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Background  Rodent malaria parasites (RMPs) serve as tractable tools to study malaria parasite biology and host-parasite-vector interactions. Among the four RMPs originally collected from wild thicket rats in sub-Saharan Central Africa and adapted to laboratory mice,  Plasmodium vinckei  is the most geographically widespread with isolates collected from five separate locations. However, there is a lack of extensive phenotype and genotype data associated with this species, thus hindering its use in experimental studies.    Results  We have generated a comprehensive genetic resource for  P. vinckei  comprising of five reference-quality genomes, one for each of its subspecies, blood-stage RNA sequencing data for five  P. vinckei  isolates, and genotypes and growth phenotypes for ten isolates. Additionally, we sequenced seven isolates of the RMP species  Plasmodium chabaudi  and  Plasmodium yoelii , thus extending genotypic information for four additional subspecies enabling a re-evaluation of the genotypic diversity and evolutionary history of RMPs.  The five subspecies of  P. vinckei  have diverged widely from their common ancestor and have undergone large-scale genome rearrangements. Comparing  P. vinckei  genotypes reveals region-specific selection pressures particularly on genes involved in mosquito transmission. Using phylogenetic analyses, we show that RMP multigene families have evolved differently across the  vinckei  and  berghei  groups of RMPs and that family-specific expansions in  P. chabaudi  and  P. vinckei  occurred in the common  vinckei  group ancestor prior to speciation. The erythrocyte membrane antigen 1 and  fam-c  families in particular show considerable expansions among the lowland forest-dwelling  P. vinckei  parasites. The subspecies from the highland forests of Katanga,  P. v. vinckei , has a uniquely smaller genome, a reduced multigene family repertoire and is also amenable to transfection making it an ideal parasite for reverse genetics. We also show that  P. vinckei  parasites are amenable to genetic crosses.    Conclusions   Plasmodium vinckei  isolates display a large degree of phenotypic and genotypic diversity and could serve as a resource to study parasite virulence and immunogenicity. Inclusion of  P. vinckei  genomes provide new insights into the evolution of RMPs and their multigene families. Amenability to genetic crossing and transfection make them also suitable for classical and functional genetics to study  Plasmodium  biology.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12915-021-00995-5.

Plasmodium vinckei genomes provide insights into the pan-genome and evolution of rodent malaria parasites