Accelerated Diversification of Nonhuman Primate Malarias in Southeast Asia: Adaptive Radiation or Geographic Speciation?

Abstract

Although parasitic organisms are found worldwide, the relative importance of host specificity and geographic isolation for parasite speciation has been explored in only a few systems. Here, we study Plasmodium parasites known to infect Asian nonhuman primates, a monophyletic group that includes the lineage leading to the human parasite Plasmodium vivax and several species used as laboratory models in malaria research. We analyze the available data together with new samples from three sympatric primate species from Borneo: The Bornean orangutan and the long-tailed and the pig-tailed macaques. We find several species of malaria parasites, including three putatively new species in this biodiversity hotspot. Among those newly discovered lineages, we report two sympatric parasites in orangutans. We find no differences in the sets of malaria species infecting each macaque species indicating that these species show no host specificity. Finally, phylogenetic analysis of these data suggests that the malaria parasites infecting Southeast Asian macaques and their relatives are speciating three to four times more rapidly than those with other mammalian hosts such as lemurs and African apes. We estimate that these events took place in approximately a 3–4-Ma period. Based on the genetic and phenotypic diversity of the macaque malarias, we hypothesize that the diversification of this group of parasites has been facilitated by the diversity, geographic distributions, and demographic histories of their primate hosts.

Evolution of the merozoite surface protein 7 ( msp7 ) family in Plasmodium vivax and P . falciparum : A comparative approach

“…Group A includes two of the three msp7 paralogs (PVX_082645 and PVX_082695) that have orthologs in all the Plasmodium species considered in this study, including rodents. The phylogenetic relationships within ortholog PVX_082695 inside Group A paralogs clade are similar to those estimated for Plasmodium species using other loci and mtDNA genomes (Muehlenbein et al, 2015; Pacheco et al 2011; Pacheco et al, 2012). Group B, considerably the largest in our phylogenetic analysis (Fig.…”

“…Thus, the events leading to the high number of msp7 paralogous genes in these two species likely occurred before their most recent common ancestor (2.36–5.27 Ma, Pacheco et al, 2011). Furthermore, some of these paralogs could be as old as the divergence of these two species from P. fieldi , which we found to possess 10 out of the 12 msp7 genes found in P. vivax and P. cynomolgi (Muehlenbein et al, 2015; Pacheco et al 2012). However, we cannot confirm this older origin for all 12 extant msp7 paralogs in P. vivax due to the absence of publicly available P. fieldi genome sequences.…”

“…1), a species with a recent common ancestor shared with P. vivax, P. cynomolgi, and P. inui. (Muehlenbein et al, 2015; Pacheco et al, 2012). Although 10 paralogs found in P. vivax and P. cynomolgi are shared with P. fieldi , it cannot be ascertained whether all 12 msp7 paralogs are shared and syntenic between the three species due to the lack of genomic information on P. fieldi .…”

A Review of Plasmodium knowlesi among Macaques in Malaysia

“…In a study by Muehlenbein et al (2015), Plasmodium parasites isolated from M. fascicularis and M. nemestrina in Sabah showed significant difference suggesting genetic specificity to different host species.…”

A critical analysis of the cynomolgus macaque, Macaca fascicularis, as a model to test HIV-1/SIV vaccine efficacy

“…The cynomolgus macaque population remaining in Mauritius is particularly interesting from an immunological stand point due to the genetic homogeneity of some alleles [14], making these animals useful for vaccine studies. Today, the only geographic overlap of cynomolgus macaque territory with rhesus distribution is the top of their range in Vietnam where pig-tail macaques also co-exist and interspecies hybridization has been documented [15].…”