Late Miocene origin and recent population collapse of the Malagasy savanna olive tree (<i>Noronhia lowryi</i>)

Abstract Debates regarding the origin of tropical savannas have attempted to disentangle the role of human, biotic and abiotic factors. Understanding the origins of savanna remains essential to identifying processes that gave rise to habitat mosaics, particularly those found in the Central Plateau of Madagascar. Documenting the evolutionary history and demography of native trees occurring in open habitats may reveal footprints left by past and recent environmental changes. We conducted a population genetic analysis of an endangered Malagasy shrub (Noronhia lowryi, Oleaceae) of the Central Plateau. Seventy-seven individuals were sampled from three sites and genotyped at 14 nuclear and 24 chloroplast microsatellites. We found a highly contrasting nuclear and plastid genetic structure, suggesting that pollen-mediated gene flow allows panmixia, while seed-based dispersal may rarely exceed tens of metres. From a phylogeny based on full plastomes, we dated the surprisingly old crown age of maternal lineages back to ~6.2 Mya, perhaps co-occurring with the global expansion of savanna. In contrast, recent demographic history inferred from nuclear data shows a bottleneck signature ~350 generations ago, probably reflecting an environmental shift during the Late Pleistocene or the Holocene. Ancient in situ adaptation and recent demographic collapse of an endangered woody plant highlight the unique value and vulnerability of the Malagasy savannas.