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Plasmodium  parasites exerted a strong selective pressure on primate genomes and mutations in genes encoding erythrocyte cytoskeleton proteins (ECP) determine protective effects against  Plasmodium  infection/pathogenesis. We thus hypothesized that ECP-encoding genes have evolved in response to  Plasmodium -driven selection. We analyzed the evolutionary history of 15 ECP-encoding genes in primates, as well as of their  Plasmodium -encoded ligands (KAHRP, MESA and EMP3). Results indicated that  EPB42 ,  SLC4A1 , and  SPTA1  evolved under pervasive positive selection and that episodes of positive selection tended to occur more frequently in primate species that host a larger number of  Plasmodium  parasites. Conversely, several genes, including  ANK1  and  SPTB , displayed extensive signatures of purifying selection in primate phylogenies, Homininae lineages, and human populations, suggesting strong functional constraints. Analysis of  Plasmodium  genes indicated adaptive evolution in  MESA  and  KAHRP ; in the latter, different positively selected sites were located in the spectrin-binding domains. Because most of the positively selected sites in alpha-spectrin localized to the domains involved in the interaction with KAHRP, we suggest that the two proteins are engaged in an arms-race scenario. This observation is relevant because KAHRP is essential for the formation of “knobs”, which represent a major virulence determinant for  P .  falciparum .

Genetic conflicts with Plasmodium parasites and functional constraints shape the evolution of erythrocyte cytoskeletal proteins