Multiple radiations of spiny mice (Rodentia: Acomys) in dry open habitats of Afro-Arabia: evidence from a multi-locus phylogeny

BACKGROUND: Spiny mice of the genus Acomys are distributed mainly in dry open habitats in Africa and the Middle East, and they are widely used as model taxa for various biological disciplines (e.g. ecology, physiology and evolutionary biology). Despite their importance, large distribution and abundance in local communities, the phylogeny and the species limits in the genus are poorly resolved, and this is especially true for sub-Saharan taxa. The main aims of this study are (1) to reconstruct phylogenetic relationships of Acomys based on the largest available multilocus dataset (700 genotyped individuals from 282 localities), (2) to identify the main biogeographical divides in the distribution of Acomys diversity in dry open habitats in Afro-Arabia, (3) to reconstruct the historical biogeography of the genus, and finally (4) to estimate the species richness of the genus by application of the phylogenetic species concept. RESULTS: The multilocus phylogeny based on four genetic markers shows presence of five major groups of Acomys called here subspinosus, spinosissimus, russatus, wilsoni and cahirinus groups. Three of these major groups (spinosissimus, wilsoni and cahirinus) are further sub-structured to phylogenetic lineages with predominantly parapatric distributions. Combination of alternative species delimitation methods suggests the existence of 26 molecular operational taxonomic units (MOTUs), potentially corresponding to separate species. The highest genetic diversity was found in Eastern Africa. The origin of the genus Acomys is dated to late Miocene (ca. 8.7 Ma), when the first split occurred between spiny mice of eastern (Somali-Masai) and south-eastern (Zambezian) savannas. Further diversification, mostly in Plio-Pleistocene, and the current distribution of Acomys were influenced by the interplay of global climatic factors (e.g., Messinian salinity crisis, intensification of Northern Hemisphere glaciation) with local geomorphology (mountain chains, aridity belts, water bodies). Combination of divergence dating, species distribution modelling and historical biogeography analysis suggests repeated “out-of-East-Africa” dispersal events into western Africa, the Mediterranean region and Arabia. CONCLUSIONS: The genus Acomys is very suitable model for historical phylogeographic and biogeographic reconstructions of dry non-forested environments in Afro-Arabia. We provide the most thorough phylogenetic reconstruction of the genus and identify major factors that influenced its evolutionary history since the late Miocene. We also highlight the urgent need of integrative taxonomic revision of east African taxa. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1380-9) contains supplementary material, which is available to authorized users.