Multidisciplinary perspectives on banana (Musa spp.) domestication

Abstract

Original multidisciplinary research hereby clarifies the complex geodomestication pathways that generated the vast range of banana cultivars (cvs). Genetic analyses identify the wild ancestors of modern-day cvs and elucidate several key stages of domestication for different cv groups. Archaeology and linguistics shed light on the historical roles of people in the movement and cultivation of bananas from New Guinea to West Africa during the Holocene. The historical reconstruction of domestication processes is essential for breeding programs seeking to diversify and improve banana cvs for the future.

Fig. 1.

Geographical distribution of M. balbisiana and subspecies of M. acuminata, the wild ancestors of cultivated bananas. Nuclear and cytoplasmic markers (8, 13, 15) differentiate M. acuminata wild diploids into clusters that fit with subspecies previously defined from morphological characters: banksii cluster from NG; malaccensis cluster from Malayan Peninsula; and burmannica, burmannicoides, and siamea cannot be discriminated by their nuclear genome and form a complex that covers South China, Thailand, Myanmar, Bangladesh, northeast India with sporadic populations southward to Sri Lanka. This complex is genetically closer to the malaccensis cluster than to other clusters, they are geographically overlapping, and several wild accessions from Thailand are identified as hybrids. Zebrina cluster from Java and its genome size is significantly (10%) higher (8). Its anthocyanin pathway is the most primeval (19), banksii is at an intermediate stage, and the other subspecies are at a more advanced step of evolution. Microcarpa was identified from morphological characters, isozymes, and chloroplastic genome; however, nuclear genome revealed similarities with other subspecies, particularly zebrina, instigating consideration of a zebrine/microcarpa complex. Truncata is endemic to the highlands of Peninsular Malaysia. Errans from the Philippines was given the status of a subspecies of M. acuminata (22), although only one accession has been studied. It is the only wild M. acuminata with the α-mitochondrial type, an important type found in a lot of diploid and triploid cultivars. It shares similarities with banksii nuclear genome. M. balbisiana has a more northerly distribution and, although not domesticated, it has been widely translocated for its many uses, thereby founding small free-growing populations from NG in the east to Sri Lanka in the west.

Fig. 2.

Phylogenetic relations between AA cvs and wild acuminata subspecies. NJtree on genetic dissimilarities from 22 simple sequence repeat markers, on 41 AAw and 131 AAcv (also refer to Fig. S2): M. acuminata subsp. are in color (in gray for unclassified AAw); clusters of AAcv, identified by the name of a representative accession, are in black. AAcv appeared as hybrids between M. acuminata subspecies as illustrated by the clusters from Spiral to Beram collected in PNG, the native area of subsp. banksii. If the contribution of the banksii genome was still found dominant for the first clusters, it decreased rapidly, balanced by an increasing contribution of zebrina/microcarpa genome, in parallel with an increasing heterozygosity. The frequency of banksii cytoplasmic type Vф (12) decreased to the benefit of hybrid forms Vα (Vф × IIα) or specifically to the Mala cluster, IIф (IIα × Vф). Contributions of these AAcv to triploids, as 2N donor (red arrows) and N donor (blue arrows), are illustrated for some AAA and AAB.

Fig. 3.

Ancient banana phytoliths recovered from archaeological excavations at Kuk Swamp, Papua New Guinea (SEM images, A–D), and at Nkang, Cameroon (optical images, E–H). For Kuk: (A and B) dorsal and lateral view of Eumusa seed phytolith recovered from sample 5, Kuk dated to 6,990 to 6,440 cal BP; (C) lateral view of another Eumusa seed phytolith from sample 5, Kuk; and (D) dorsal view of Eumusa seed phytolith recovered from sample 28, Kuk predating 3,000 cal BP. Morphotypes shown in A–C are specific to M. acuminata (Fig. S3 A, B and D). The morphotype with lobate margins shown in D occurs in M. acuminata (Fig. S3A) and a similar morphotype occurs in Musa schizocarpa (Fig. S3 E and G). For Nkang: (E–H) multidimensional diagnostics of Musa-type volcaniform phytolith from Pit F9, Horizon 7 at Nkang, dated to 2,750 to 2,100 cal BP; (E) small indentation on left side of crater rim; (F) rectangular base, psilate surface, eccentric cone, and continuous rim; (G) processes along the edge of the base; and (H) processes along the base.

Fig. 4.

Dendrograms and maps indicating the development and dispersal of the major banana cognate sets referred to here. Maps indicate different color-coded branches of each dendrogram; the identification of the four cognate sets was moderated by linguistically informed judgments on the likelihood of similar developments being independent. *muku (A) is restricted to areas near NG, with the center of diversity along the west, whereas the *punti terms (B) are widespread with little indication of a “homeland.” *baRat (D) is ambiguous between a homeland in the Philippines, Borneo, or on mainland SEA. *qaRutay (C) is the term with the most divergent dendrogram, with an unambiguous origin in the Philippines and many clades being attested to both the east and the west, including NG and South Asia. Likely homelands for the different terminologies are shown in yellow shading, and two locations for *qaRutay are similarly shaded for the subclade containing *kela, found in the extreme west and extreme east of the range. Phylogeographies of individual clades for the different cognate sets are presented in Fig. S5.

Fig. 5.

Genetically derived contact areas between M. acuminata subsp. at the origin of cultivated diploids and corresponding linguistic evidence. (A) The three main contact areas: north among malaccensis, microcarpa, and errans; east between errans and banksii; and south among banksii, zebrina, and microcarpa. (B) Linguistic extension for terms *muku (“1”), *qaRutay (“2”), *baRat (“3”), and their derivatives (Fig. 4).

Fig. 6.

Origins and migrations of the main triploid subgroups. Plain arrows indicate long-term prehistoric migrations of triploid cvs to Africa and Pacific islands. Gray dotted arrows indicate (i) the migrations of Mlali AAcv subgroup, which is not found in ISEA today, to mainland southeast Asia, where it contributed to AAA Cavendish, then to India, where it met M. balbisiana to give AAB Pome; and (ii) migrations of the Mlali subgroup to the East African coast. Black dotted arrows indicate the route of M. balbisiana from south China to NG over Taiwan and the Philippines, if Austronesian speakers were instrumental in the dispersal of this species.