Zingiberales

The apomorphies (derived characteristics common to a taxonomic group) are considered to be specialised isomorphic root hair cells, penni-parallel leaf venation, supervolute ptyxis (left and right halves of immature leaf lamina rolled into each other), diaphragmed air chambers in leaves and stem, presence of intracellular silica bodies, epigynous flowers and an inferior ovary, pollen grains without distinctive aperture but with a reduced exine layer and an elaborated intine layer, nuclear endosperm development, and arillate seeds.[18][19][20]

The Zingiberales have always been considered a unique and coherent (monophyletic) group, although accounting for <4% of extant monocots, which has led some authors to suggest they should constitute a higher taxonomic rank than order.[20] For a brief history of the taxonomy of this order, see Scitamineae, and Kress 1990.[16] They were first described by August Grisebach, their botanical authority, in 1854 as Zingiberides, an order of monocotyledons, subdivided into two families, Scitamineae and Musaceae.[2]

Based on morphological grounds alone, early systems, such as Bentham and Hooker (1883) placed the Scitamineae as an Ordo (family) of the Epigynae alliance in the monocotyledons, incorporating both of Grisebach's families.[22] Later systems such as the Engler system (1903)[23] and the Wettstein system (1924),[24] also considered Scitamineae as a monocotyledon order and were influential for a long period of time. Variants included Scitaminales (Warming 1912).[25] Hutchinson (1926), although initially using Scitamineae, later followed Takenoshin Nakai (1930).[26][27] in adopting Zingiberales as the name for the order (6 families) in Division Calyciferae,[28] although credit is generally given to Nakai. This usage was followed by Takhtajan (1966) within superorder Lilianae[29] and by Dahlgren (1985) in its own superorder Zingiberiflorae.[21]

In contrast the Cronquist system retained Scitamineae as the name for this order with eight families, but organised the order in the subclass Zingiberidae of the class Liliopsida (monocotyledons).

Using molecular phylogenetics, which was first applied to the order in 1993,[30] the Angiosperm Phylogeny Group (APG) system (1998),[4] (which generally followed Dahlgren, but with less divisions) confirmed the position of Zingiberales as a monophyletic order within the monocots, placing it in the commelinoid clade, as sister group to Commelinales, which Dahlgren had treated within a separate superorder. This was an ordinal system that did not examine subordinal structure. The 2003 revision (APG II) changed commelinoid to commelinid, but not the relationships, [5] and this remained unchanged in the subsequent 2009 APG III system[31] and 2016 APG IV system without addressing interfamilial relationships.[32]

The order, which now has more than 2,600 species, distributed in 68 genera over eight families, has been subdivided from early times. In the Bentham & Hooker system (1883), their Ordo Scitamineae had four tribes: Zingibereae, Maranteae, Canneae, and Museae. These have become progressively divided to form the modern phyletic classification into the following monophyletic families: Zingiberaceae (gingers), Musaceae (bananas), Heliconiaceae (heliconias), Strelitziaceae (bird-of-paradise), Costaceae (spiral gingers), Cannaceae (canna lilies), Marantaceae (prayer plants), and Lowiaceae (Orchidantha).[6][20] The APG II system (2003) provided a classification of families for the first time, retaining Kress's eight families.[5]

Families (genera/species)[33]

• order Zingiberales Griseb.
  • family Cannaceae Juss. (1/10 Canna cannas)
  • family Costaceae Nakai (7/143 e.g. Costus spiral gingers)
  • family Heliconiaceae Vines (1/194 Heliconia heliconias)
  • family Lowiaceae Ridl. (1/18 Orchidantha)
  • family Marantaceae R.Br. (29/570 e.g. Maranta prayer plants)
  • family Musaceae Juss. (3/91 e.g. Musa bananas)
  • family Strelitziaceae Hutch. (3/7 e.g. Strelitzia birds of paradise)
  • family Zingiberaceae Martinov (50/1,600 e.g. Zingiber gingers)

Families of Zingiberales

Canna coccinea
(Cannaceae)

Tapeinochilos ananassae
(Costaceae)

Heliconia latispatha
(Heliconiaceae)

Orchidantha maxillarioides
(Lowiaceae)

Maranta leuconeura
(Marantaceae)

Musa rosea
(Musaceae)

Strelitzia reginae
(Strelitziaceae)

Etlingera elatior
(Zingiberaceae)

Based on morphology alone, the Zingiberales have been considered to form two main groups, each with four families, utilising the number of fertile stamens;

Banana-families

• Musaceae, Strelitziaceae, Lowiaceae, Heliconiaceae. A paraphyletic basal assemblage with 5 or (rarely) 6 fertile stamens at maturity, arranged in as trimerous inner and outer whorls. In those with five stamina, the sixth may regress and be absent (Strelitziaceae and Lowiaceae, some Musaceae) or develop as an infertile staminode (Heliconiaceae, some Musaceae). Petals and stamens are often fused at the base to form a floral tube. These are known as the banana-families or the bananas on the basis of large banana-like leaves. For this reason these four families were previously all included in Musaceae, but the exact relationship between them remains some what uncertain;[8][11][20]

Ginger-families

• Zingiberaceae, Costaceae, Cannaceae, Marantaceae (the gingers). A monophyletic derived terminal clade with the number of fertile stamens reduced to one (Zingiberaceae, Costaceae) or to one half, with a single theca (Cannaceae, Marantaceae). The remaining components of the androecium develop as four or five elaborate petaloid staminodia, highly modified from sterile stamens. This group may have one (Cannaceae, Marantaceae) or two (Zingiberaceae, Costaceae) anther pollen sacs. The infertile stamina are homologous with the fertile stamina in the bananas and other monocots) but assume the structure and function of petals as pollinator attraction. This group demonstrate complex patterns of fusion among their floral organs including the staminodes. In Zingiberaceae and Costaceae the staminodes fuse to form a staminodial labellum which provides much of the floral display. In general the flowers of this group display higher degrees of organ fusion and specialisation.[8][11][20]

Using combined morphology and molecular data, Kress and colleagues (1993, 1995, 2001) confirmed the broad separation into two clades based on morphology alone, and produced an infraordinal structure.[20][30][34] In this scheme, they divided the families of the order as follows, with the ginger group as one suborder, and the banana group divided amongst three separate suborders:[35]

Suborder Zingiberineae Kress ("gingers"; 2 superfamilies)

• Superfamily Cannariae Kress
  • Cannaceae A.L. Jussieu
  • Marantaceae Petersen
• Superfamily Zingiberariae Kress
  • Costaceae Nakai
  • Zingiberaceae Lindley

Suborder Strelitziineae Kress

• • Lowiaceae Ridley
  • Strelitziaceae Hutchinson

Suborder Musineae Kress

• • Musaceae A.L. Jussieu

Suborder Heliconiineae Kress

• • Heliconiaceae Nakai

While the two sister family groups that constitute the Zingiberineae (Cladogram I) and also the basal Strelitziineae (Strelitziaceae-Lowiaceae) sister group (Cladogram II) were strongly supported, the position of Musaceae and Heliconiaceae were not. In the above model (Model 1), Musaceae appears as the first branching family, and Heliconiaceae placed as sister to the Zingiberineae (Cladogram III). Other studies placed these and the Strelitziaceae-Lowiaceae sister group in a trichotomy with the remaining families.[36] While a revision of the first model (Model 2) placed Heliconiaceae as the first branching lineage with Musaceae in a sister relationship with Strelitziineae, which in turn was sister to Zingiberineae (Cladogram IV).[37] A third model (Model 3) supports Musaceae as the basal group but places Heliconiaceae as sister to Strelitziineae (Cladogram V).[7] The failure to resolve the ancient rapid divergences of this order with multi-gene phylogenies and plastid data has important implications for understanding the evolution of characteristics.[37][38]

Finally in 2016 Sass and colleagues, using multiplexed exon capture were able to resolve the entire phylogenetic tree with high support. This confirmed the place of Musaceae as sister to the remaining families, confirming Model 3.[38]

The common ancestor of the Zingiberales together with those of its sister order, the Commelinales, is estimated to have originated 158 Mya (million years ago) in the Early Cretaceous, with separation of the two orders between 80–124 Mya, and with rapid radiation into the major lineages in the mid Cretaceous ca. 60–100 Mya and six of the eight families established by the end of the Cretaceous,[35][38] Estimates of crown group age (most recent common ancestor of the sampled species of the clade of interest) vary widely between 34 and 110 Mya, and may need revision in the light of developing knowledge of the topology of the order.[9][38]

Fossil-calibrated molecular estimates suggest a date of 110 to 80 Mya for the diversification of primary lineages.[37] If Musaceae is the stem family of the order, as seems likely this places the origin of Zingiberales ca. 124 Mya, with diversification occurring ca. 110 Mya in the middle Cretaceous. That origin (124 Mya) was congruent with the breakup of the southern land mass, Gondwana.[7]

Probably the ancestral Zingiberales were distributed in tropical Gondwanal and encompassing present-day Americas, Africa, and Southeast Asia. Within this land mass, Australia seems the most likely anestral area, with subsequent dispersals between Africa and neotropical America. Earlier studies had implied Southeast Asia as the origin.[35] The current distribution of the Zingiberales seems to be a product of numerous secondary and tertiary dispersal events between the major tropical regions of the world.[7]

Zingiberales demonstrate an evolutionary trend in the ontogeny of the perianth (sepals and petals). The appearance of a dimorphic perianth (in which petals and sepals differ in appearance) is variable throughout the commelinid monocots, with a transition from an undifferentiated monomorphic perianth to a dimorphic one occurring independently in the two sister orders, Commelinales and the Zingiberales.[12] The evolution of floral morphology within Zingiberales demonstrates a marked correlation between the reduction of the number of fertile stamens, and increased petaloidy.[7] The ancestral Zingiberales flower is thought to have had 5–6 fertile stamens, following which the staminode evolved in the lineage leading to Heliconiaceae+Zingiberineae, finally leading to 2–5 staminodia dominating the floral display.[12]

The phylogenetic diversification and biogeographic dispersal of the Zingiberales was, in part, driven by the evolutionary radiation and diversification of their associated animal pollinators, which include bats, birds, non-flying mammals and insects.[35] Six of the eight families of the Zingiberales contain taxa specialised for pollination by vertebrates, which appears to be the plesiomorphic state in the order.[35] Of these six families two are exclusively vertebrate-pollinated (Strelitziaceae, Heliconiaceae).[35] Pollination by insects also occurs in six families with one (Marantaceae) or possibly two (Lowiaceae) families predominantly specialised for insect visitors.[35]

Seed and fruit fossils of the Zingiberales appear in the Santonian of the Late Cretaceous, ca. 85 Mya, and thought to represent Musaceae and Zingiberaceae, but the place of the oldest Zingiberales fossil, Spirematospermum with its distinctive seeds remains uncertain, but is most likely Zingiberaceae.[9] The leaf fossil record for Zingiberales also extends back to the Late Cretaceous.[7] Other fossil records include rhizomes and phytoliths.[37][38]

The four families of the basal banana group exhibit less taxonomic diversity than the terminal ginger group. The three genera of Musaceae are distributed in tropical Asia and Africa, although fossil evidence reveals their presence in North America and Africa in the Tertiary, while the three genera of Strelitziaceae are allopatric (isolated from each other) being found in Madagascar, southern Africa and the Amazon Basin respectively and Lowiaceae occurs in Southeast Asia. The largest family in this group, the Heliconiaceae is primarily neotropical, but also occurs in the Pacific from Samoa to Sulawesi.[35]

Of the four Zingiberineae (gingers) families, three (Zingiberaceae, Costaceae, Marantaceae) are pantropical. The fourth, Cannaceae is restricted to the New World, although widely cultivated. This suborder contains the two largest families (Zingiberaceae and Marantaceae) and the largest number of species.[35]