Helonias, Tanaka, 2019

Tanaka, Noriyuki, 2019, Taxonomy, evolution and phylogeography of the genus Helonias (Melanthiaceae) revisited, Phytotaxa 390 (1), pp. 448-450 : 448-450

12. Helonias breviscapa (Maxim.) Tanaka (1998a: 111) ( Figs. 27 , 28 ).

≡ Heloniopsis breviscapa Maximowicz (1867: 436) . ≡ Heloniopsis japonica (Thunb.) Maxim. var. breviscapa (Maxim.) Honda (1938: 1678) . ≡ Hexonix breviscapa (Maxim.) Wang & Tang (1949: 113) . ≡ Heloniopsis orientalis (Thunb.) Tanaka var. breviscapa (Maxim.) Ohwi (July 1953 b: 68). ≡ Heloniopsis orientalis (Thunb.) Tanaka subsp. breviscapa (Maxim.) Kitamura & Murata (1966: 72) . Type (lectotype, designated here):― JAPAN. Kiusiu, in m. ignivomo Wunzen [Kyûshû, Nagasaki Pref., Mt. Unzen], medio Majo, 1863, C.J. Maximowicz s.n. (K-000901111*!). Isolectotypes: NY-00319713*–5*!, P-00730557*–9*!, US-00650432*!

=? Scilla japonica Thunberg (in Murray 1784 May–June: 329; August 1784: 137; 1802: t. 4). ≡ Hexonix japonica (Thunb.) Rafinesque (1837: 13) . Type:― JAPAN. Thunberg (Holotype: UPS-THUNB 8323*!). Japanese name:―Kochô (‘Kotjo’ in Thunberg 1784); Shôjôbakama ( Itô 1829, Iinuma 1861).

= Sugerokia nipponica Ohwi (1930: 566) . ≡ Heloniopsis nipponica (Ohwi) Nemoto (1936: 1058) . Type:― JAPAN. Honshû. Prov. Yamato [Nara Pref.], Yoshino, between Kashiwagi and Obagamine, 19 May 1928, J. Ohwi (Holotype: KYO, photograph in TNS!). Japanese name:―Yamato-shôjôbakama ( Nemoto 1936); Shirobana-shôjôbakama ( Hiyama 1939: 79).

= Heloniopsis japonica (Thunb.) Maxim. var. flavida Nakai (1933: 243) . Japanese name:―Kibana-shôjôbakama ( Nakai 1933). ≡ Heloniopsis breviscapa Maxim. var. flavida (Nakai) Hara (1947: 149) . ≡ Hexonix breviscapa (Maxim.) F.T.Wang & Tang var. flavida (Nakai) Wang & Tang (1949: 113) . ≡ Heloniopsis orientalis (Thunb.) Tanaka var. flavida (Nakai) Ohwi (July 1953 b: 68. Type:― JAPAN. Honshû. Prov. Yamato [Nara Pref.]. Not designated. – Heloniopsis japonica (Thunb.) Maxim. var. grandiflora (Franch. & Sav.) Nakai (1933: 243) , p.p., excl. syn.

= Heloniopsis japonica Maxim. var. yakusimensis Masamune (1934: 551) . Japanese name:―Hime-shôjôbakama ( Masamune 1934). ≡ Heloniopsis yakusimensis (Masam.) Honda (1938: 1679) . ≡ Sugerokia yakusimensis (Masam.) Koidzumi (1939: 53) . ≡ Heloniopsis breviscapa Maxim. var. yakusimensis (Masam.) Hara (1947: 148) . ≡ Hexonix breviscapa (Maxim.) F.T.Wang & Tang var. yakusimensis (Masam.) Wang & Tang (1949: 113) . ≡ Heloniopsis orientalis (Thunb.) Tanaka var. yakusimensis (Masam.) Ohwi (July 1953 b: 68). ≡ Heloniopsis yakusimensis (Masam.) Masamune (1969: 11) , isonym. Type:― JAPAN. Kyûshû. Kagoshima Pref.: Isl. Yakushima, ca. 1500 m, G. Masamune (from the protologue). The following specimen is possibly holotype, as it coincides well with the original description: Isl. Yakushima, 6 April 1927, G. Masamune (TI!).

= Heloniopsis japonica (Thunb.) Maxim. var. albiflora Honda (1938: 1678) . ≡ Heloniopsis breviscapa Maxim. var. albiflora (Honda) Hara (1947: 149) . Type:― JAPAN. Honshû. Prov. Musasi [Tokyo Pref.], Sekido, [3 April] 1938, T. Sakai s.n. (Holotype: TI!). Paratypes cited in the additional specimens examined below. Japanese name:―Sirobana-shôjôbakama ( Honda 1938).

= Heloniopsis japonica (Thunb.) Maxim. var. tesselata Nakai ex Honda (1938: 1679) . Type:― JAPAN. Honshû. Prov. Awa [Chiba Pref.], Mt. Kiyozumi, April 1937, T. Nakai s.n. (Holotype: TI!). Japanese name:―Kiyozumi-shôjôbakama ( Honda 1938).

– Heloniopsis pauciflora auct. non A.Gray: Miquel (1867: 146), as to specimens from Kiusiu by Maximowicz, ‘ Helionopsis ’.

– Sugerokia japonica Miquel (1870: 52) , p.p., as to synonyms? Scilla japonica , Heloniopsis breviscapa Maxim. , and specimens from Mt. Wunzen, Kiusiu [distributed under the name Heloniopsis pauciflora by Maximowicz with the date of 1865].

– Heloniopsis japonica auct. non Maxim.: Matsumura (1905: 197), p.p.; Honda (1938: 1677), p.p.

– Sugerokia japonica auct. non Miquel: Koidzumi (1930: 95).

Japanese name:―Kochô-shôjôbakama (Tanaka 1998, based on ‘Kojyo’ for Scilla japonica in Thunberg 1784: 137), Shirobana-shôjôbakama (e.g. Iwasaki 1824; Makino 1891, under Heloniopsis japonica Maxim. , p.p.?; Koidzumi 1930), Tsukushi-shôjôbakama ( Honda 1938), Yakushima-shôjôbakama ( Honda 1938).

Description:―Rhizome cylindrical, subannulate with many close scars, to 5 cm long, to 1.5 cm in diam., pale brown. Roots filiform, to 1.5 mm in diam., white, some showing signs of contraction. Leaves hysteranthous, main fresh rosette leaves 7–15, persistent usually for fully 1 year (sometimes for ca. 2 years), spatulate or narrowly oblanceolate, 3.5–21.5 cm long, to 3.5 cm wide, often minutely undulate at margin, apex with apiculus 0.5–1 mm long, light (often yellowish) green, chartaceous (thin to moderately thick in texture), young fresh leaves somewhat glossy, mature leaves almost dull. Stem usually ca. 2–17 cm long at anthesis, becoming elongate toward fruiting stage; peduncle to 37 cm long in fruit; scale-like leaves 5–11 (excl. basal ones), linear-lanceolate, narrowly lanceolate, narrowly elliptic-oblong, to ca. 3.8 cm long, apex acute or acuminate; inflorescence compactly racemose or sub-umbellate, rachis to 1.7 cm long at anthesis, to 8 cm long in fruit; pedicels terete, 2–7 mm long at anthesis, to 23 mm long in fruit, 6-ribbed, ebracteate. Flowers 1–11, usually nodding at mid anthesis, funnelform, 1–1.9 cm across, scent or odorless. Tepals 6, obconically expanded, sometimes slightly recurved distally, 5–7(–9)-veined, white, often tinged (purplish) pink proximally, turning creamy yellow or sometimes pink with progression of anthesis, eventually green after anthesis, (oblong-)oblanceolate or spatulate, 8.3–14 mm long, 1.8–5.2 mm wide, apex rounded to subacute; abaxial basal part scarcely to moderately gibbous; adaxially shallowly to moderately cannaliculate toward base, proximal submarginal portions winged (lamellate) inward; wings extending over proximal ca. 1/4 of tepal, connate proximally to those of adjoining tepals for 0.25–1 mm in height, and also adnate to opposite filament for 0.7–1.8 mm in height, forming a sheathing nectary; surface of the nectary positioned nearly as high as base of ovary (or top of receptacle); base of tepal affixed to receptacle (apex of pedicel) for ca. 1.5 mm in length. Stamens 6, equaling or exceeding tepals; filaments filiform, 5–12.5(–15) mm long, 0.4–0.6 mm wide, nearly straight, scarcely dilated but slightly complanate toward base, white or pale purplish pink; anthers affixed to filament on adaxial portion close to base of connective (i.e. [sub]dorsi-basifixed), bilocular, (dark) purple, narrowly ovate or oblong-ovate, (1.5–)2–3.5(–4.5) mm long, base sagittate, apex scarcely confluent between thecae, sometimes minutely apiculate; pollen whitish. Pistil 1, 9–19.5 mm long, exceeding stamens and tepals; ovary globose, slightly trilobed, 2–4 mm long, 2–5 mm across, apex emarginate-concave, (pale yellowish) green or dark purplish pink, subdistal portion of carpel divergently protruding in fruit; ovules numerous, multiseriate (ca. 8-seriate) on central axile placentae; style terete, slightly narrowed proximally, straight or sometimes upcurved distally in nodding flowers, 6.7–13(–18.5) mm long, white or pale purplish pink; stigma discoid or depressed capitate, sometimes obtusely trigonous, or slightly trilobed to tricleft, 1.0–2.5(–3.3) mm across, white or pale purple. Capsules antrorse, broadly obpyramidal, tripartite, subtriangular in frontal aspect, obcordate or broadly obdeltoid in lateral aspect, 5–8 mm long, 1–1.5 cm across; lobes mitriform (or ovoid-pyriform), ascending, strongly divergent. Seeds with white or pale brownish testa, linear-fusiform, usually falcate, 4.8–6.7 mm long, 0.3–0.5 mm wide, proximally sublinear, distally subulate; body of seed oblong-fusiform, 1.4–1.7 mm long, 0.3–0.4 mm wide, brown.

Additional specimens examined (see also Tanaka 1998a):― JAPAN. Honshû. Chûbu Distr. Shizuoka Pref.: Mt. Higaneyama, 10 April 1920, fl., Ôsaka-fu Joshi Senmon-gakkô (MAK-137590). Chûgoku Distr. Yamaguchi Pref.: Tokuyama-shi, Nakasu-kita, Datoko, 11 April 1971, fl., H. Manabe no. 3 (TNS); Abu-gun, Tokusa, Mt. Nodôyama, ca. 900 m, N. Miake no. 5 (TNS-285022). Kantô Distr. Chiba Pref.: Awa-gun, Mt. Kiyosumi, May 1938, fl., S. Asano (TNS-59232). Kanagawa Pref.: prov. Sagami, Mt. Hakone, [May] 1910, fl. yellow, G. Koizumi s.n. (paratype of Heloniopsis japonica var. albiflora, TI !); Mt. Tanzawa, April 1960, fr., D. Yoshikawa (TNS-140984). Tokyo Pref.: Tama-shi, Sekido 7 April 1952, fl., U. Mizushima (TI, TNS-02633). Kinki Distr. Hyôgo Pref.: Kôbe, Mt. Rokkô, 11 April 1948, fl., C. Kataoka (TNS-132386). Kyôto Pref.: prov. Yamashiro, Mt. Hiei, [29 March] 1911, fl.-albi, T. Nakai s.n. (paratype of Heloniopsis japonica var. albiflora, TI !). Mie Pref.: Ise, Rokusôdani, 24 March 1961, fl., S. Okuyama 13565 (TNS-261521). Nara Pref.: Yoshino-gun, Mt. Mikamiyama, May 1888, fr., H. Sakurai (TNS-3836). Ôsaka Pref.: Mt. Kongôsan, 25 April 1953, fl., M. Togashi 720 (BM-001118052, TNS-105921); Mt. Kongôsan, 5 May 1935, fr., Z. Yoshino (TI). Wakayama Pref.: Mt. Kôyasan, Yatate, 20 Mar., G. Murata 22166 (TNS-305431). Kyûshû. Fukuoka Pref.: Nogouchi-keikoku, 27 March 1932, fl., H. Arao (TNS-255640). Kagoshima Pref.: Mt. Takakuma, 20 March 1944, fl., Y. Satake & S. Okuyama (TNS-79936–79938); Isl. Sakurajima, April 1904, fl., Y. Yoshise (MAK-137580). Kumamoto Pref.: Mt. Aso, Akamizu, 500 m, 2 April 1954, fr., Y. Shimada (TNS-248995); Kami-mashikigun, Yabe-machi, 280 m, 1 April 1994, T. Kawasaki 1059 (TNS-605322). Miyazaki Pref.: Sakatani-mura, Inotani, 22 Mai 1942, fr., S. Hattori 760 (TNS-307327); Kawaminami-mura, 10 March 1950, fl., M. Nagasawa (TNS-98301). Nagasaki Pref.: Simabara in montibus, bot. Japonicus s.n. (LE-01011595*); Mt. Unzendake, 29 March 1912, fl., Z. Tashiro (TNS-29965). Ôita Pref.: Mt. Kujyû, 24 April 1908, Nakamura 698 (TNS-79925). Saga Pref.: Ogi-gun, Mt. Hikodake, 22 April 1980, fr., T. Hashimoto (TI). Shikoku. Ehime Pref.: Shingû-mura, March 1889, fl., T. Makino (TNS-3838). Kôchi Pref. : Kami-gun, mononobe-mura, 3 March 1976, fl., K. Suzuki (MAK-270211); Nagaoka-gun, Ôtoyo-mura, Tatekawa, 5 May 1893, T. Makino (MAK-137567). Tokushima Pref.: Mt. Kôtsusan, 30 April 1903, J. Nikai (TNS-49296); Naka-gun, Aioi-chô, 300 m, 22 April 1983, fr., M. Takahashi & K. Ueda 1522 (TI); Mima-gun, Tsuzuro, 28 March 1940, fl., T. Yoshinaga (TI).

Distribution:― Japan: Honshû (southern Kantô District and westward to Chûgoku District), Shikoku, Kyûshû ( Fig. 29-B ).

Habitat:―Shady or semishady moist rocks or slopes usually along or near streams in forests at elevations ca. 150–900 m.

Conservation status:―The species is comparatively widespread, and assessed as LC according to the criteria set out in IUCN (2001). However, local populations near human habitation may be more or less subject to disturbance and threats.

Flowering:―March–April.

Ripening:―May.

Remarks:―Plants of Helonias breviscapa here circumscribed have often been treated as conspecific with H. orientalis (including its synonymous taxa) or as infraspecific taxa of the latter ( Miquel 1870, Ohwi 1953a, b, 1965, Kitamura 1964, Kitamura & Murata 1966). The two species may look somewhat alike, but H. breviscapa differs from H. orientalis by the thinner, less glossy, somewhat lighter (yellowish) green leaves usually minutely undulate at the margin ( Fig. 27G ), usually smaller flowers, and white tepals of which the proximal submarginal wings are relatively shorter and the nectary is positioned nearly as high as the ovary base ( Fig. 28B, C ; Tanaka 1997b, 1998a). Compared with H. orientalis , H. breviscapa is usually in warmer regions with less snowfall in winter in Japan. Their geographic ranges overlap partly ( Fig. 29-O, -B ) ( Tanaka 1997e, 1998a; Kawano et al. 2007). They were recognized as distinct by Maximowicz (1867), Hara (1947), and Tanaka (1998a). A few local forms of Helonias breviscapa have hitherto been recorded. For example, plants from Kyûshû ( Figs. 27A , 28A, B ), which were recognized as Heloniopsis breviscapa var. breviscapa ( Hara 1947) , usually have comparatively broad oblanceolate tepals which are abaxially often tinged (pinkish) purple and scarcely gibbous at the basal portion. Those from Isl. Yakushima, southern Kyûshû, which were distinguished as H. breviscapa var. yakusimensis ( Hara 1947) , are usually somewhat smaller in habit and have 1 or a few flowers and slightly thicker leaves. Those from the Kinki District, central Honshû ( Figs. 27C, D , 28D ), named H. breviscapa var. flavida ( Hara 1947) , have white, slightly longer, narrowly oblong-oblanceolate tepals with a slightly gibbous base. When some typical representatives of these varieties are compared, they may look somewhat distinct from one another. However, they are rather indistinct in delimitation due to a gradational variation between them when many samples from different localities are compared ( Tanaka 1998a). For instance, plants from eastern Shikoku (Tokushima Pref.; Figs. 27B , 28C ) have tepals scarcely inflated at the base and often tinged with purple toward the base like those from Kyûshû. Some plants from the Kinki District of Honshû also have tepals tinged purplish proximally and scarcely gibbous at the base ( Figs. 27D , 28D ). Fuse et al. (2004) stated that the leaves of H. breviscapa var. flavida are somewhat thin and spotted with reddish brown in winter, while those of H. breviscapa var. breviscapa are slightly thicker and spotted with brown to blackish purple in winter. In my observation, however, this distinction is not necessarily constant between them. For instance, under a cultivated condition in Tokyo, the leaves of plants from Kyûshû ( H. breviscapa var. breviscapa ) often turn reddish brown in winter. Those from different localities (Kyûshû, Shikoku, and the Kinki District of Honshû) often turn similarly brownish, irrespective of the original localities ( Fig. 27A–D ). Such coloration of the leaves appears to reflect coldness in winter, and may change to some extent in response to the fluctuation of temperature and habitat conditions. It seems more reasonable to regard these varieties ( breviscapa , yakusimensis , flavida) as local forms (races) not distinctly delimited from one another. I have noticed that the flowers of some plants from Kyûshû (Fukuoka and Miyazaki Pref.) and Shikoku (Tokushima Pref.) are fragrant, while those from the Kinki District (Nara, Mie, and Wakayama Pref.) are odorless. This intraspecific variation in floral fragrance needs a further survey. Despite these variations, Helonias breviscapa as a whole appears to retain a fairly high unity, possessing a unique combination of features as noted earlier. It is noteworthy that Helonias breviscapa ( Fig. 27G ) and H. koreana ( Fig. 23H ) share somewhat thin, dull or subdull leaf blades usually with minutely undulate margins. They usually occur in regions which are drier and less snowy in winter than the habitats of H. orientalis . Helonias breviscapa occurs in warmer regions than H. koreana . The relationship between the species of H. ser. Heloniopsis and the geographic and climatological features of their ranges are dicussed in Part III-5. Tanaka (1998a) once assigned Scilla japonica to Helonias breviscapa on the basis of the description by Thunberg (1784) (especially of floral color: corolla albo purpurea ) and the scapes figured in Thunberg (1802). Very recently (July 2018) I had an opportunity to examine the image of the scapes of the type material (Thunberg s.n., UPS-THUNB 8323*). Unexpectedly, the scapes looked fairly similar to those of H. orientalis . Further studies are necessary to precisely identify them. Scilla japonica is tentatively placed in the above synonymy. Nakai (1933) described the perianth of Heloniopsis japonica var. flavida as greenish yellow at anthesis, but did not cite any specimen. White tepals of Helonias breviscapa turn yellow or yellowish green soon after the peak anthesis, and moreover, the floral parts are persistent even at the fruiting stage. So the flowers after anthesis are often taken as those at anthesis with yellow or yellowish green tepals. At present there is no means to examine Nakai’s taxon as to the flowering stage and floral color on a specimen basis. A few herbarium specimens of Helonias breviscapa record the flowers as yellow, e.g., Kanagawa Pref., Hakone, May 1910, fl. yellow, G. Koizumi s.n. (paratype of Heloniopsis japonica var. albiflora, TI !); Mie Pref., Suzuka Mts, Gozaisho-dake, 20 Apr. 1941, fl. yellow, Morimoto no. 5 (TI!). The flowers appear to be past the flowering stage, implying the possibility that they were white at anthesis. Doi (1983: 135) recorded a yellow-flowered form of Helonias breviscapa as “ Heloniopsis orientalis C. Tanaka subsp. breviscapa Kitam. f. satsumensis Doi ” based on a specimen from southern Kyûshû, Japan (Kagoshima Pref., Ijûin-chô, April 1938, Toshio Shin, currently preserved at HIRO, the image seen). However, the name did not accompany a description nor a diagnosis in Latin, hence it was invalidly published. He noted that the flowers are yellow from the beginning of flowering. Such a yellow-flowered form has not been reported from anywhere since then. Studies based on fresh living plants seem necessary for a more precise understanding of this form.

Part III. Evolution and phylogeography

Evolutionary aspects of various characters (Part I) and taxa (Part II), and the historical background of the current distribution of Helonias (Part II) are discussed.

1. Pseudoduality in generation of flowering stems in vernal species, and variation in dormancy of leaf and flower buds

Pseudodual generation of flowering stems in vernal species, and its origin:―In mature plants of vernal species, such as Helonias bullata , H. thibetica and H. orientalis , two kinds of buds are produced in a basal rosette ( Fig. 1A, B ; Part I-2). One is a flower bud (inflorescence bud) that develops into a flowering stem (sexual reproductive organ; F in Fig. 1 ); the other is a leaf bud that develops a basal rosette of leaves (vegetative organs; L in Fig. 1 ). Both types of buds may be regarded as of the same generation, since they develop in the same growing season ( Fig. 1C, D ). Contemporaneous development of two kinds of buds in Helonias is unusual. Many related perennials, such as Veratrum L. and Anticlea Kunth ( Melanthiaceae - Melanthieae; Dahlgren 1985), produce only one kind of bud that develops into vegetative and sexual reproductive organs consecutively. In these plants, development of vegetative organs precedes development of sexual organs. They complete their yearly growth cycle within a single growing season (from spring through autumn). Helonias differs from Veratrum and allied genera in having leaves that persist after a single season, but their mode of development appears basically similar. As in Veratrum , the two organs of Helonias develop successively. That is, in temperate vernal species of Helonias , a leaf bud sprouts in the growing season (spring to summer), and around the time when the development of most fresh leaves is nearly completed, the flower bud starts to form (usually from July to September). Unlike in Veratrum and its allies, the flower bud of Helonias is formed, but does not sprout. Instead, it remains dormant until the coming spring (F in Figs. 1A, B , 4 ). The vegetative and the sexual organ of Helonias thus develop successively as in Veratrum , but their growth periods are largely separated by a cold season inserted in the middle of the yearly growth cycle. A flower bud initially forms in one year and the fresh flowering stem develops in the next (F in Fig. 1C, D ). Rosulate leaves sprouted in the preceding year (R in Fig. 1 ) are regarded as of the same generation, since they originate within a single growth cycle, then develop sequentially. Two kinds of buds sprouting nearly concurrently in the spring from a rosette (F and L in Fig. 1C, D ), mentioned above, are regarded as two generations, or two consecutive generations. That is, the flower bud (F in Fig. 1A, B ) is of the same generation as the rosulate leaves sprouted in the preceding year (R in Fig. 1C, D ); the leaf bud (L in Fig. 1A, B ) to sprout in the current growing season is of the next generation. Thus the flower buds (flowering stems) superficially look dual in generation. Supposedly, ancestral Helonias grew in warmer regions with no severe cold season, and the two kinds of organs developed nearly consecutively as in Veratrum . Then the climate became cooler and was accompanied by a cold season or, alternatively, the plants extended their range to cooler regions with severe winters. Through the course of evolution, the ancestors eventually acquired a gapped, prolonged yearly growth cycle in which the development of the sexual organs became separated seasonally from development of vegetative organs due to the insertion of a cold season. This yearly growth cycle naturally requires a longer span than a non-gapped growth cycle as seen in Veratrum . It takes a span over two years (or two growing seasons with a cold season in between) when estimated from the time of sprouting of a leaf bud (in spring) to the death of a flowering stem in the following year (usually in late spring to early summer). If estimated from the time of initial formation of a leaf bud, usually from summer to early autumn in the year preceding sprouting, then an entire growth cycle spans over three years (or three growing seasons with two cold seasons in between) ( Fig. 2 ). Chamaelirium (including Chionographis ), which is closely allied to Helonias ( Tanaka 1997e, 2017a, b), also has such a gapped, prolonged yearly growth cycle and a flowering stem pseudodual in generation, suggesting that Chamaelirium and Helonias are sister groups sharing a common ancestor.

Reduced dormancy in leaf and flower buds of Asian subtropical species:―In Helonias kawanoi and H. jinpingensis in the subtropics, anthesis is usually in late summer to autumn. In H. kawanoi , the flower bud sprouts shortly after most fresh leaves nearly complete their development ( Figs. 2 , 16A, D. E ). That is, the two organs develop nearly consecutively. This mode of development differs from other temperate vernal species in which the sprouting of a flower bud is suppressed until the spring (F in Figs. 1A, B , 4 ). The yearly growth cycle of H. kawanoi and H. jinpingensis was probably secondarily acquired as a result of adaptation to a warm subtropical climate. Under such a climate with no severe cold season, dormancy of the flower bud may have been reduced or lost. In temperate vernal species of Helonias , the leaf bud is similar to the flower bud, initially formed from summer to early autumn in the central portion of a rosette, then remaining dormant until spring (L in Figs. 1A, B , 4 ). In H. kawanoi , H. leucantha and H. umbellata , however, the leaf bud often begins to sprout in autumn and winter ( Figs. 16A, D, E for H. kawanoi , 18F for H. leucantha ), although growth appears more or less suppressed under the cooler conditions ( Fig. 2 ). In these species the dormancy of the leaf bud appears to have been reduced. The basic mode of development of ancestral Helonias (or of the Helonias and Chamaelirium lineage) might have been similar to that of the subtropical species. The phenological process of a yearly entire growth cycle in seven species of Helonias is schematized in Fig. 2 . Ancestral Helonias is presumed to have existed somewhere in the northern circumpolar region in the Paleogene when temperatures became predominantly lower toward the end of the period (for a geological and climatological aspect, see: Chaney 1947, Tanai 1967, 1972, 1988, 1992, Uemura 1995, Ogasawara & Uemura 2006). The historical background of the migration or extension of the ancestral populations of Helonias is discussed below (section 5).

2. Trends in the evolution of characters and structures

Evaluation of character states from an evolutionary perspective:―In the course of evolution, simple structures of plants often become more complex by fusion of similar or dissimilar parts or by developing additional structures. In general, with an increase of such complexity, the level of structural organization or specialization becomes higher. It is often difficult to determine evolutionary directions in phenotypic characters, but in characters showing stepwise structural changes, it seems possible to draw fairly reasonable inferences on directions. In Helonias , for instance, the tepals and the filaments of several species (e.g., H. sect. Helonias , H. subsect. Ypsilandra ) are free and the nectaries are more or less shallow, while those of some other species (H. ser. Heloniopsis ) are adnate to form saccate or tubular nectaries (Part I-8). These are judged to be derived, more advanced structures (i.e. apomorphies). As for the pistil, the degree of connation among three carpels to form a single columnar style varies among taxa (Part I-8). It is evident that the carpels least connate among them are most primitive in state, and those entirely connate along their length are most advanced (Part III-2-3). Evolution in the reverse direction (or retrogressive evolution), from a higher level of organization or specialization to a lower level, is highly improbable in these structures of Helonias . Inferences from these structures therefore appear to be applicable to the determination of evolutionary directions of characters (Part III-2) and to the elucidation of the process of phyletic diversification in this genus (Part III-3, -4). In inferring evolutionary trends of characters, the corresponding character states in other related genera, such as Chamaelirium , Xerophyllum and Veratrum , were also taken into account (e.g. floral color, nectar-secretion in tepals, morphology of ovaries, capsules and seeds). Table 10 shows evolutionary trends of several characters thus inferred.

Inflorescence:― Helonias has different types of inflorescence (Part I-7). Helonias sect. Helonias and H. subsect. Ypsilandra (H. sect. Heloniopsis ) have a raceme, while H. subsect. Heloniopsis has a raceme, subumbel or an umbel. From a structural point of view, umbels appear more advanced or specialized than racemes. Flowers considered to be primitive, such as those of H. sect. Helonias , are borne in racemes, while flowers regarded as advanced, such as those of H. ser. Heloniopsis , form umbels . In related genera such as Chamaelirium , Xerophyllum and Veratrum , racemes or panicles are common ( Britton & Brown 1896, Tamura 1998, Utech 2002). Considering these facts, it is highly probable that the inflorescence of Helonias was originally a raceme, but evolved to become a subumbel or an umbel through abbreviation of the rachis. With this change, the arrangement of flowers on the rachis also changed from spiral (in a raceme; e.g. Fig. 13C ) to subverticillate (in an umbel; e.g. Fig. 23E ). In H. sect. Helonias and H. subsect. Ypsilandra , the nectary at the base of the tepal is shallow and the nectar is exposed (Part I-8), so even insects with short mouthparts (trophi) could suck the nectar. In H. ser. Heloniopsis (H. subsect. Heloniopsi s), the nectary is saccate or tubular (Part I- 8), suggesting that the flowers of H. ser. Heloniopsis are adapted to pollinators that can extract nectar from such deeper nectaries. The evolutionary shift from raceme to umbel may also be related to the kinds and habits of pollinators. This shift is supposed to have improved the efficiency in pollination. Whether the inflorescence is a raceme or an umbel, flowers in aggregation (e.g. Figs. 4A–E , 13C , 25A–D ) must have been more effective in attracting insects. This state is likely to have increased the opportunity for pollination. The ebracteate inflorescence of Helonias (e.g. Figs. 13C , 18D , 23G ) is also shared by the closely allied Chamaelirium ( Tanaka 2017b) , so it must have been the original state. The bracteate inflorescences of H. jinpingensis and H. kawanoi ( Fig. 16C ) appear to be secondarily derived ( Table 10).

Pistil:―In Helonias , the three carpels are connate to form a columnar style the relative length of which differs among the species (Part I-8; Tanaka 1997c, e). The style is shortest in H. bullata ( Fig. 5D , Table 6; Tanaka 1997a). In H. thibetica (H. subsect. Ypsilandra ) and H. subsect. Heloniopsis the style is well developed and the pistil often exceeds the stamens (Part I-8; e.g. Figs. 13B, C , 16B , 27A–D , 28A , Table 6 for H. thibetica ). In Helonias , pistils with a relatively short style (columnar part) and long stigmatic segments, such as those of H. bullata ( Fig. 5D ) and H. yunnanensis var. yunnanensis ( Fig. 7B ), are regarded as more primitive. This state apparently shifted evolutionarily toward a relatively long style and short stigmatic segments. A pistil with a long style and discoid or (sub)capitate stigma occurs in H. thibetica (e.g. Figs. 3A–C , 14A ) and subsect. Heloniopsis (e.g. Figs. 3D, E , 20D , 22A , 24F , 28A ; Tanaka 1997c, e), and is regarded as the most advanced state. The evolution of the pistil in Helonias thus appears to be directional and anagenetic.

Anthers:―The anthers of Helonias vary in structure, shape, size, and in position relative to the stigmas (Part I-8). The anthers of H. bullata (H. sect. Helonias ) and H. subsect. Ypsilandra are unilocular and basifixed (e.g. Figs. 5B , 14E ). They expose their pollen not only laterally but also apically ( Fig. 2 in Tanaka 1997a), hence they may readily smear pollen on insects foraging for pollen and/or nectar. In H. subsect. Heloniopsis the filament tends to be located closer to the opposing tepal ( Figs. 19B–E , 22A–E , 28B, C, E ; Tanaka 1997b, c, e). The anthers are virtually bilocular, extrorse, and often comparatively long ( Figs. 22F , 24F , 28F ; Tanaka 1997c), accordingly their pollen is likely to be smeared on insects trying to extract nectar from the base of the tepals. They appear to be more adapted to insects seeking nectar ( Tanaka 1997e), although insects seeking only pollen, such as flies, also visit and pollinate the flowers, as reported by Takahashi (1988). During the course of evolution the anthers of Helonias appear to have changed from unilocular to bilocular ( Tanaka 1997c). Almost perfectly bilocular anthers are produced in H. breviscapa ( Fig. 28F ; Tanaka 1997c) and may represent the ultimate evolutionary outcome. It is also noteworthy that the anthers of H. ser. Heloniopsis , especially of Helonias koreana ( Fig. 24F ) and H. orientalis , are (sub)dorsi-basifixed, i.e. the anther is affixed to the filament adaxially slightly above the connective base (Part I-8). This state is obviously apomorphic.

Floral structure:―Flowers of Helonias are highy diversified especially in structure (Part I-8). For instance, the tepals are almost flat or only slightly canaliculate in H. sect. Helonias and H. subsect. Ypsilandra , while they are more prominently grooved especially in H. ser. Heloniopsis . Nectaries are nearly flat or only slightly concave in H. sect. Helonias and H. subsect. Ypsilandra , they are markedly saccate in H. ser. Heloniopsis (Part I-8). In H. sect. Helonias , H. subsect. Ypsilandra and H. ser. Umbellatae , the filaments and tepals are distinct or almost so. They are basally fused in H. ser. Heloniopsis (Part I-8). From a structural point of view, the floral evolution of Helonias appears to have advanced stepwise from the state in H. sect. Helonias ( Figs. 4 , 5 ) and H. subsect. Ypsilandra (e.g. Fig. 7 ), through H. ser. Umbellatae (e.g. Figs. 17 , 19 , 20 , 22 ), and lastly to H. ser. Heloniopsis (e.g. Figs. 24 , 26 , 28 ; Tanaka 1997e). The flower of H. ser. Heloniopsis , which is made up of a single pistil and six surrounding subunits each consisting of a stamen and the opposing tepal that jointly form a saccate or tubular nectary, is viewed as an integrated apparatus for achieving efficient pollination through the behavior of certain insects ( Tanaka 1997e).

Ties with insects:―The flowers of many species of Helonias are fragrant and the tepals are nectariferous and often pink, bluish, violet or white (Part I-8). It is obvious that these features effectively attract insects foraging for nectar and/or pollen (Part I-11, Takahashi 1988). The flowers of Helonias are basically similar to one another, so they must have been coevolving with the insects since their origin. In this connection, it is notable that the flowers of H. leucantha (H. ser. Umbellatae ), H. breviscapa , H. koreana , and H. orientalis (H. ser. Heloniopsis ) are often odorless or nearly so, perhaps indicating that fragrance is not always necessary for attracting some kinds of pollinators, which may discern the flowers by other sensory means, such as vision. In the most closely allied Chamaelirium the flowers have no nectaries ( Tanaka 2017b). It is therefore obvious that close ties with insects foraging for nectar have been a principal factor for the evolution of Helonias ( Fig. 30 , List 2).

Traits securing seed production under poor availability of pollen vectors:― Helonias orientalis blooms in early to mid spring. Although infrequently visited by insects ( Takahashi 1988, as Heloniopsis ), the flowers produce numerous seeds in the field ( Kawano & Masuda 1980). The following three traits of this species appear to cooperate effectively to secure seed production under poor availability of pollen vectors: high self-compatibility (known also in H. bullata and H. thibetica ; Part I-12), long flowering duration (known also in many species such as H. bullata , H. thibetica and H. subsect. Heloniopsis ; Part I-8), and widely open, funnel-shaped flowers that are structurally highly accessible for a wide variety of insects (known also in H. bullata ; Part I-11). Judging from the high similarity in sexual reproductive characters (e.g. self-compatibility, floral morphology, flowering phenology, pollination ecology) among the species, these three traits appear to have been cooperating as essential, effective sexual means to survive over the course of evolution in Helonias .

Evolution of structurally advanced flowers of Helonias ser. Heloniopsis coupled with a reduction in flower number and an increase in ovule number:―Flowers of Helonias ser. Heloniopsis appear to be the most advanced in Helonias . For instance, the tepals are proximally adnate to the opposing filament to form a saccate or tubular nectary ( Utech & Kawano 1981 for Heloniopsis orientalis ; Tanaka 1997b, e) and also connate to adjoining ones ( Figs. 24C–E , 26A, C , 28E ). The inflorescence comprises a comparatively small number of flowers (up to 14; Figs. 23 , 25 , 27 ) each bearing numerous ovules (e.g. to 189 per locule in H. orientalis ( Table 1); Utech 1978 for H. orientalis ; Tanaka 1997c, d). Such advanced floral structures appear to have evolved as a result of adaptation to insects foraging mainly for nectar. Presumably, the flowers improved pollination efficiency through restructuring and thereby enabled a reduction in flower number and an increase in ovule number in individual flowers. Utech (1978) reported that the total number of ovules per inflorescence is, on average, similar between Helonias bullata and Heloniopsis orientalis , although the number of flowers per inflorescence and the number of ovules per locule differ significantly. From my observations, I believe that H. bullata is the more primitive species and H. orientalis is one of the most advanced in the genus. The two species nearly represent the two extremes of phyletic evolution ( Fig. 30 , List 2). Similar data come from studies on plastid DNA sequences ( Kim et al. 2016). The evolutionary trend toward H. orientalis , which produces comparatively fewer flowers and more numerous ovules, appears to be well reflected in this data. Floral evolution in Helonia s thus appears to have been directional and anagenetic. In both Helonias bullata and H. orientalis , seedling establishment in habitats is equally very low (Part I-15; Kawano & Masuda 1980, Sutter 1984), and asexual reproduction by rhizomic division is fairly limited. Accordingly, to survive, they need to produce numerous seeds enough to cover the low rates of seedling and rhizomic recruitment. This necessity of producing numerous seeds needed for survival may account for the similarity in the total number of ovules per inflorescence between the two species ( Utech 1978) mentioned above. Presumably, in H. bullata bearing comparatively few ovules (per locule or ovary; Table 1), production of a necessary number of ovules for survival was achieved by producing many flowers (per scape), while in H. orientalis having comparatively few flowers (per scape), it was attained by producing numerous ovules in individual flowers. Since the ovules similar in total number are produced by fewer flowers, the pollination efficiency in individual flowers of H. orientalis is regarded as higher than that of H. bullata . An increase in ovule number per locule may have resulted in producing narrower seeds, because a locular space available for fertilized ovules to develop is likely to be more or less limited. Divergence in seed width (Part I-10) must have occurred at an early stage of evolution in Helonias , as it is seen between the two sections H. sect. Helonias ( H. bullata ) and H. sect. Heloniopsis (including H. orientalis ).

3. Phylogenetic divergence and relationships

Evolutionary facets of the respective taxa (Part II) are outlined mainly on the basis of comparative studies of character states (Parts I, III-2).

Helonias :― Helonias is most closely allied to Chamaelirium in North America and eastern Asia ( Tanaka 1997e, 2017b). They share many similar features; for instance, the persistent oblanceolate or spatulate leaves in a basal rosette, a flowering stem with the growth period usually markedly separated from development of the rosette in the preceding year (Part III-1; F and R in Fig. 1C, D ; Fig. 2 ), peduncles with scale-like leaves (e.g. Figs. 1C , 21A, B ), ebracteate pedicels (e.g. Figs. 12A , 13C ), and carpels connate dorsally to adjoining ones along their ventral sutures (e.g. 26C–E). Helonias as a genus is monophyletic ( Fig. 30 , List 2), consisting of two sections Helonias and Heloniopsis (Part II) .

Sect. Helonias :― Helonias bullata has three styles distinct nearly to the base ( Fig. 5D ; Tanaka 1997a), suggesting that it is the most primitive member of the genus, at least in style characteristics. Helonias bullata also has fewer ovules (per locule or ovary) and slightly larger (broader) seeds than its congeners ( Fig. 5F , Table 1; Tanaka 1997c). The surface of the nectary is nearly flat. These character states may also be primitive in Helonias . Helonias sect. Helonias is regarded as paraphyletic ( Tanaka 1997e).

Sect. Heloniopsis :―In Helonias sect. Heloniopsis the three styles (carpels) are consistently connate to one another partially or entirely along their length to form a single column (e.g. Figs. 9A–C , 12 , 14A , 22A ). This character state is regarded as more advanced than in H. sect. Helonias . Helonias sect. Heloniopsis is monophyletic ( Fig. 30 , List 2), and all members are in eastern Asia (Figs. 15, 29, 31, 32). This section is composed of two subsections: H. subsect. Ypsilandra and H. subsect. Heloniopsis (Part II) . The former subsection is considered to be more primitive (Part II; Tanaka 1997e) and occurs west of the range of the latter ( Fig. 32 ). The species of H. subsect. Heloniopsis are either insular or coastal ( Figs. 29 , 31-3 , -4, 32-3, -4).

Subsect. Ypsilandra :― Helonias subsection Ypsilandra appears more advanced in several characters than H. sect. Helonias . For instance, the styles (columnar part) are longer ( Figs. 9A–C , 10E , 12 , 14A , Table 6), the stigmatic segments are relatively shorter ( Figs. 7B , 9A–C , 10E , Table 6), and the stigmatic portion is sometimes simple and unlobed ( Figs. 3A–C , 13A–C ), the anthers are unilocular and not septate between the thecae ( Fig. 14E ), and the seeds are significantly more numerous and narrower ( Figs. 7G , 9D , Table 1). In H. subsect. Ypsilandra , Helonias yunnanensis var. yunnanensis is regarded as the most primitive taxon, since it has the shortest style and a deeply trifurcate stigma ( Fig. 7B , Table 6). All other members of the section are regarded as descendants from the ancestral lineage of this variety ( Fig. 30 , List 2). Helonias jinpingensis with a short style and a somewhat deeply trifurcate stigma also appears to be primitive. Helonias alpina , with longer styles and slightly shorter stigmatic segments ( Fig. 10E ) than H. jinpingensis , may be slightly more advanced. Helonias parviflora ( Figs. 11 , 12 ), with a very slightly trilobed (or nearly trigonous) stigma, is regarded as more advanced, at least in pistil characters. Helonias thibetica ( Figs. 13 , 14 ) with a relatively long slender style and a small capitate or discoid stigma ( Figs. 3A–C , 14A , Table 6) is the most advanced in pistil characteristics in this subsection. In H. subsect. Ypsilandra , the flowers have shifted from nearly adichogamous (in species other than H. thibetica ) to protogynous (in H. thibetica ) (Part I-13). This subsection is regarded as paraphyletic ( Tanaka 1997e), and presumed evolutionary relationships between the members are shown in Fig. 30 (List 2). From plastid DNA sequence analyses, Fuse & Tamura (2016) suggested that Helonias s.str. (H. sect. Helonias in the present paper), Ypsilandra (H. subsect. Ypsilandra ) and Heloniopsis (H. subsect. Heloniopsis ) are all monophyletic. Heloniopsis is monophyletic as shown in Fig. 30 and in Tanaka (1997e), but the monophyly of Helonias and Ypsilandra is not supported by the present study, because many characteristics of Heloniopsis , such as long united styles, discoid or subdiscoid stigmas, and filaments liberated from the ovary base (List 2-14), cannot have been derived if they did not pass through the precursory stages as possessed by Helonias and Ypsilandra . It is highly improbable that similar characteristics have developed independently in Ypsilandra and Heloniopsis as an outcome of parallel evolution, and the ancestral lineage of Heloniopsis , which linked Helonias and Heloniopsis directly and had intermediate character states between them, was entirely extinct, whereas species of Ypsilandra are extant. This discordance in results between morphology and DNA sequence analyses probably stems from the difference in research objects (whole characters of organisms manifested as the total sum of all genic activities involved vs. selected fractions of DNA molecules) and methods employed (clustering objects by synapomorphies vs. degree of similarity among DNA sequences).

Subsect. Heloniopsis :―Several character states of Helonias subsect. Heloniopsis are regarded as more advanced than those of H. subsect. Ypsilandra . For instance, the tepals are usually more markedly canaliculate toward the base ( Figs. 19D, E , 20A, B , 22D, E , 24D, E , 26A , 28E ), the nectaries are usually more prominently saccate ( Figs. 22D, E , 24A–E , 26A–C ), the stamens tend to be located closer to the tepals ( Figs. 19B–E , 22B–E , 24B–E , 26A–C , 28B, C, E ; Tanaka 1997e – Fig. 2 ), and the anthers are virtually bilocular, extrorse, and often longer ( Figs. 20C , 24F , 28F ). These character states are considered to be apomorphies, and this subsection is regarded as monophyletic in sharing them ( Fig. 30 , List 2). Helonias thibetica (H. subsect. Ypsilandra ) has protogynous flowers, tepals slightly canaliculate toward the base, a pistil exserted beyond the tepals, and a capitate or discoid stigma. These features approach those of H. subsect. Heloniopsis (Part II) , suggesting that H. subsect. Heloniopsis originated from the ancestry of H. thibetica ( Fig. 30 , List 2; Tanaka 1997c, d, e). Helonias subsect. Heloniopsis consists of two series: H. ser. Umbellatae and H. ser. Heloniopsis (Part II) .

Ser. Umbellatae :―Several character states of Helonias subsect. Heloniopsis are regarded as more advanced than those of H. subsect. Ypsilandra , as stated in the preceding section. In addition, the umbels, sub-umbels or somewhat compact racemes in species of H. ser. Umbellatae (Part I-7, II-2) also appear to be more advanced character states. The apex of the leaves of H. ser. Umbellatae tends to be slightly more prominently apiculate than in its congeners (apiculus of H. ser. Umbellatae to ca. 2 mm long vs. to ca. 1.3 mm long in other species), probably suggesting that species in this series originated from the same ancestry (List 2-14). Of the three species of H. ser. Umbellatae , H. kawanoi appears to be the most primitive in some floral characters. For instance, the inner filaments of H. kawanoi are close to the base of the ovary ( Fig. 17E ), thereby approaching H. subsect. Ypsilandra , where the inner filaments are adnate to the base of the ovary ( Fig. 14C ; Tanaka 1997a). Further, the tepals of H. kawanoi are shallowly canaliculate proximally and the nectary is least concave. The autumnal flowering is also indicative of an old origin of this species. These facts suggest that H. kawanoi diverged earlier than H. umbellata and H. leucantha from the ancestral lineage of H. ser. Umbellatae ( Fig. 30 , List 2). Helonias kawanoi ( Figs. 16 , 17 ) is a dwarf plant with small comparatively thin leaves, short slender flowering stems, bracteate pedicels, and solitary or a few small autumnal flowers. All these character states are considered to be apomorphies ( Fig. 30 , List 2). Supposedly, H. kawanoi has acquired many of its unique features as a consequence of adaptation to an ecologically unusual location. Being small, the plants can not only utilize microhabitats for their life space, but also colonize on such unusual locations as steep cliffs and banks along streams that may overflow after heavy rainfall. Often growing among mosses, H. kawanoi may be viewed as an element of the moss layer community in the vertical stratification of vegetation. Helonias leucantha ( Figs. 18–20 ) is normally larger than H. umbellata ( Figs. 21 , 22 ), and usually has larger leaves and slightly larger, pendulous, campanulate flowers that bloom from (late December) January through mid March. All of these character states are viewed as apomorphies. Helonias leucantha grows on shady moist rocky slopes near streams. It appears to share an immediate ancestry with H. umbellata ( Fig. 30 , List 2). Helonias umbellata usually grows on moist rocky slopes in shade or semi-shade at low to high elevations of Taiwan. It usually flowers from (late January) February through March, except on high peaks. Helonias umbellata , endemic to Taiwan, is geographically isolated from two Ryukyuan species H. leucantha and H. kawanoi ( Fig. 29 ; Tanaka 1997e, 1998a). The Ryukyuan species overlap in distribution on four small islands; Tokunoshima, Okinawa, Ishigaki and Iriomote ( Tanaka 1998a) , but there are no reports of their co-occurrence in the same habitats on these islands, thereby implying that their habitat preferences subtly differ. Moreover, their flowering periods scarcely overlap ( Tanaka 1997d). The three species of H. ser. Umbellatae therefore appear to be isolated from one another, at least by one or more of the following; geography, ecology, sexual reproduction. Flowers of both Helonias umbellata (e.g. Figs. 21A–C , 22A ) and H. kawanoi (e.g. Figs. 16A, B , 17C ) are similar in shape (both obconic), but differ in size. Flowers of H. umbellata and H. leucantha (e.g. Figs. 18B, D , 19A ) differ in shape, degree of fragrance, and usually in size ( Table 8). Their pollinators are also likely to differ to some extent in kind and/or visiting frequency.

Ser. Heloniopsis :― Helonias ser. Heloniopsis comprises Helonias koreana , H. orientalis , and H. breviscapa (see Part II). They share subumbels or umbels of comparatively few flowers ( Figs. 23A–G , 25A–E , 27A–D ), tepals with submarginal wings (lamellae) by which they are connate basally to adjoining tepals and adnate to opposing filaments (e.g. Figs. 24C–E , 26A , 28E ), and sheath-like (tubular) nectaries formed by the adnation (e.g. Figs. 24A–E , 26A–C , 28E ). All of these structures are obviously apomorphies. Helonias ser. Heloniopsis is therefore a monophyletic group ( Fig. 30 ; Tanaka 1997e). In H. ser. Umbellatae , the proximal submarginal portions of the tepal are raised or ridged, but not winged ( Figs. 17D , 19D, E , 20A, B , 22D, E ). Further, unlike H. ser. Heloniopsis , they are not connate between adjoining tepals in H. kawanoi (e.g. Fig. 17D ) and H. leucantha (e.g. Fig. 19E ). In H. umbellata , however, they are occasionally minutely connate basally between adjoining tepals ( Fig. 22D ). In all three species of H. ser. Umbellatae , there is no adnation between the tepals and their opposing filaments ( Figs. 17D, E , 19D, E , 22B, D, E ; Tanaka 1997b, e, 1998a). There is no doubt that the proximal submarginal wings of the tepals of H. ser. Heloniopsis are derived from the ridged or raised submarginal portion of the tepal of H. ser. Umbellatae . As aforementioned, like H. ser. Heloniopsis , H. umbellata occasionally has proximal ridges minutely connate basally to those of adjoining tepals ( Fig. 22D ). The floral structure of H. ser. Heloniopsis therefore appears to have originated from the one as seen in H. umbellata ( Tanaka 1997b, e). Evolution in the reverse direction, i.e. from H. ser. Heloniopsis to H. ser. Umbellatae , is unlikely. It is also improbable that the floral structure exactly the same as that of H. ser. Heloniopsis developed independently in a different lineage as a consequence of parallel evolution. Taking all these improbabilities into account, the cladogram based on some fractions of plastid DNA sequences presented by Fuse & Tamura (2003, as Heloniopsis ) does not appear to reflect the actual phylogeny (cladogenesis). In their analyses, two species of H. ser. Heloniopsis ( Helonias orientalis and H. breviscapa here circumscribed) cluster with three species of H. ser. Umbellatae (here circumscribed), but not with the Korean species ( Heloniopsis koreana and H. tubiflora in their paper) of the same H. series Heloniopsis . Their observations on the floral structure also do not necessarily coincide with mine (see also related remarks under H. koreana in Part II of present paper). Results of my observations on phenotypic characters thus markedly contradict those of their analyses on DNA sequences and floral morphology. As stated above, in my data, Helonias koreana is phylogenetically close to the rest of species of H. ser. Heloniopsis ( Fig. 30 ), and in data published by Fuse & Tamura (2004), Korean species deviate significantly from the remaining (Japanese and Taiwanese) species of H. subsect. Heloniopsis . This incongruence might suggest that the degree of divergence in DNA sequence is not necessarily correlated with phylogenetic distance. Obviously, this issue needs further studies. In Helonias koreana (including Heloniopsis tubiflora ), the adnate portion between a tepal and the opposite filament is nearly as high (long) as or slightly higher (longer) than the connate portion between adjoining tepals ( Figs. 24C, D ), while in H. orientalis and H. breviscapa the adnate portion is consistently higher (longer) than the connate portion ( Figs. 26A , 28E ). In this respect, I regard the character state of H. orientalis and H. breviscapa to be more advanced than in H. koreana . This view is reflected in constructing the phylogram in Fig. 30 (List 2) in which H. orientalis and H. breviscapa are clustered as sister species. Helonias ser. Heloniopsis appears most closely allied to Helonias umbellata of H. ser. Umbellatae ( Tanaka 1997e) , since the tepals of the latter are sometimes basally connate ( Fig. 22D ) like those of H. ser. Heloniopsis . Helonias ser. Heloniopsis and H. umbellata are hence likely to be monophyletic, sharing a common ancestry ( Fig. 30 , List 2). Two species of H. ser. Umbellatae , H. kawanoi and H. leucantha , are somewhat specialized and do not appear to be directly related to H. ser. Heloniopsis . Helonias umbellata , on the contrary, appears less specialized except for some characters (e.g. umbellate inflorescence) and even occurs at high elevations on Taiwan, implying that it can survive a cooler climate. The ancestor of H. umbellata may have evolved the lineage of ser. Heloniopsis while staying somewhere in or around the current range (such as Japan and Korea) of ser. Heloniopsis as a consequence of northward migration. The three species of H. ser. Heloniopsis appear to have individual preferences for climatic conditions. They appear to have phyletically diverged as a result of adaptation to different climatic types covering maritime regions of the Far East. For related remarks see section 5.

4. Process of phyletic diversification

A phylogenetic tree or phylogram (phenogram) based on cladistic analyses of phenotypic characters is shown in Fig. 30 . It is revised from Tanaka (1997e) and was constructed from hypotheses based on observations in the present study.

Attempts to construct phylograms (cladograms) from analyses of DNA sequences are valuable, but we need to be cautious especially in applying the results to classifications of organisms. DNA fractions used for phylogenetic analysis are generally limited in portion and sampling and hence the results may fluctuate to some degree. For instance, if samplings from highly variable species are strongly biased, the resultant phylogram inferred may more or less deviate in topology from the true one. Further, as stated earlier (Part III-3), analyses based only on the degree of similarity between DNA sequences often override paraphyletic lineages recognizable by phenotypical cladism, and hence it seems difficult for them to faithfully trace the true process of phylogenetic diversification. To obtain a phylogram closer to the actual phylogenesis, data from other aspects (particularly phenotypic characters) need to be taken into account.

In this study, in constructing the phylogenetic tree, the taxa are clustered by synapomorphies inferred from comparative surveys of character states (Part I, III-2). The character states regarded as apomorphies are enumerated in List 2 under the respective lineages or clades that correspond to those in Fig. 30 . Synapomorphies for lineage 1 rest on the presumption that Chamaelirium (including Chionographis ) is the sister lineage of Helonias , which is also supported by plastid DNA sequence data ( Fuse & Tamura 2000, Givnish et al. 2016, Kim et al. 2016).

LIST 2. Character states regarded as apomorphies, which are presumed to have been acquired by each lineage in Fig. 30 , are enumerated below under the respective lineage numbers corresponding to those in Fig. 30.

1) Immediate (closest) ancestral lineage common to lineages 2 and 3 (vs. lineage of Chamaelirium ).

1. Anthers become distinctly unilocular, losing adaxial septum (furrow) between thecae.

2. Apex of ovary becomes emarginate-depressed.

3. Carpels of ripe fruit become abaxially protruding subdistally.

4. Three styles become connate basally to form very short column.

2) Lineage of Helonias bullata .

1. Tepals become pink.

3) Immediate ancestral lineage common to lineages 4 and 5.

1. Plants become somewhat smaller, as reflected in leaf size and scape height.

2. Pedicels become slightly shorter.

3. Stamens become slightly shorter.

4. Anthers become latrorse (except apical part which is antrorsely dehiscent).

5. Abaxial septum (furrow) between thecae as in H. bullata becomes lost (i.e. anthers become perfectly unilocular with no septum between thecae).

6. Style (columnar part) becomes slightly longer.

7. Ovules per locule become more numerous.

8. Seeds (with testa) become more slender (linear-fusiform).

4) Lineage of Helonias yunnanensis var. yunnanensis .

1. Whole body (habit) often becomes reduced in size, as reflected in leaf size, scape height, and flower size.

2. Stamens usually become further shortened.

5) Immediate ancestral lineage common to lineages 6 and 7.

1. Style (columnar part) becomes slightly longer.

6) Lineage of Helonias jinpingensis .

1. Pedicels become relatively slightly longer.

2. Pedicels become bracteate at base.

3. Flowering in late summer to early autumn.

7) Immediate ancestral lineage common to lineages 8, 9 and 10.

1. Style becomes relatively slightly longer.

2. Stigmatic lobing becomes relatively slightly reduced.

8) Lineage of Helonias yunnanensi s var. mesostyla .

1. Apomorphy not yet specified.

9) Lineage of Helonias alpina .

1. Tepals become slightly longer.

2. Tepals become narrowly oblong(-oblanceolate).

3. Style becomes slightly longer.

4. Stigmatic lobing slightly reduced.

5. Filaments become longer.

10) Immediate ancestral lineage common to lineages 11 and 12.

1. Stigma becomes only slightly trilobed.

11) Lineage of Helonias parviflora .

1. Flowers become slightly smaller, as reflected in tepals.

12) Immediate ancestral lineage common to lineages 13 and 14.

1. Pedicels become longer.

2. Flowers become protogynous.

3. Flowers tend to become slightly larger.

4. Stigma and stamens usually become exserted beyond tepals.

5. Stigma becomes discoid.

13) Lineage of Helonias thibetica .

1. Stigma becomes slightly smaller.

2. Stigma usually becomes (sub)capitate.

14) Immediate ancestral lineage common to lineages 15 and 16.

1. Apiculus at leaf apex becomes (relatively) slightly more prominent.

2. Racemes tend to become slightly more compact at anthesis.

3. Inner filaments become liberated from base of ovary.

4. Anthers become adaxially affixed to filament (i.e. adaxially basifixed).

5. Anthers become extrorse.

6. Anthers become virtually bilocular with traces of apical confluence between thecae.

15) Lineage of Helonias kawanoi .

1. Whole body (habit) becomes significantly smaller, as reflected in rhizome, leaves, height of scape, cauline scaly leaves, flowers. 2. Leaves become somewhat thinner (in texture).

3. Main parallel veins of leaves become slightly raised adaxially.

4. Flowering in late summer to autumn (or dormancy in development of flowering stem becomes almost lost).

5. Pedicels become bracteate.

6. Flowers (per scape) become fewer.

7. Inflorescence becomes usually (sub)umbellate.

8. Ovary becomes sessile.

9. Seeds (incl. testa) become smaller (shorter).

16) Immediate ancestral lineage common to lineages 17 and 18.

1. Tepals become more distinctly canaliculate toward base.

2. Proximal submarginal portions of tepal become more prominently raised.

3. Nectary at base of tepal becomes more prominently concave.

4. Filaments tend to become slightly closer basally to opposing tepal (rather than to base of ovary).

17) Lineage of Helonias leucantha .

1. Entire body (habit) becomes slightly larger, as reflected in leaves.

2. Flowering in (late December) January through early March.

3. Flowers become campanulate with tepals recurved distally.

4. Flowers become less fragrant (nearly odorless).

5. Tepals usually become narrowly oblong-elliptic.

6. Ovary sometimes becomes (nearly) sessile (due to abbreviation of short gynophore or gynophore-like floral axis).

18) Immediate ancestral lineage common to lineages 20 and 21.

1. Racemes become slightly more compact.

2. Proximal submarginal ridges of tepal become more closely juxtaposed basally with those of adjoining tepals.

19) Lineage of Helonias umbellata .

1. Inflorescence usually becomes (sub)umbellate.

2. Proximal submarginal ridges of tepal sometimes become minutely connate basally to those of adjoining tepals.

3. Ovary sometimes becomes (almost) sessile (due to abbreviation of short gynophore or gynophore-like floral axis).

20) Immediate ancestral lineage common to lineages 22 and 23.

1.?Apiculus at leaf apex becomes moderate.

2. Flowers (per scape) tend to become fewer.

3. Flowers tend to become less fragrant or odorless.

4. Proximal submarginal ridges of tepal become lamellate (winged) and directed inward.

5. Proximal submarginal wings (lamellae) of tepal become connate basally to those of adjoining tepals.

6. Proximal submarginal wings of tepal become adnate proximally to opposing filament, forming sheathing nectary.

7. Anthers often become affixed (to filament) slightly above base of connective (i.e. (sub)dorsi-basifixed).

8. Anthers tend to become slightly longer.

9. Traces of apical confluence between thecae tend to become slightly less distinct.

10. Ovary becomes perfectly sessile.

21) Lineage of Helonias koreana .

1. Leaf blades become slightly thinner (in texture).

2. Leaf blades become nearly dull.

3. Filaments become slightly dilated toward base.

4. Filaments become more complanate and often subancipital (two-edged or narrowly winged) toward base.

22) Immediate ancestral lineage common to lineages 23 and 24

1. Basal adnation between proximal submarginal wings of tepal and opposing filament becomes more advanced (viz. adnate portion becomes longer).

23) Lineage of Helonias orientalis .

1. Leaves become somewhat firmer (thicker) in texture.

2. Proximal submarginal wings of tepal become relatively longer.

3. Basal adnation between proximal submarginal wings of tepal and opposing filament becomes slightly more advanced (viz. adnate portion becomes longer).

24) Lineage of Helonias breviscapa .

1. Basal abaxial gibbosity of tepal often becomes less conspicuous.

2. Nectary at adaxial base of tepal becomes relatively higher in position (surface of nectary becomes nearly as high as base of ovary or top of receptacle).

3. Traces of apical confluence between thecae often become indistinct.

5. Historical background of the current geographic ranges

The distributions of the sections of Helonias are remarkably disjunct. Helonias bullata is restricted to eastern North America ( Figs. 6 , 31 ), while H. sect. Heloniopsis is restricted to eastern Asia ( Figs. 31 , 32 ). The main factor behind this large scale disjunction may have been drastic climatic change. According to paleobotanical surveys, the so-called Arcto-Tertiary Geoflora, which comprises many species of deciduous broad-leaved trees, once extensively covered northern circumpolar regions ( Chaney 1947, Tanai 1967, 1972, 1988, 1992, Uemura 1995, Ogasawara & Uemura 2006). The flora began to migrate southwards in response to lowering temperatures toward the end of the Eocene and early Oligocene. Ancestral plants of Helonias , which are presumed to have been members of the Geoflora, may also have migrated southward and in the process may have separated into two groups, one reaching Asia and the other North America ( Fig. 31 ) ( Tanaka 1997e). Helonias bullata ( Figs. 4 , 5 ) of North America appears to be the most primitive, since its three styles tend to be largely free ( Fig. 5D , Part III-3). This remarkable disjunction in the range of Helonias appears to have originated at an early stage of diversification ( Fig. 30 ; Tanaka 1997e) before the existence of many of the current species of Helonias (most species of H. sect. Heloniopsis such as H. parviflora , H. thibetica , H. umbellata , and H. orientalis ).

Of the Asian members of Helonias (H. sect. Heloniopsis ), H. yunnanensis var. yunnanensis ( Figs. 7 , 15-Yy) appears to be the most primitive ( Fig. 30 ), since it has the shortest style ( Fig. 7B , Part III-3; Tanaka 1997c, e). Presumably, the ancestral plants of this Helonias yunnanensis migrated from area at high latitudes (encircled by broken line in Fig. 31 ) to somewhere in or around the Tibetan Plateau and the Himalaya of today ( Figs. 31 , 32 ). After having settled there, they probably underwent gradual uplift caused by the subduction of the so-called Indian Plate (Indo-Australian Plate) under the Eurasian Plate. The ancestors of H. yunnanensis var. yunnanensis must have gradually adapted to alpine or subalpine environments created by the orogenesis of that region. This variety is now confined to the highlands between ca. 2700 and 4300 m (Fig. 15-Yy). Plants in such harsh alpine situations have inevitably become smaller and mostly correspond to Ypsilandra yunnanensis var. micrantha (or var. himalaica ). Helonias alpina ( Figs. 10 , 15-A; elev. 3962–4267 m) may also have differentiated in the highlands. Some ancestors of H. yunnanensis var. yunnanensis in the eastern part of the plateau may have evolved species such as H. jinpingensis now on the border between southern Yunnan and northern Vietnam (Fig. 15-J) and H. parviflora in Guizhou ( China) (Fig. 15-P). The ancestor of H. parviflora is likely to have branched off the lineage of H. thibetica which is now widespread over the eastern stretch or periphery of the Himalaya and Tibetan Plateau (Figs. 15-T, 30, 32). Ancestral plants of H. ser. Umbellatae (subsect. Heloniopsis) , whose descendants are now in Taiwan and the Nansei Islands (including the Ryukyus) in Japan ( Figs. 29 -Ka, -L, -U, 31, 32), may have originated from the ancestor of H. thibetica (Figs. 15-T, 30) which was once in the Far East maritime regions (including today’s southern China, Taiwan, the Nansei Islands, and lands subsided under the Taiwan Strait and East China Sea).

Thus, the geographic range of ancestral Asian Helonias after settlement in or around the present Tibetan Plateau and the Himalayan regions is presumed to have extended eastward over time and through evolutionary progression ( Figs. 30 , 32-B, -C ; Tanaka 1997e). Li (1944) recognized 14 phytogeographic regions in China. If his regional divisions are adopted, a presumable approximate course of range extension of ancestral Asian Helonias (H. subsect. Ypsilandra and probably H. ser. Umbellatae in part) would be:―Tibetan Highland Region (14) → Sino-Himalayan Region (4) → Southwestern China Plateau Region (3) → Southern China Maritime Region (1) (number in parentheses assigned by Li, 1944).

During warmer geological periods the ancestors of Helonias ser. Umbellatae (or of H. umbellata ; Figs. 29 , 31-3 , 32-3 ) are supposed to have extended their range to somewhere in or around today’s Japan and Korea ( Fig. 32-D ). After the climate cooled again, some may have migrated south, while others may have remained to form the ancestral lineage of H. ser. Heloniopsis ( Figs. 29 , 30 , 31-4 , 32-4 ).

The approximate course of migration or extension of geographic range of Helonias traced from this study is outlined in Fig. 33 . Infrageneric taxa, such as H. subsect. Ypsilandra and H. ser. Umbellatae , have their own geographical ranges disjunct from one another ( Figs. 29 , 31 , 32 ), and the largest scale disjunction between the two sections ( Helonias and Heloniopsis ) appears to reflect not only the most drastic climatic change in the evolutionary history of Helonias but also the deepest diversification in the genus.

Fuse & Tamura (2004) suggested that Heloniopsis as a remnant of the Arcto-Tertiary flora has migrated from the north to the present range (via Sakhalin in case of species distributed in Japan and Taiwan). However, no remarks were made on the migration route of Ypsilandra ( Helonias subsect. Ypsilandra ) and the geological age and palaeogeological states of eastern Asia when the migration had occurred. It is hard to accept their view, considering the process of phylogenetic progression in Helonias s.lat. as traced from the present study ( Figs. 30–33 , List 2).

The three species of Helonias ser. Heloniopsis , H. koreana , H. orientalis and H. breviscapa , appear to be adapted to different climates. Helonias orientalis ( Fig. 29-O ) in Japan and southern Sakhalin, Russia, tends to be more abundant in snowy regions, such as along the coast of Honshû facing the Sea of Japan (see Japan Meteorological Agency 1971, 1972, for climatological data). Helonias breviscapa ( Fig. 29-B ), which is confined to southwestern Japan mainly facing the Pacific, appears to prefer a somewhat warmer climate with less snowfall in winter ( Tanaka 1998a). Helonias koreana ( Fig. 29 -Ko), endemic to the Korean Peninsula, appears to be adapted to a bitter cold, drier, and less snowy winter (see Central Meteorological Observatory, Tokyo 1929).

Plants, such as Helonias orientalis and H. koreana , that occur in very cold regions may be protected from coldness and dryness by being covered by snow. The three different types of climate appear to be closely related to the geographic features of the respective regions. It is generally accepted that the following three factors are prerequisite for creating such different climatic types: a) high atmospheric pressure develops over the Siberian region in winter, resulting in strong seasonal wind toward Japan; b) the Sea of Japan between the eastern Asian mainland and the Japanese archipelago provides moisture to the dry air mass blowing from the Siberian region; c) the high mountains in Honshû, Japan obstruct the northwesterly wind, creating two markedly contrasting climatic types in winter ( Uemura 2011).

The three species of Helonias ser. Heloniopsis may be closely related to such geographic and climatic features. These features appear to have become remarkable especially from the mid-Pleistocene onward (e.g. maps 30- 27–30 in Minato et al. 1965 for the process of palaeogeographical changes in eastern Asia). If the timing of establishment of these features (or the above three factors) becomes more precise, the approximate time of origin of the three species may also become clearer.

Because of fluctuating temperatures in the Neogene period of the Tertiary and in the Quaternary ( Minato et al. 1965, Tanai 1972, 1992, Uemura 1995, Ogasawara & Uemura 2006), some north-southward migration of vegetation, including Helonias , must have occurred. The occurrence of H. orientalis in southern Sakhalin, Russia ( Miyabe & Kudo 1932, Sugawara 1937, 1939), which is at the northernmost limit of its range ( Fig. 29 ), may have resulted from such migrations during the Quaternary. Despite such migrations, the relative geographic ranges of the species of Helonias may not have changed extensively.

Helonias are small hemicryptophytes with basal rosulate leaves spreading on the ground. They prefer moist or wet situations, such as swamps, meadows or steep rocky slopes along streams in forests, that are not necessarily so heavily covered by larger plants. In general, these habitats are more exposed than closed, dense forest floors, and are hence more likely to soon dry if water becomes scarce. Ample precipitation may therefore be required to maintain stable populations.

The main factors for the eastward migration in Asia of Helonias sect. Heloniopsis ( Fig. 32-B–D ) may have been ample precipitation and moderate temperatures.Asian Helonias appears to be more abundant and diversified in regions blessed with such climatic factors, e.g., maritime regions of the Far East including Japan and Taiwan, and the Himalaya and Tibetan Plateau ( Fig. 32 , Table 10; Yan 2002 for climatological data for China). Eastern North America, where H. bullata occurs (e.g. Figs. 6 , 31 ), resembles eastern Asia in climate, especially in precipitation and temperature (e.g. plates 20, 24, 26 in Good 1974).

Figures

FIGURE 1. Buds and their sprouting in Helonias. A. H. bullata (material Bu-1; photo on 5 April 2013). B. H. orientalis (O-3; 15 November 2014). C, D. H. thibetica (T-1; C on 19 February 2014, D on 2 March 2014). Flower buds or fresh flowering stem designated by F, leaf buds or sprouting leaves by L, rosulate leaves developed in previous years by R. In Fig. C, two of leaves developed in the preceding year marked with single white circle (dot); two of leaves developed the year before last marked with paired white circles (dots). Photo A by Jim Fowler at site of “Bu-1” in South Carolina; B–D by the author at Hachioji, Tokyo.

FIGURE 2. Diagram of phenology of rosette leaves and flowering stems (scapes) in Helonias. Phenological transition of rosette leaves (L) and flowering stem (F) in their lifetime (from bud formation to death) is schematized.Approximate magnitude of growth rate of two organs is expressed by line or shape of ellipse or lance (expanded portion). State of organs showing static, increasing or decreasing growth rate is represented respectively by line, or by expanding or narrowing (closing) portion of an ellipse or lance. Broken line represents period during which older leaves die, although their death is usually concentrated in growing season (April to July or August). In H. bullata, for example, leaf bud (see L-row) is initially formed in summer of year 0, it stays dormant until coming spring, and then develops rapidly in spring to summer (expanded open portion) of year 1. Mature leaves wither in growing season of following year (broken line in year 2). Flower bud of H. bullata (see F-row) is initially formed in fresh rosette (in L-row) in summer of year 1; like leaf bud it stays dormant until next spring, and then develops rapidly in spring (expanded shaded portion) of year 2. Flowering stem dies around summer of same year (closing shaded portion). Leaf bud (see L-row) of H. kawanoi, H. leucantha or H. umbellata after formed soon starts to sprout in late summer onwards (of year 0), although its growth appears more or less suppressed in subsequent cooler seasons (*). Phenological progression of flowering stem of H. kawanoi (F-row) tends to be lagged (**) when cultivated under lower temperature (in Tokyo) than in natural habitats.

FIGURE 3. Young slightly open flowers of Helonias thibetica (A–C; material T-1) and H. umbellata (D, E; U-1), showing protogyny. A. Flowers with precociously protruding pistil. B, D. Flowers similar in stage to A with frontal tepals removed to show indehiscent anthers. C, E. Closeup of densely papillulate mature stigma from flower in B and D, respectively.

FIGURE 4. Helonias bullata (material Bu-1; photos A–E on 28 April 2014, F on 13 June 2002). A. Habit and boggy habitat. B. Young opening flowers with indehiscent anthers. C, D. Young flowers visited by a Bombus species sucking nectar.E. Flowers visited by a halictid bee. F. Fully dehisced, ascending capsules. All photos taken by Jim Fowler.

FIGURE 5. Helonias bullata (A–E; material Bu-2). A. Young flower with indehiscent anthers. B. Anthers seen from above. Three outer anthers dehisced earlier than three inner ones of which one marked with IS. C. Proximal interior of partial flower, showing nectar (n) secreted at adaxial bases of tepals. D. Pistil showing basal connation (*) among three styles. E. Proximal portion of flower in vertical section. IF; inner filament. OF; outer filament. F. Seeds (Bot. Gard. Harvard Univ., year 1879, K). Photos A, C, E on 21 May 1996, B on 22 May 1996, D on 28 May 1996, all taken at Hachioji, Tokyo.

FIGURE 6. Geographic range (dotted areas) of Helonias bullata in eastern North America (Data based principally on Utech 1978).

FIGURE 7. Helonias yunnanensis var. yunnanensis. A. Habit and habitat (Y-1; photo on 24 May 2014). B. Closeup of inflorescence (Y-1 on 24 May 2014). C–E. Isolectotype (G. Forrest 12055, E-00115522). C. Habit. D, E. Closeup of inflorescence. F. Part of infructescence with dehisced capsules (G. Forrest 14961, E-00115516). G. Seeds (Gaoligongshan Biodiversity Survey 27019, GH-00293355). Photos A & B by Yang Niu.

FIGURE 9. Helonias yunnanensis var. mesostyla. A. Flower with frontal tepal and stamen removed.B. Pistil.C. Fruit with persistent floral parts. One frontal tepal removed. D. Two seeds. A, B from N Myanmar (Kermode 17139, holotype, K-001235138). C, D from Yunnan, China (Gaoligongshan Biodiversity Survey 32015, GH-00292433). Scale on right corner for B and D. Drawn by Noriyuki Tanaka.

FIGURE 10. Helonias alpina from SE Tibet (F. Kingdon-Ward 7084). A, B. Habit. C–E. Closeup of inflorescence. A–D: Holotype (K- 000400242*). E: Isotype (E-00115520). Stigmas arrowed in E.

FIGURE 11. Helonias parviflora from China (J. Esquirol 2013, isolectotype, E-00115519). A. Habit. B, C. Closeup of inflorescence.

FIGURE 12. Helonias parviflora (S.W. Teng 90072, A). A. Pedicellate flower with frontal tepal and filament removed. B. Pistil. Drawn by Noriyuki Tanaka.

FIGURE 13. Helonias thibetica (material T-1). A. Young, slightly open flowers with protruding stigma (photo: 13 February 2014). B. Young flowers with anthers not yet dehiscent (19 February 2014). C. Flowers with dehiscent anthers and tepals turning creamy yellow (23 February 2014). D. Ripe fruits (5 April 2014). E. Same infructescence as D with dehiscing capsules exposing fertile seeds set by artificial selfing (3 May 2014). F. Rosette mostly of fresh leaves with young bud in center (14 August 2013). All photos taken at Hachioji, Tokyo.

FIGURE 14. Helonias thibetica (material T-1). A. Flower. B. Proximal part of flower with nectar (n) secreted from adaxial bases of tepals. Two frontal tepals removed. C. Vertical section of flower. D. Proximal interior of partial flower. E. Two anthers showing adaxial side (left) and abaxial side (right), respectively. F. Vertical section of capsule with persistent floral parts. IF; inner filament. OF; outer filament. n; nectar. Scale at C also for D.

FIGURE 16. Helonias kawanoi (material Ka-3). A–C; one and same plant. A. Flowering plants with sprouting fresh leaves (arrowed) (photo: 3 December 2014). B. Umbellate flowers (4 December 2014). C. Ascending flowers after anthesis (19 December 2014). D, E. Rosettes with sprouting leaves (arrowed) and flowering stems (D on 15 November 2014; E on 19 December 2014). All photos taken at Hachioji, Tokyo.

FIGURE 17. Helonias kawanoi (A, B, E: material Ka-3. C, D, F: material Ka-1). A. Young slightly open flower with anthers not yet dehiscent. Three frontal tepals removed. B. Closeup of densely papillulate stigma (st) of same flower as A. C. Flower with frontal tepal and stamen removed. D. Interior of partial flower. E. Vertical section of flower. F. Dehisced anther with apical confluence between thecae (arrowed), side view. IF; inner filament. OF; outer filament.

FIGURE 18. Helonias leucantha. A, B, E–G: material L-4. C, D: L-2. A. Flowering plant (photo on 24 January 2015). B. Raceme from plant in A (24 January 2015). C. Young slightly open flowers with protruding stigmas (21 January 2013). D. Raceme of pale purplish pink flowers (3 February 2013). E. Infructescence with dehiscing capsules (30 April 2012). F. Rosette with flower bud (long arrow) and sprouting small fresh leaves (short arrow) (19 December 2014). G. Plant with fresh green leaves and yellowish leaves developed in preceding year (arrowed) (14 August 2014).All photos at Hachioji, Tokyo.

FIGURE 19. Helonias leucantha. A. Flower (material L-1). B. Proximal interior of flower with frontal tepals and stamens removed (L- 3). C. Vertical section of flower (L-1). D. Interior of partial flower (L-1). E. Proximal interior of partial flower (L-2). IF; inner filament. Scale at B also for C.

FIGURE 20. Helonias leucantha. A. Proximal part of flower, cross section (L-2). B. Proximal part of flower with ovary removed, cross section (L-2). C. Indehiscent anthers with rudimentary apical confluence between thecae (arrowed) (L-2). D. Distal part of pistil and dehisced anthers with rudimentary apical confluence between thecae (arrowed) (L-2). E. Dehiscing capsule with persistent floral parts (L-4). F. Seeds (L-4). OF; outer filament. OVB; base of ovary. Scale at A also for C and D.

FIGURE 21. Helonias umbellata. A. Young slightly open flowers with protruding pistils (material U-1; photo on 3 March 1989). B. Flowering plant (U-2; 14 March 1989). C. Umbel (U-1; 30 March 1992). D. Plant with fresh leaves (light green) and leaves developed in preceding year (darker green) grown in greenhouse during winter (U-3; 14 March 2015). All photos at Hachioji, Tokyo.

FIGURE 22. Helonias umbellata. A–E: material U-1. F: U-4 (in spirit). A. Flower with two frontal tepals and stamens removed. B. Closeup of proximal interior of flower. C. Vertical section of flower with ovary shortly stipitate at base. D. Proximal interior of partial flower. Minutely connate portions between adjoining tepals arrowed. E. Proximal part of flower in cross section. F. Distal part of flower with anthers showing apical confluence between thecae (arrowed). Scale at B also for C–E.

FIGURE 23. Helonias koreana.A–F: One and same umbel showing phenological transition of flowers (material Ko-2). A. Young flowers mostly with indehiscent anthers (photo on 8 March 2015). B. Flowers mostly with dehisced anthers at early to mid anthesis (9 March 2015). C. Flowers becoming nodding at mid to late anthesis (12 March 2015). D. Nodding flowers at late anthesis (14 March 2015). E. Nodding flowers after anthesis with persistent floral parts (26 March 2015). F. Slightly ascending young fruits (19 April 2015). G. Short raceme of white flowers at late anthesis (Ko-w-1; 15 April 2008). H. Fresh rosulate leaves minutely undulate along margins (Ko-2; 23 May 2015). All photos at Hachioji, Tokyo.

FIGURE 24. Helonias koreana. A–F: material Ko-1. A. Flower at late anthesis. B. Vertical section of flower at late anthesis. C. Proximal interior of flower, showing connate portions between adjoining tepals (long arrows) and adnate portion between tepal and opposing filament (short arrow). D. Perianth cut and opened, showing tepals connate basally by proximal submarginal lamellae. E. Proximal part of flower in cross section. Two larger arrows point connate portions between adjoining tepals, and two smaller arrows indicate margins of tepal. F. Stigma (st) and adaxial side of anther (in spirit). Portion of anther affixed to filament indicated with ‘F’. Thecal connation below insertion point of filament indicated with arrow. F; filament. IF; inner filament. OF; outer filament. OVB; basal inside of ovary. Scale at B also for C, D and F.

FIGURE 25. Helonias orientalis (A–D, F; material O-2. G; O-1. H; O-3) and white flowered form (E; O-w-1). A. Young slightly open flowers with protruding pistil (photo: 25 March 2014). B, C, D. Sub-umbellate flowers (B on 31 March 2014; C on 29 March 2014; D on 5 April 2012). E. Compact raceme of white flowers (30 March 2012). F. Infructescence (29 April 2014). G. Dehisced capsules (14 May 2014). H. Rosette with flower bud (arrow) in center (14 August 2014). All photos at Hachioji, Tokyo.

FIGURE 26. Helonias orientalis. A–C; material O-3. D, E; O-2. A. Proximal interior of partial flower. Connate portion between adjoining tepals arrowed.Adnate portions between tepals and opposing filaments marked with asterisks (*). B. Proximal portion of flower in vertical section. Surface of nectary arrowed. IF; inner filament. C. Proximal part of flower in cross section. D. Slightly dehisced capsule with persistent floral parts. E. Three valvate, dehisced capsule. Scale at A also for C; at D also for E.

FIGURE 27. Helonias breviscapa. A–D. Inflorescence and rosette turned brown in winter. A; material from Kyûshû Br-4 (Photo: 29 March 2014). B; Shikoku Br-3 (22 March 2014). C; Honshû Br-2 (19 March 2014). D; Honshû Br-1 (24 March 2014). E. Ripe fruits (Br-2; 12 May 2012). F. Dehiscing capsules (Br-2; 2 May 2014). G. Fresh rosulate leaves with minutely undulate margins (Br-1; 14 Aug. 2013). All photos at Hachioji, Tokyo.

FIGURE 28. Helonias breviscapa. A. Flower (material Br-5). B, C. Vertical section of flower (B; Br-5. C; Br-3). Surface of nectary arrowed. D. Proximal exterior of flower, side view (Br-1). E. Flower with pistil removed, front view (Br-2). Two connate portions between submarginal lamellae of adjoining tepals arrowed. F. Bilocular anthers with no apical confluence between thecae arrowed (Br-2). IF: inner filament. OF: outer filament.

FIGURE 30. Phylogram of 12 species of Helonias constructed from analyses of phenotypical characters. Each lineage is numbered 1 to 24. Infrageneric categories, A to C, are shown as vertical lines on right corner. Character states regarded as apomorphies acquired by respective lineages are enumerated in List 2.

FIGURE 31. Geographic ranges of two sections Helonias and Heloniopsis. Ancestral plants of Helonias are presumed to have been in northern high latitudes approximate area of which is encircled with broken line.They are supposed to have been separated into two groups, and eventually one group reached eastern N. America and the other eastern Asia as consequence of their southward migrations (A). ① Sect. Helonias. ②–④ Sect. Heloniopsis. ② Subsect. Ypsilandra. ③ Subsect. Heloniopsis ser. Umbellatae. ④ Subsect. Heloniopsis ser. Heloniopsis. For historical aspect of range extension, see also Figs. 32, 33 and text (Part III).

FIGURE 32. Geographic ranges of Sect. Heloniopsis in Asia with presumable approximate course of range extension in past. A–D: Presumable approximate course of migration or extension of range of ancestral plants of Helonias. Ancestral plants are supposed to have arrived in or around present Tibetan Plateau from northern high latitudes (A; see also Fig. 31) and have further extended their range eastward (B, C) and northeastward (D).

FIGURE 33. Flowchart illustrating presumable approximate course of migration of ancestral population of Helonias (cf. Figs. 31 & 32). A. Southward migration from northern high latitudes, which resulted in large-scale disjunction in distribution. B, C. Eastward extension of range. D. Northeastward extension of range.

FIGURE29.Distributionofsixspeciesbelongingtotwoseriesofsubsect.HeloniopsisinEAsia.B:Heloniasbreviscapa.Ka:H.kawanoi.Ko: H.koreana.L:H.leucantha.O:H.orientalis.U:H.umbellata.Ser.UmbellataecomprisesKa,LandU.Ser.HeloniopsisconsistsofB,KoandO.