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Parasitic protozoan parasites have evolved many co-evolutionary paths towards stable transmission to their host population. Plasmodium spp., the causative agents of malaria, and related haemosporidian parasites are dipteran-borne eukaryotic pathogens that actively invade and use vertebrate erythrocytes for gametogenesis and asexual development, often resulting in substantial morbidity and mortality of the infected hosts. Here, we present results of a survey of insectivorous bats from tropical Africa, including new isolates of species of the haemosporidian genus Nycteria. A hallmark of these parasites is their capacity to infect bat species of distinct families of the two evolutionary distant chiropteran suborders. We did detect Nycteria parasites in both rhinolophid and nycterid bat hosts in geographically separate areas of Sub-Saharan Africa, however our molecular phylogenetic analyses support the separation of the parasites into two distinct clades corresponding to their host genera, suggestive of ancient co-divergence and low levels of host switching. For one clade of these parasites, cytochrome b genes could not be amplified and cytochrome oxidase I sequences showed unusually high rates of evolution, suggesting that the mitochondrial genome of these parasites may have either been lost or substantially altered. This haemosporidian parasite-mammalian host system also highlights that sequential population expansion in the liver and gametocyte formation is a successful alternative to intermediate erythrocytic replication cycles., (Copyright © 2015 The Authors. Published by Elsevier Ltd.. All rights reserved.)