Geography beats ecology in shaping the evolutionary story of jujube’s wild relatives

The jujube is one of the world’s oldest cultivated fruits, yet the wild genus it belongs to has quietly staged one of the tropics’ more remarkable evolutionary journeys. A new study of Ziziphus, the genus of roughly fifty species that includes the domesticated jujube, has traced how geography and ecology have alternately driven and constrained its diversification across Africa, Asia and Australasia. The research, published in Frontiers of Biogeography, offers a vivid case study of how lineages move between continents and biomes, and what traits make those moves possible.

Ziziphus is a thorny, fly-pollinated genus of trees, shrubs, lianas and geoxyles — dwarf shrubs with massive underground woody structures and minimal aerial growth. Its species occupy every major lowland tropical biome, from closed rainforest to open savanna and desert. The team, led by Jess Rickenback of the University of Edinburgh, set out to answer a deceptively simple question: when a genus spans multiple continents and biomes, which force structures its diversification more — the geography of where species live, or the ecology of the biomes they inhabit?

To find out, the researchers built the most complete phylogeny of Ziziphus to date, sampling 38 of the genus’s roughly 50 species — a coverage of 76 percent — alongside all five species of its sister genus Paliurus as an outgroup. They extracted DNA from 73 herbarium leaf samples and two silica-dried samples, sequencing the nuclear ribosomal internal transcribed spacer (ITS) region and the plastid trnL-trnF marker, both of which have proven suitable for reconstructing species-level relationships in Rhamnaceae. The combined dataset spanned 66 taxa and 1,810 nucleotide characters.

The team used maximum likelihood analyses in RAxML and Bayesian inference in MrBayes to reconstruct relationships, then employed BEAST to generate a time-calibrated phylogeny. Calibration relied on the divergence between Paliurus and Ziziphus, anchored with two fossil calibrations: the Eocene Archaeopaliurus boyacensis at 66 million years and the younger Paliurus favonii at 44 million years. Using the younger fossil, the stem age of Ziziphus was estimated at 34.4 million years, with a crown age of 27.51 million years — placing the genus’s origin in the Oligocene.

The phylogeny revealed that Ziziphus originated in closed biomes in Asia during the Oligocene, in the region of present-day Indochina, where climate and biome stability have persisted since that epoch. The ancestral area was inferred as the Indo-Pacific with 54 percent probability. From this Asian rainforest cradle, the genus staged long-distance dispersals into Africa and Arabia at roughly 23, 17 and 14 million years ago, and two separate transitions into Australia.

Crucially, the dispersals into Africa involved biome switching. One lineage colonised the expanding tropical grassy biome — the savannas — while another entered the desertic biome. These transitions coincided with the closure of the Tethys Sea between 20 and 14 million years ago, which ended an 80-million-year geographic isolation of Africa and created a land connection with Asia. The timing and location of this connection align closely with the majority of Ziziphus’s dispersals into Africa, suggesting that both geographical and ecological opportunity converged simultaneously.

The Miocene was a period of global cooling and drying driven by tectonic uplift and expanding Antarctic sea ice. This led to the expansion of C4 grasses and the formation of extensive savannas across Africa between 10 and 15 million years ago. The Ziziphus lineages that entered these new open biomes were therefore riding a wave of ecological change that was reshaping the tropics — a pattern reflected in other African genera such as Manilkara, Guibourtia and Acridocarpus.

In contrast to the African story, the Australian species showed no close relationship with their geographically nearest Asian relatives. Ziziphus quadrilocularis evolved around 17 million years ago, while Ziziphus suluensis and Ziziphus oenopolia both arose less than 5 million years ago, indicating multiple independent long-distance dispersal events from Asia. Australia was dominated by rainforest during the Oligocene with warm humid conditions continuing into the Miocene, which may have made establishment of a closed-biome species relatively straightforward. Such within-biome, across-continent dispersals are comparatively rare in Ziziphus, but they demonstrate that biome conservatism — lineages staying within their ancestral ecological setting — can operate across vast geographic distances.

The researchers quantified phylogenetic signal in geography, biome and functional traits using consistency and retention indices alongside the delta statistic. Geography scored the highest retention index at 0.72 and showed a delta statistic an order of magnitude larger than biome, confirming that at a global scale, geography structures Ziziphus’s diversification more than ecology. Biome had a retention index of 0.58, lower than geography but higher than any functional trait. This means diversification events have tended to be confined within continental-scale areas more than within particular biomes.

Among functional traits, leaf hair scored a retention index of 0.61 — higher than biome, habit or any other trait — suggesting it acts as a key synapomorphy for open and desertic clades. Hairy leaves are adaptations against herbivory and reduce water loss, and they evolved independently multiple times in lineages occupying open and desertic biomes. Spinescence, by contrast, showed a retention index of zero, indicating that while nearly all Ziziphus species are spiny, the trait provides no grouping information and unarmed species lost spines independently.

Habit showed a low consistency index but one of the highest retention indices, indicating it has changed multiple times independently while providing substantial grouping information. The ancestral habit was tree, with shrub, liana and geoxyle forms evolving more recently. Lianas dominate Ziziphus in closed biomes, where 18 of 32 closed-biome species are climbing plants adapted to use tree trunks and canopy in a quest for light. One of only two reversals back into closed biomes, at roughly 10 million years ago, was associated with a secondary evolution of the liana form.

The geoxylic habit — dwarf shrubs with massive underground woody structures — evolved only once, in the African savannas, and is the youngest habit in the genus at roughly 3 million years old. This replicates patterns seen across other geoxylic lineages, where radiations peaked around 2.3 million years ago, reflecting the rise of fire-adapted woody species in savanna ecosystems. The youngest Ziziphus species are predominantly found in open biomes, consistent with the globally young geological age of savanna.

The study demonstrates that geography and ecology are often conflated in structuring diversification, as shown in African Ziziphus. The African species form a clade united both by geography and by biome — all occupy open or arid settings. The establishment of African Ziziphus coincided with major savanna expansion and the end of Africa’s geographic separation from Asia, presenting both opportunities simultaneously. At smaller scales, biome switches associated with dispersal events structure diversification, while at the global scale, continental geography predominates.

The findings suggest that Ziziphus’s evolutionary history is one of repeated ecological opportunity seized through long-distance dispersal. The genus evolved out of closed Asian rainforests, colonised expanding African grasslands and deserts, and twice reached Australia. Hairy leaves facilitated transitions into open and desertic biomes, while the liana habit enabled a return to closed forest. The dispersal into Africa also drove the evolution of the geoxylic life form, a striking adaptation to fire-prone savanna. The researchers note that a more complete phylogeny would increase the robustness of these results, and future work should prioritise incorporating endemic New Guinean species, whose preserved specimens yielded DNA too degraded for analysis. Including more spineless species would also clarify whether spine losses are independent events or connected, allowing inferences about the evolutionary costliness of spiny resource allocation.

Subject of Research: Geography and ecology structure diversification in Ziziphus Mill. (Rhamnaceae)

Article Title: Geography and ecology structure diversification in Ziziphus Mill. ( Rhamnaceae )

Article References: Rickenback, J., Lehmann, C. E. R., Hauenschild, F., Hughes, M. J., Pezzini, F. F., & Pennington, R. T. (2024). Geography and ecology structure diversification in Ziziphus Mill. (Rhamnaceae). Frontiers of Biogeography, 17, Article e133817. https://doi.org/10.21425/fob.17.133817

Image Credits: AI Generated

DOI: 10.21425/fob.17.133817

Keywords: Geography, ecology, structure, diversification, Ziziphus, Mill, Rhamnaceae, scientific research