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

Abstract

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.

Keywords: Acomys; Africa; Arabia; Biogeography; Plio-Pleistocene; Sahara; Savanna; Somali-Masai; Zambezian savanna.

Fig. 1

Multilocus phylogeny of the genus Acomys. a Bayesian phylogeny of the concatenated multi-locus matrix calculated in MrBayes. The support from Bayesian analysis in MrBayes (posterior probability, PP) and maximum likelihood analysis in RAxML (bootstrap probability, BP) is indicated by different colours on the nodes (black PP > 0.95, BP < 70; violet PP < 0.95, BP > 70; blue PP > 0.95, BP > 70). Five main Acomys groups (subspinosus, spinosissimus, russatus, wilsoni and cahirinus) are shown by different colours. The results of four different species delimitation approaches (“by-eye” prior; two delimitation approaches based on mtDNA: mPTP, ABGD; and a multilocus species delimitation in STACEY - see more details in the text) are shown in columns on the right, where individual “species” are separated by black lines. Additional information for 26 delimited taxa are provided, abbreviation of the lineages, and previously used taxonomic assignments. b DensiTree cloudogram of coalescent species trees from STACEY (for MCC species tree with PP see Additional file 4)

Fig. 2

Analysed samples and the distribution of genetic variability in the genus Acomys. a Geographical distribution of the genus Acomys according IUCN (orange background); the origin of newly genotyped individuals is shown by red circles, while georeferenced sequences from GenBank are shown by black circles; b distribution of genetic lineages in the subspinosus and spinosissimus groups; c distribution of genetic lineages in the russatus and wilsoni groups; d distribution of genetic lineages in the cahirinus group

Fig. 3

Divergence dating and the reconstruction of historical biogeography. Numbers on the nodes represent medians of estimated divergence date, and the horizonal bars show 95% highest posterior density of these estimates. Stars indicate the positions of fossil constrains used for the calibration of molecular clock (see Table 3 for more details). Different colours on the nodes represent reconstructed ancestral regions for each clade, according to the map in the frame: South Africa region (S), Zambezian region (Z), Somali region (E), Sudanian region (W), Sahara region (N), Arabian region (A)

Fig. 4

The probability of Acomys occurrence based on the MaxEnt modelling of bioclimatic niches. More intensive colour indicates higher probability of suitable conditions. a The model for the present; white dots indicate the sampled localities; b prediction for the last glacial maximum (21 ka); c prediction for the last interglacial period (120–140 ka)