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The family Bathyergidae (comprising six genera) is a group of subterranean rodents endemic to sub-Saharan Africa. Our understanding of the evolution and species richness of the South African bathyergid genera Georychus, Bathyergus and Cryptomys is limited, with the majority of species listed as Least Concern by the IUCN Red List of Threatened Species. Genetic data suggest that several cryptic species may be present in these genera. To explore genetic and ecological distinctiveness, and evaluate taxonomic richness across the ranges of Georychus, Bathyergus and to a lesser degree, Cryptomys, as well as evaluate possible scenarios which have historically influenced evolutionary patterns, we employed four protein coding markers (one mitochondrial and three nuclear) along with distribution wide sampling schemes and large sample sizes. In addition, possible ecological differences among the different intra-generic clades were explored. Genera appear to have originated in the north-eastern interior of South Africa, following novel habitats created through the Post-African I erosion cycle and dramatic changes in climate and phytogeography. In each genus, multiple geographically discrete genetic lineages (clades) are supported by both the mitochondrial and nuclear data. These lineages bear signature of the fragmentation of wider historical distributions through major environmental changes since the middle Miocene (major uplift events, Post-African II erosion cycle, drainage evolution of major river systems, sea-level fluctuations as well as climatic changes and vegetation shifts), thereby leading to long-term isolation. Along with protracted periods of separation, it appears that ecological differences further delimit the lineages in relation to geology, phytogeographic preference, elevation, rainfall and temperature. As such, two lineages in Georychus (Clades 1 and 2) and one lineages in Cryptomys (Clade I) occur at higher elevations above the Great Escarpment (in older deposits harbouring grassland vegetation, with higher rainfall and lower daily temperatures), with the remaining lineages within these genera (Clades 3, 4 and 5 in Georychus and Clades III and IV in Cryptomys) occupying a low-land distribution with contrasting climatic and geological characteristics. Although significant differences in ecological variables were also observed between Bathyergus clades, these were not consistent, given their largely low-land distributions. Our results corroborate and expand previous suggestions that several cryptic species are present within the South African Bathyergidae.