Evolutionary dynamics and biogeography of Musaceae reveal a correlation between the diversification of the banana family and the geological and climatic history of Southeast Asia

Abstract

Tropical Southeast Asia, which harbors most of the Musaceae biodiversity, is one of the most species-rich regions in the world. Its high degree of endemism is shaped by the region's tectonic and climatic history, with large differences between northern Indo-Burma and the Malayan Archipelago. Here, we aim to find a link between the diversification and biogeography of Musaceae and geological history of the Southeast Asian subcontinent. The Musaceae family (including five Ensete, 45 Musa and one Musella species) was dated using a large phylogenetic framework encompassing 163 species from all Zingiberales families. Evolutionary patterns within Musaceae were inferred using ancestral area reconstruction and diversification rate analyses. All three Musaceae genera - Ensete, Musa and Musella - originated in northern Indo-Burma during the early Eocene. Musa species dispersed from 'northwest to southeast' into Southeast Asia with only few back-dispersals towards northern Indo-Burma. Musaceae colonization events of the Malayan Archipelago subcontinent are clearly linked to the geological and climatic history of the region. Musa species were only able to colonize the region east of Wallace's line after the availability of emergent land from the late Miocene onwards.

Keywords: Ensete; Musa; Musella; Southeast Asia; ancestral area analysis; dispersal; diversification; historical biogeography.

Figure 1

Maximum clade credibility tree of Musaceae (detail of the large Zingiberales phylogram in Supporting Information Fig. S1). Ancestral area reconstructions (AARs) with the highest likelihood values are shown as boxes at each node. A single box refers to a specific distribution range, whereas multiple boxes depicted either above or below the branches indicate alternative AARs. In the case of low likelihood values, more than one ancestral area is shown. The following abbreviations are used: A, Africa; B, Southwest India and Sri Lanka; C, northern Indo‐Burma; D, South China; E, southern Indo‐Burma; F, Sumatra and Malayan Peninsula; G, Borneo; H, Philippines; I, New Guinea and surrounding islands; J, Northwest Australia; K, Lesser Sunda Islands; L, Sulawesi; Pl., Pliocene; P., Pleistocene. Lagrange provides two ranges per node; in cases in which only one range is present at a certain node, both lineages inherited the same ancestral distribution range. ‘All nodes =>’ above a branch indicates that all nodes of this clade are characterized by the same ancestral area.

Figure 2

Diversification plots. (a) Semi‐logarithmic lineage through time (LTT) plots of Ensete–Musella and Musa. The solid black lines represent the mean LTT plots of the empirical analysis, and the dashed black lines represent the upper and lower boundaries of the 95% confidence intervals. Simulated LTT plots (under pure birth) with 95% confidence intervals are indicated in gray (mean value represented by dashed gray line). (b) Net diversification rates through time under a Yule process are shown as solid black lines. 95% highest posterior density intervals are indicated in gray. Ma, million years ago.

Figure 3

Overall net diversification of Ensete–Musella and Musa as calculated with Bayesrate. Ninety‐five percent highest posterior density for Ensete–Musella and Musa are depicted in dark gray and light gray, respectively.

Figure 4

Diversification patterns in Musaceae. (a) Phylorate plot with estimates of net diversification rates of the Musaceae phylogenetic tree obtained from the Bayesian analysis of macroevolutionary mixtures (BAMM) analyses. Colors at each time along the branches indicate net diversification rates. Arrows indicate shifts in diversification rate based on shifts in marginal probability along the phylogram. (b) Macroevolutionary cohort matrix for speciation in Musaceae. Every cell in the matrix is coded by a color indicating the pairwise probability between two lineages and their common macroevolutionary rate regime. Dark red indicates a pairwise probability of 1, whereas a deep blue color marks a pairwise probability of shared macroevolutionary dynamics of 0. In total, three major cohorts could be identified representing a different rate regime for each Musaceae genus. In addition, within each genus, rate dynamics are highly correlated.

Figure 5

Posterior estimates of speciation and extinction rates, in blue and orange, respectively, associated with the area of distribution of Musa (northern Indo‐Burma vs Malesia). Speciation rates were defined a priori to be equal (Supporting Information Table S4). White bars fall out of the 95% confidence interval. The northern Indo‐Burmese region is indicated in black, whereas Malesia is indicated in gray.

Figure 6

Tertiary maps of Southeast Asian paleogeography and land availability. (a) Early Miocene (30 million yr ago, Ma). (b) Middle Miocene (20 Ma). (c) Late Miocene (10 Ma). (d) Pliocene (5 Ma). Dark black lines show the dispersal patterns of Musa along Southeast Asia reflecting a qualitative and generalized interpretation of Fig. 2. The arrow indicates the direction of dispersal. Spiral arrow indicates in situ diversification. Aust., Australia; Bor., Borneo; Jav., Java; LSI, Lesser Sunda Islands; N Gui., New Guinea; Phi., Philippines; Sul., Sulawesi; Sum., Sumatra.