SR; Goloboff & al. 2003). A default change probability was used. Two hundred thousand replicates were run, each with four replicates of random sequence addition, saving four trees per replicate. A clade with SR ≥ 85%, 70–84%, or 50–69% was considered strongly, moderately, or weakly supported, respectively. Maximum likelihood analysis was carried out in IQ-TREE version 1.6.10 (Nguyen & al. 2015) under partition models (Chernomor & al. 2016) implemented with the “-spp” command, whereas Bayesian Markov chain Monte Carlo (MCMC; Yang & Rannala 1997) phylogenetic analysis was accomplished in MrBayes version 3.2.6 (Ronquist & al. 2012). Both analyses were run via the CIPRES Science Gateway version 3.3 (Miller & al. 2010). The data matrix was divided into five partitions based on the identity of DNA regions (the trnL intron and the adjacent trnL-trnF intergenic spacer were combined as a single partition). The most appropriate model of sequence evolution for each DNA partition was chosen by the Akaike Information Criterion (AIC; Akaike 1974) scores, using FindModel ( http://www.hiv.lanl.gov/content/sequence /findmodel/findmodel.html; Posada & Crandall 1998). The General Time Reversible (GTR; Tavaré 1986) nucleotide substitution model was selected for one partition (matK), whereas GTR with a gamma distribution for among-site rate variation (G) was selected for two partitions (ndhF and psbA-trnH). The Hasegawa-Kishino-Yano (HKY; Hasegawa & al. 1985) substitution model was selected for one partition (trnLF [= trnL intron + trnL-trnF intergenic spacer]), while HKY with G was selected for the remaining partition (rbcL). Clade support in the maximum likelihood analysis was measured by a non-parametric bootstrap resampling (BS; Felsenstein 1985) with 2000 replicates. Similar to the differentiation of the SR values in the parsimony analysis, a clade with BS ≥ 85%, 70–84%, or 50–69% was considered strongly, moderately, or weakly supported, respectively. In the Bayesian analysis, four independent analyses, each using four MCMC chains, were simultaneously run; each run was set for 10 million generations. The default prior settings were used except for the prior parameter of rate multiplier (“ratepr” [=variable]). The temperature parameter was set to 0.08. Trees and all parameter values were sampled every 1000th generation. Convergence was assessed by checking the standard deviation of split frequencies of the runs with values < 0.01 interpreted as indicative of a good convergence and by checking for adequate effective sample sizes (ESS > 200) using Tracer version 1.6 (Rambaut & al. 2013). The first 25% of all trees sampled were discarded as burn-in and the 50% majority-rule consensus tree was created from the remaining trees. A clade with posterior probabilities (PP) ≥ 0.95, 0.9–0.94, or 0.5–0.89 was considered strongly supported, weakly supported, or unsupported, respectively.

Ancestral character-state reconstructions of thorn occurrence in Artabotrys

The presence/absence of thorns in all accessions included was surveyed from literature (Blume 1830; Bentham 1861; Oliver 1868; Hooker & Thomson 1872; King 1892; Diels 1915, 1931; Pellegrin 1920; Craib 1925; Le Thomas 1969; Posluszny & Fisher 2000; Chalermglin 2001; Nurainas 2004; Jessup 2007; Li & al. 2011; Chen & Eiadthong 2020), from specimen labels and/or from personal observations in the field. Ten thousand post burn-in trees (2500 from each run) from the Bayesian analysis were used as input trees for parsimony and maximum likelihood ancestral character-state reconstructions in Mesquite version 3.6 (Maddison & Maddison 2018). Character state changes were treated as unordered. The “Mk1” model was adopted for the maximum likelihood ancestral character-state reconstructions, with default model settings. The “trace over trees” option was chosen and reconstructions across the input trees were summarized at each node of the Bayesian 50% majority-rule consensus tree using the “uniquely best state” option.

Morphology

The morphological data of Artabotrys multiflorus for comparison were derived from Fischer (1937) and study of the type specimen. Two gatherings of A. cf. multiflorus from southwestern Thailand (Keßler PK 3227 [B, BKF, CMUB, L] and Aongyong 16 [CMUB]) were studied morphologically (herbarium codes according to Index herbariorum;  http://sweetgum.nybg.org/science/ih/). Aongyong 16 is a voucher for molecular phylogenetic analyses and, although sterile, can be identified as the same taxon as Keßler PK 3227 because both gatherings have coriaceous leaves and both were collected ± 3 km apart at the same elevation. The indumentum terminology used followed Hewson (1988). The abbreviation “c.” (circa) was added when there was a single observation/measurement. The term “almost glabrous” means “with fewer than ten hairs”.

Results

The parsimony analysis resulted in 21 most parsimonious trees with 759 steps. The consistency and retention indices (CI and RI) were both 0.89. There was no strong topological conflict (SR ≥ 85%) in the analyses of each plastid region. The ingroup monophyly was maximally supported as shown in Fig. 1. Artabotrys and Xylopia were each recovered as a maximally supported sister clades. In the former genus, a maximally supported clade composed of two accessions of A. thomsonii Oliv., both from Africa, was retrieved as the sister group of a large maximally supported clade consisting of the remaining accessions of Artabotrys. In this large clade, there were two strongly supported sister clades: a clade of A. pierreanus Engl. & Diels and A. stolzii Diels (PP 1, BS 87%, SR 91%), both from Africa, and a clade containing the rest of the genus from Asia-Australasia (PP 1, BS 99%, SR 99%). The relationships in this Asian-Australasian clade were largely unresolved. There was a moderately to strongly supported clade (PP 1, BS 80%, SR 81%) comprising thorn-bearing species: A. carnosipetalus Jessup, A. harmandii (four accessions), A. hexapetalus (L. f.) Bhandari (two accessions), A. oblanceolatus Craib, A. siamensis (two accessions) and A. spinosus (four accessions). There were two strongly supported clades of A. harmandii (A. harmandii-1 + A. harmandii-2 [PP 1, BS 98%, SR 98%] and A. harmandii-3 + A. harmandii-4 [PP 1, BS 94%, SR 96%]) and of A. spinosus (A. spinosus-1 from Mun River + A. spinosus-2 from Chi River [PP 1, BS 99%, SR 99%] and A. spinosus-3 + A. spinosus-4 [PP 1, BS 100%, SR 99%], both from the Mekong River). The two clades of A. harmandii did not show sister relationships, nor did the two clades of A. spinosus. Two accessions of A. siamensis also did not form a clade. Outside the thorn-bearing clade, A. cf. multiflorus was retrieved as the sister group of a strongly supported clade (PP 1, BS 100%, SR 99%) composed of A. uniflorus (Griff.) Craib and Artabotrys sp. 1 THA with weak to strong support (PP 1, BS 60%, SR 59%).

Fig. 1.

Phylogram from Bayesian inference, showing relationships within Artabotrys. Bayesian posterior probabilities (PP), maximum likelihood bootstrap values (BS) and parsimony symmetric resampling values (SR) are indicated: PP/BS/SR. ** = BS and/or SR < 50%. Scale bar unit = substitutions per site. AUST. = Australasia.

img-z4-1_69.jpg

In Artabotrys, the occurrence of thorns was inferred to have evolved once in the thorn-bearing clade (Fig. 2). The character state “thorns present” was reconstructed at the crown node of the thorn-bearing clade in all 10 000 input trees under the parsimony criterion. Under the maximum likelihood approach it was reconstructed in 9833 trees, while the remaining 167 trees were equivocally reconstructed.

Fig. 2.

Maximum likelihood and parsimony ancestral character-state reconstructions of thorn occurrence in Artabotrys across 10000 post burn-in trees from Bayesian phylogenetic inference shown on Bayesian 50% majority-rule consensus tree.

img-z5-1_69.jpg

Discussion

A new species of Artabotrys from Thailand

Artabotrys cf. multiflorus is somewhat poorly supported as the sister species of a strongly supported clade composed of A. uniflorus and Artabotrys sp. 1 THA (Fig. 1). However, A. uniflorus and Artabotrys sp. 1 THA possess only one flower per hook with rather thick and fleshy petals (personal observations), whereas each hook of A. cf. multiflorus bears more or less five flowers exhibiting thin and rather chartaceous petals (Fig. 3). Upon a closer comparison with the type specimen (Fig. 4) and protologue (Fischer 1937) of A. multiflorus, A. cf. multiflorus differs in several respects (Table 1), i.e. number of flowers per hook (Fig. 3, 4), petal shape, length, width and apex (Fig. 4, 5A, 5B) and number of carpels per flower. In addition, the elevation where A. cf. multiflorus (c. 510 m) and A. multiflorus (c. 914 m) occur is also considerably different. The exact locality of A. multiflorus cannot be traced, but it is expected to be somewhere in the Burmese Dawna range (Fischer 1937 [as “Dawnas”]), northwest of the locality of A. cf. multiflorus (Kanchanaburi Province, Thailand). On the basis of these differences, A. cf. multiflorus is described here as new to science. As a consequence, A. multiflorus is most likely to be absent from the flora of Thailand.

Artabotrys angustipetalus Photikwan & Chaowasku, sp. nov.Fig. 3, 5.

Holotype: Thailand, Kanchanaburi Province, Thung Yai Naresuan Wildlife Sanctuary, 17 Feb 2002 [in flower], Keßler PK 3227 (BKF! [SN144809]; isotypes: B!, BKF!, CMUB!, L! [L.1749583, L.1749584]).

DiagnosisArtabotrys angustipetalus is morphologically close to A. multiflorus C. E. C. Fisch. The former differs primarily from the latter by having more or less five flowers (vs > 12) per hook, linear (vs oblong to oblong-lanceolate) petals, acute (vs obtuse) petal apex, longer and narrower petals and fewer carpels per flower.

Description — Woody climbers to 30 m long, c. 10 cm in diam.; young twigs almost glabrous; petiole 4–7 mm long, grooved on upper surface, almost glabrous on both surfaces; leaf blade coriaceous, 10.7–14.2 × 4.8–7.7 cm, elliptic, sometimes ± obovate, glabrous on both surfaces including secondary veins, apex cuspidateacute, base cuneate; midrib slightly raised and glabrous on upper surface, raised and glabrous on lower surface; secondary veins 10–12 per side, angle with midrib 65°–80° (at middle part of leaf blade). Inflorescences terminal developing to ± leaf-opposed; flowering peduncle and inflorescence axis hook-shaped, first curve 17–27 mm long, 3–4 mm wide (at midpoint of curve), second curve 7–10 mm long, 2–2.3 mm wide (at midpoint of curve), both curves puberulous with appressed hairs, bearing ± 5 flowers per hook, divided into 1 or 2 fascicles, with several bracts at base of each fascicle, ± ovate; flowering pedicel 12–18 mm long, puberulous with appressed hairs. Sepals free, 2–2.5 × 2–2.5 mm, broadly ovate, apex acute-acuminate, sometimes slightly obtuse, outside and margin puberulous with appressed hairs, inside glabrous. Outer petals 29–30 × c. 3 mm, linear, apex acute, divided into a blade and a claw, claw c. 3.8 mm long, upper rim of claw slightly raised and curved, outside of outer petals puberulous with appressed hairs on blade, more densely so on claw, margin puberulous with appressed to erect hairs, inside puberulous with appressed hairs on blade, claw glabrous, but upper rim of claw tomentose with erect hairs; inner petals 30–31 × 2–2.5 mm, linear, apex acute, divided into a blade and a claw, claw c. 3.5 mm long, upper rim of claw distinctly raised and curved, covering stamens and carpels, outside of inner petals puberulous with appressed hairs on blade, but tomentose with erect hairs on claw (c. ⅔ of claw length from upper rim), remaining area of claw puberulous with appressed hairs, margin puberulous with appressed to erect hairs, inside puberulous with appressed hairs on blade, claw glabrous, but upper rim of claw tomentose with erect hairs. Torus c. 1 × 2 mm, slightly elevated, apex flat-topped, tomentose-villous with erect hairs on areas unoccupied by stamens and carpels. Stamens 25–32 per flower, 1.1–1.2 mm long, connective apex ± truncate, covering thecae. Carpels 7 or 8 per flower, 1.1–1.4 mm long; stigmas terete and curved; ovaries glabrous; ovules 2 per ovary, basal. Fruit unknown.

Phenology — Flowering material collected in February.

Distribution and ecology — Kanchanaburi Province, SW Thailand; occurring in primary evergreen forests at an elevation of c. 510 m.

Field notes — Bark blackish; flowers with very sweet fruity smell, petals greenish yellow.

Table 1.

Main morphological differences between Artabotrys angustipetalus and A. multiflorus.

img-z6-14_69.gif

Fig. 3.

Holotype of Artabotrys angustipetalus Photikwan & Chaowasku – Keßler PK 3227 (BKF [SN144809]).

img-z7-1_69.jpg

Fig. 4.

Isotype of Artabotrys multiflorus C. E. C. Fisch. – Parkinson 5220 (E [E00393106]).

img-z8-1_69.jpg

Fig. 5.

Flowering organs of Artabotrys angustipetalus. – A: abaxial side of outer petal (left), adaxial side of outer petal (right); B: abaxial side of inner petal (left), adaxial side of inner petal (right); C: adaxial side of outer petal claw; D: adaxial side of inner petal claw; E: adaxial side of stamen (left), abaxial side of stamen (right); F: view from above showing sepals; G: carpel.

img-z9-1_69.jpg

Conservation status — DD (Data Deficient) according to IUCN (2012) because this species is known from only two collections. Further explorations are required before an assessment can be made.

Additional specimen examined (paratype) — Thailand: Kanchanaburi Province, Thongphaphum District, Phuye, without date [sterile], Aongyong 16 (CMUB).

Evolution of thorns in Artabotrys

The occurrence of thorns in Annonaceae is exceptional. Besides certain species of Artabotrys, thorns are also present in a few species of Annona L. (H. Rainer, personal communication; e.g. A. spinescens Mart., personal observations on a specimen at P [P01984538]), which belongs to the tribe An-noneae of the subfamily Annonoideae (Chatrou & al. 2012). Based on the ancestral character-state reconstructions of thorn occurrence in Artabotrys, this trait is inferred to have evolved only once as a synapomorphy of the thorn-bearing clade (Fig. 2), which is equivalent to clade D2 in Chen & al. (2019). Three species of Artabotrys that are absent in our analyses, A. brevipes Craib, A. manoranjanii M. V. Ramana & al. and A. pleurocarpus Maingay ex Hook. f. & Thomson, also possess thorns according to Insura (2009), Ramana & al. (2016) and personal observations. According to Insura (2009), at least one additional species, A. vanprukii Craib, endemic to Thailand, also exhibits thorns. The synapomorphic thorn occurrence is systematically powerful in elucidating coarse phylogenetic placements of Asian-Australasian species of Artabotrys, i.e. species with thorns are (or will be) members of the thorn-bearing clade, whereas those without thorns are (or will be) recovered outside the thorn-bearing clade. This is clearly exemplified in the new species A. angustipetalus, which does not possess thorns and has been recovered outside the thorn-bearing clade (Fig. 1, 2). Observations in living plants reveal that thorns generally emerge in pairs and are generally found along the lower part of stems (Fig. 6A). In some species, e.g. A. spinosus, these thorns can appear on the upper part of stems as well, even on young orthotropic branches (personal observations). According to Posluszny & Fisher (2000), these thorns represent plagiotropic branches that do not develop further. We have observed the development of thorns in a sapling and noticed that a thorn emerged rather soon, i.e. as a second plagiotropic branch at a height of only c. 25 cm (Fig. 6B). One of the possible functions of thorns is herbivore protection, especially from larger vertebrate animals (Grubb 1992; Ronel & Lev-Yadun 2012; Nascimento & al. 2020). Additionally, as demonstrated by Fisher & al. (2002), light plays an important role for thorn development in A. hexapetalus, i.e. the more shaded the areas, the more thorns are developed. It seems that there is more driving force for plants in shaded areas to grow orthotropic branches up above to reach light and find support from other plants. Therefore, the growth of the less necessary plagiotropic branches is possibly minimized by developing more thorns instead. The orthotropic branches of the thorn-bearing species of Artabotrys can grow very fast and at some point after they reach other plants, fewer thorns but more plagiotropic branches with hooks are developed (personal observations). Regarding thorns in a few species of Annona, mentioned above, further ontogenetic study is indispensable to ascertain if they are homologous with thorns in Artabotrys species because the branching architecture of Annona is distichous, without the distinction between orthotropic and plagiotropic branches, whereas the branching architecture of Artabotrys is spiral, with the distinction between orthotropic and plagiotropic branches (Johnson 2003).

Fig. 6.

Thorns of Artabotrys species. – A: pairs of thorns at lower part of stems of A. siamensis [= A. siamensis-1]; B: thorn as a second plagiotropic branch of a sapling of Artabotrys sp.

img-z10-1_69.jpg

Three species in the thorn-bearing clade, Artabotrys harmandii, A. siamensis and A. spinosus, each appear to be non-monophyletic (Fig. 1). There are some morphological differences (e.g. leaf and/or petal shape) between two lineages/clades of each species; however, we believe that more resolved phylogenetic hypotheses incorporating more DNA sequences, particularly nuclear DNA markers via baiting (e.g. Couvreur & al. 2019; Brée & al. 2020), are required before any solid taxonomic conclusion on these species can be drawn.

Acknowledgements

We are grateful to the curators of the herbaria B, BKF, CMUB, E, L and P for the material studied. Kithisak Aongyong, Vittaya Kaewjaroay, Aimorn Rodphitak and Saksan Kaitongsuk provided useful material for molecular phylogenetic analyses. Torsakul Nawanin scanned the holotype of Artabotrys angustipetalus. The first author is indebted to the scholarship project for the promotion of science and mathematics talented teachers (PSMT) for supporting the M.Sc. study at Chiang Mai University. The last author thanks the Thailand Science Research and Innovation (TSRI) for the research grant. Partial financial support for this study was from Chiang Mai University. Heimo Rainer is kindly thanked for providing the information on Annona species having thorns. Thomas Couvreur and an anonymous reviewer considerably improved an earlier draft of this article.

References

1.

Akaike H. 1974: A new look at the statistical model identification. –  IEEE Trans. Automat. Contr. 19: 716–723. Google Scholar

2.

Bentham G. 1861:  Anonaceae. – Pp. 9–11 in: Flora hongkongensis: a description of the flowering plants and ferns of the island of Hongkong. – London: L. Reeve. Google Scholar

3.

Blume C. L. 1830: Anonaceae. – In: Flora Javae nec non insularum adjacentium. – Bruxellis: J. Frank. Google Scholar

4.

Brée B., Helmstetter A. J., Bethune K., Ghogue J. P., Sonké B. & Couvreur T. L. P. 2020: Diversification of African rainforest restricted clades: Piptostigmateae and Annickieae (Annonaceae). –  Diversity 12: article 227. Google Scholar

5.

Chalermglin P. 2001: Family Annonaceae [in Thai]. – Bangkok: Ban and Suan. Google Scholar

6.

Chaowasku T., Aongyong K., Damthongdee A., Jongsook H. & Johnson D. M. 2020: Generic status of Winitia (Annonaceae, Miliuseae) reaffirmed by molecular phylogenetic analysis, including a new species and a new combination from Thailand. –  Eur. J. Taxon. 659: 1–23. Google Scholar

7.

Chaowasku T., Damthongdee A., Jongsook H., Ngo D. T., Le H. T., Tran D. M. & Suddee S. 2018a: Enlarging the monotypic Monocarpieae (Annonaceae, Malme-oideae): recognition of a second genus from Vietnam informed by morphology and molecular phylogenetics. –  Candollea 73: 261–275. Google Scholar

8.

Chaowasku T., Damthongdee A., Jongsook H., Nuraliev M. S., Ngo D. T., Le H. T., Lithanatudom P., Osathanunkul M., Deroin T., Xue B. & Wipasa J. 2018b: Genus Huberantha (Annonaceae) revisited: erection of Polyalthiopsis, a new genus for H. floribunda, with a new combination H. luensis. –  Ann. Bot. Fenn. 55: 121–136. Google Scholar

9.

Chatrou L. W., Pirie M. D., Erkens R. H. J., Couvreur T. L. P., Neubig K. M., Abbott J. R., Mols J. B., Maas J. W., Saunders R. M. K & Chase M. W. 2012: A new subfamilial and tribal classification of the pantropical flowering plant family Annonaceae informed by molecular phylogenetics. –  Bot. J. Linn. Soc. 169: 5–40. Google Scholar

10.

Chen J., Chalermglin P. & Saunders R. M. K. 2018: Two new species and two new records of Artabotrys (Annonaceae) from Thailand. –  PhytoKeys 95: 71–81. Google Scholar

11.

Chen J. & Eiadthong W. 2020: New species and new records of Artabotrys (Annonaceae) from peninsular Thailand. –  PhytoKeys 151: 67–81. Google Scholar

12.

Chen J., Thomas D. C. & Saunders R. M. K. 2019: Geographic range and habitat reconstructions shed light on palaeotropical intercontinental disjunction and regional diversification patterns in Artabotrys (Annonaceae). –  J. Biogeogr. 46: 2690–2705. Google Scholar

13.

Chernomor O., von Haeseler A. & Minh B. Q. 2016: Terrace aware data structure for phylogenomic inference from supermatrices. –  Syst. Biol. 65: 997–1008. Google Scholar

14.

Couvreur T. L. P., Helmstetter A. J., Koenen E. J. M., Bethune K., Brandão R. D., Little S. A., Sauquet H. & Erkens R. H. J. 2019: Phylogenomics of the major tropical plant family Annonaceae using targeted enrichment of nuclear genes. –  Frontiers Pl. Sci. 9: article 1941. Google Scholar

15.

Craib W. G. 1925: Contributions to the flora of Siam. Additamentum XV. –  Bull. Misc. Inform. Kew 1925: 7–23. Google Scholar

16.

Diels L. 1915: Anonaceae africanae. III. –  Bot. Jahrb. Syst. 53: 434–448. Google Scholar

17.

Diels L. 1931: Anonaceae novae. –  Notizbl. Bot. Gart. Berlin-Dahlem 11: 73–86. Google Scholar

18.

Edgar R. C. 2004: MUSCLE: multiple sequence alignment with high accuracy and high throughput. –  Nucleic Acids Res. 32: 1792–1797. Google Scholar

19.

Felsenstein J. 1985: Confidence limits on phylogenies: an approach using the bootstrap. –  Evolution 39: 783–791. Google Scholar

20.

Fischer C. E. C. 1937: Contributions to the flora of Burma: XIII. –  Bull. Misc. Inform. Kew 1937: 436–440. Google Scholar

21.

Fisher J. B., Posluszny U. & Lee D. W. 2002: Shade promotes thorn development in a tropical liana, Artabotrys hexapetalus (Annonaceae). –  Int. J. Pl. Sci. 163: 295–300. Google Scholar

22.

Goloboff P. A. & Catalano S. A. 2016: TNT version 1.5, including a full implementation of phylogenetic morphometrics. –  Cladistics 32: 221–238. Google Scholar

23.

Goloboff P. A., Farris J. S., Källersjö M., Oxelman B., Ramírez M. J. & Szumik C. A. 2003: Improvements to resampling measures of group support. –  Cladistics 19: 324–332. Google Scholar

24.

Grubb P. J. 1992: A positive distrust in simplicity – lessons from plant defences and from competition among plants and among animals. –  J. Ecol. 80: 585–610. Google Scholar

25.

Guo X., Tang C. C., Thomas D. C., Couvreur T. L. P. & Saunders R. M. K. 2017: A mega-phylogeny of the Annonaceae: taxonomic placement of five enigmatic genera and support for a new tribe, Phoenicantheae. –  Sci. Rep. 7: article 7323. Google Scholar

26.

Hasegawa M., Kishino H. & Yano T. 1985: Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. –  J. Molec. Evol. 22: 160–174. Google Scholar

27.

Hewson H. J. 1988: Plant indumentum. A handbook of terminology [Australian Flora and Fauna Series 9]. – Canberra: Australian Government Publishing Service. Google Scholar

28.

Hooker J. D. & Thomson T. 1872:  Anonaceae. – Pp. 45–94 in: Hooker J. D. (ed.), The flora of British India 1. – London: L. Reeve & Co. Google Scholar

29.

Insura T. 2009: Systematics and some ecological characteristics of Artabotrys R. Br. (Annonaceae) in Thailand [in Thai with English abstract]. – Bangkok: M.Sc. thesis, Kasetsart University. Google Scholar

30.

IUCN. 2012:  IUCN Red List categories and criteria: version 3.1, ed. 2. – Gland & Cambridge: IUCN. Google Scholar

31.

Jessup L. W. 2007: Annonaceae. – Pp. 18–57 in: Wilson J. G. (ed.), Flora of Australia 2. – Canberra: CSIRO Publishing. Google Scholar

32.

Johnson D. M. 2003: Phylogenetic significance of spiral and distichous architecture in the Annonaceae. – Syst. Bot. 28: 503–511. Google Scholar

33.

Keßler P. J. A. 1993: Annonaceae. – Pp. 93–129 in: Kubitzki K., Rohwer J. G. & Bittrich V. (ed.), The families and genera of vascular plants 2. – Berlin: Springer Verlag. Google Scholar

34.

King G. 1892: Materials for a flora of the Malayan Peninsula, no. 4. –  J. Asiat. Soc. Bengal, pt. 2, Nat. Hist. 61: 1–130. Google Scholar

35.

Kumar S., Stecher G. & Tamura K. 2016: MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. –  Molec. Biol. Evol. 33: 1870–1874. Google Scholar

36.

Le Thomas A. 1969: Annonaceae. – Pp. 1–371 in: Aubreville A. (ed.), Flore du Gabon 16. – Paris: Muséum national d'Histoire naturelle. Google Scholar

37.

Li B. T. & Gilbert M. G. 2011: Artabotrys. – Pp. 701–703 in: Wu Z. Y., Raven P. H. & Hong D. Y. (ed.),  Flora of China 19 (Cucurbitaceae through Valerianaceae, with Annonaceae and Berberidaceae). – Beijing: Science Press; St. Louis: Missouri Botanical Garden Press. Google Scholar

38.

Maddison W. P. & Maddison D. R. 2018: Mesquite: a modular system for evolutionary analysis, version 3.6. – Published at  http://www.mesquiteproject.org/ [accessed 26 Sep 2019]. Google Scholar

39.

Miller M. A., Pfeiffer W. & Schwartz T. 2010:  Creating the CIPRES Science Gateway for inference of large phylogenetic trees. – Pp. 45–52 in: Gateway Computing Environments Workshop (GCE). – Piscataway: IEEE. Google Scholar

40.

Nascimento L. F. D., Guimarães P. R., Onstein R. E., Kissling W. D. & Pires M. M. 2020: Associated evolution of fruit size, fruit colour and spines in neotropical palms. –  J. Evol. Biol. 33: 858–868. Google Scholar

41.

Nguyen L. T., Schmidt H. A., von Haeseler A. & Minh B. Q. 2015: IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. –  Molec. Biol. Evol. 32: 268–274. Google Scholar

42.

Nurainas 2004: Artabotrys (Annonaceae) in Sumatra. – Floribunda 2: 117–127. Google Scholar

43.

Oliver, D. 1868.  Order III. Anonaceae. – Pp. 13–39 in: Flora of Tropical Africa 1, Ranunculaceae to Conna-raceae. – London: L. Reeve & Co. Google Scholar

44.

Pellegrin M. F. 1920: Plantae Letestuanae novae ou plantes nouvelles récoltées par M. Le Testu de 1907 à 1919 dans le Mayombe congolais. –  Bull. Mus. Natl. Hist. Nat. 26: 654–659. Google Scholar

45.

Pirie M. D., Chatrou L. W., Mols J. B., Erkens R. H. J. & Oosterhof J. 2006: ‘Andean-centred’ genera in the short-branch clade of Annonaceae: testing biogeographical hypotheses using phylogeny reconstruction and molecular dating. –  J. Biogeogr. 33: 31–46. Google Scholar

46.

Posada D. & Crandall K. A. 1998: MODELTEST: testing the model of DNA substitution. –  Bioinformatics 14: 817–818. Google Scholar

47.

Posluszny U. & Fisher J. B. 2000: Thorn and hook ontogeny in Artabotrys hexapetalus (Annonaceae). –  Amer. J. Bot. 87: 1561–1570. Google Scholar

48.

Ramana M. V., Swamy J. & Chandramohan K. 2016: Artabotrys manoranjanii sp. nov. (Annonaceae) from the Andaman Islands, India. –  Nordic J. Bot. 34: 413–415. Google Scholar

49.

Rambaut A., Suchard M. & Drummond A. 2013: Tracer, version 1.6. – Published at  http://tree.bio.ed.ac.uk/software/tracer/ [accessed 18 May 2017]. Google Scholar

50.

Ronel M. & Lev-Yadun S. 2012: The spiny, thorny and prickly plants in the flora of Israel. –  Bot. J. Linn. Soc. 168: 344–352. Google Scholar

51.

Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Höhna S., Larget B., Liu L., Suchard M. A. & Huelsenbeck J. P. 2012: MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. –  Syst. Biol. 61: 539–542. Google Scholar

52.

Saunders R. M. K., Guo X. & Tang C. C. 2020: Friesodielsia subaequalis (Annonaceae): a new nomenclatural combination following conservation of the generic name against Schefferomitra. –  Phytotaxa 464: 183–184. Google Scholar

53.

Simmons M. P. 2004: Independence of alignment and tree search. –  Molec. Phylogen. Evol. 31: 874–879. Google Scholar

54.

Staden R., Beal K. F. & Bonfield J. K. 2000:  The Staden Package, 1998. – Pp. 115–130 in: Misener S. & Krawetz S. A. (ed.), Bioinformatics methods and protocols. – Meth. Molec. Biol. 132. – Totowa: Humana Press. Google Scholar

55.

Tavaré S. 1986: Some probabilistic and statistical problems in the analysis of DNA sequences. – Lectures Math. Life Sci. 17: 57–86. Google Scholar

56.

Turner I. M. 2009: Artabotrys (Annonaceae) in Borneo: new species and new synonyms. – Fol. Malaysiana 10: 59–88. Google Scholar

57.

Turner I. M. 2018: Annonaceae of the Asia-Pacific region: names, types and distributions. –  Gard. Bull. Singapore 70: 409–744. Google Scholar

58.

Turner I. M. & Utteridge T. M. A. 2015: Artabotrys byrsophyllus and A. tipuliferus spp. nov. (Annonaceae) from Peninsular Malaysia and Thailand. –  Nordic J. Bot. 33: 562–566. Google Scholar

59.

Wiens J. J. 1998: Combining data sets with different phylogenetic histories. –  Syst. Biol. 47: 568–581. Google Scholar

60.

Xue B., Tan Y. H., Thomas D. C., Chaowasku T., Hou X. L. & Saunders R. M. K. 2018: A new Annonaceae genus, Wuodendron, provides support for a post-boreotropical origin of the Asian-neotropical disjunction in the tribe Miliuseae. –  Taxon 67: 250–266. Google Scholar

61.

Yang Z. & Rannala B. 1997: Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. –  Molec. Biol. Evol. 14: 717–724. Google Scholar

Appendices

Appendix 1

Specimens for molecular phylogenetic analyses and their GenBank accession numbers. Unavailable sequences are denoted with —, whereas newly generated sequences are denoted with **.

img-A2c6_69.gif

Continued

img-Akza_69.gif
© 2021 The Authors · This open-access article is distributed under the CC BY 4.0 licence
Ekkaphon Photikwan, Anissara Damthongdee, Hathaichanok Jongsook, and Tanawat Chaowasku "Artabotrys angustipetalus (Annonaceae), a new species from Thailand, including a plastid phylogeny and character evolutionary analyses of thorn occurrence in Artabotrys," Willdenowia 51(1), 69-82, (23 March 2021). https://doi.org/10.3372/wi.51.51106
Received: 18 May 2020; Accepted: 12 October 2020; Published: 23 March 2021
JOURNAL ARTICLE
14 PAGES


Share
SHARE
KEYWORDS
Annonaceae
Artabotrys
evolution
new species
systematics
taxonomy
Thailand
RIGHTS & PERMISSIONS
Get copyright permission
Back to Top