Somatic mutations trace the global spread and microevolution of Cavendish bananas

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Abstract

Bananas (Musa spp.) are among the earliest domesticated fruit crops, with a cultivation history spanning nearly 10,000 years. Among the hundreds of banana cultivars, the clonally propagated triploid Musa acuminata Cavendish subgroup now dominates global trade (~95%), following the mid-20th-century devastation of Gros Michel bananas by Fusarium wilt (Panama disease). Despite its global ubiquity, the origin, dissemination history, and genomic microevolution of Cavendish bananas remain poorly understood. Here, we traced the global expansion and genome evolution of Cavendish bananas using 144 whole-genome sequences from individual plants cultivated by over 18 commercial producers across 21 countries. Our collection included historical specimens from Chatsworth House (the estate of the Duke of Devonshire, the Cavendish family), where Cavendish bananas were first documented, maintaining the original lineage for ~200 years continuously. Using naturally accumulated somatic mutations as endogenous lineage barcodes, we generated high-resolution phylogenies tracing the global dissemination of Cavendish bananas. Our analysis revealed that the Chatsworth House lineage is not the most recent common ancestor of all extant Cavendish bananas, but instead is close to a major dissemination hub for non-Asian Cavendish plants, seeding independent lineages in the Canary Islands and Australia during the early 19th century. Phylogenetic dating through mutations as a molecular clock further indicated that the most recent common ancestor of Cavendish bananas was likely present in Asia around the 10th century, and that dissemination to Central and South America may have occurred prior to the establishment of the Chatsworth House lineage in the late 18th century. Finally, we identified strong signatures of positive selection on a gain-of-function allele of SLR1, a DELLA protein that represses gibberellin signaling and regulates stem elongation and stress tolerance, representing the presence of intense selective pressures imposed during two centuries of clonal cultivation. Together, our findings illuminate the mutation-driven diversification and historical spread of Cavendish bananas, the world’s most important clonally propagated fruit crop, and provide a genomic framework for understanding banana domestication, global dissemination, and recent microevolution.

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