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

Abstract

Background and AimsWith >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 -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 that 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. MethodsUsing 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 genera in the alooid clade. Available taxonomic classifications for Aloe sensu stricto were contrasted against the obtained topology in an effort to stabilise taxonomy. Genus-level representations of the family Asphodelaceae were sequenced with the same tool. Key resultsThe 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 phylogenetic structure in habit (growth form), and vegetative or reproductive morphology that are mainstays of -taxonomy. ConclusionRepeated incidents of adaptive radiation and niche specialisation appear to underlie species diversity in Aloe. This study illustrates the power of combined (nuclear) phylogenomic and -taxonomic inference, including the utility of herbarium genomics, in resolving the systematics of big genera. Lay summaryThe alooids are a group of >700 succulent plants, such as Aloe vera. Testing their taxonomy with genetics is difficult as Aloe genomes are large and very similar between species. A targeted approach was used to classify alooids with highly variable nuclear genes in {+/-}300 species. The evolutionary relationships of alooids are determined principally by geographic distribution patterns, rather than plant morphology or flower shape.