Nuclear phylogenomics reveals strong geographic patterns in the evolutionary history of aloe and related genera (alooids)

Abstract

BACKGROUND AND AIMS : With >700 species, Aloe and its generic kin (alooids) are a morphologically diverse group of succulent plants with a wide range across Africa, Madagascar and the Arabian Peninsula. Species such as Aloe vera and A. ferox are cultivated at scale for natural products, whole foods, and cosmetics. Despite substantial α-taxonomy contributions, infrageneric classification of Aloe has remained unresolved. Molecular systematics has been compromised by the lack of informative characters in standard markers and high costs of obtaining informative nuclear loci from large genomes (e.g. >15 Gbp), and the difficulty of obtaining quality DNA extractions from material of known provenance. Here these constraints are overcome with target capture sequencing, which allows cost-effective sequencing of informative low-copy nuclear loci and unlocks genetic resources from preserved specimens in herbaria as well as silica-dried tissues. METHODS : Using a custom kit for alooids, 189 nuclear loci were sequenced in 294 species, including 50 herbarium specimens, to build a new phylogenomic framework for the big genus Aloe and 11 closely related alooid genera. Genus-level representations of non-alooid members of Asphodelaceae were sequenced with the same tool. The monophyly of Asphodelaceae subfamilies, alooid genera and infrageneric taxonomic groups of Aloe sensu stricto was tested with the obtained topologies. KEY RESULTS : The new phylogenomic framework demonstrates the monophyly of the alooids and confirms recent classifications in which smaller genera (Aloidendron, Aloiampelos, Aristaloe, Gonialoe, Kumara) are separated. Strong geographic patterns in the Aloe phylogeny are contrasted by less obvious phylogenomic structure in habit (growth form), and vegetative or reproductive morphology, which are mainstays of α-taxonomy. CONCLUSIONS : Repeated incidents of adaptive radiation and niche specialization appear to underlie species diversity in Aloe. This study illustrates the power of combined (nuclear) phylogenomic and α-taxonomic inference, including the utility of herbarium genomics, in resolving the systematics of big genera.