Ubiquitous Hepatocystis infections, but no evidence of Plasmodium falciparum-like malaria parasites in wild greater spot-nosed monkeys (Cercopithecus nictitans)

Abstract

Western gorillas (Gorilla gorilla) have been identified as the natural reservoir of the parasites that were the immediate precursor of Plasmodium falciparum infecting humans. Recently, a P. falciparum-like sequence was reported in a sample from a captive greater spot-nosed monkey (Cercopithecus nictitans), and was taken to indicate that this species may also be a natural reservoir for P. falciparum-related parasites. To test this hypothesis we screened blood samples from 292 wild C. nictitans monkeys that had been hunted for bushmeat in Cameroon. We detected Hepatocystis spp. in 49% of the samples, as well as one sequence from a clade of Plasmodium spp. previously found in birds, lizards and bats. However, none of the 292 wild C. nictitans harbored P. falciparum-like parasites.

Fig. 1

Collection sites of blood samples from greater spot-nosed monkeys in Cameroon. Red circles indicate 12 locations (CS1-CS12) where samples were collected from hunted animals. Orange circles denote sites where Plasmodium falciparum-like parasites were previously detected in wild gorilla populations (Liu et al., 2010).

Fig. 2

Evolutionary relationships of haemosporidian sequences from greater spot-nosed (GSN) monkeys (Cercopithecus nictitans). A maximum likelihood tree of mitochondrial cytb sequences (726 bp) is shown, with Plasmodium and Hepatocystis reference sequences in black, newly derived sequences highlighted in red (only a subset of Hepatocystis sequences is shown), and one Plasmodium falciparum-like sequence (MO454) previously reported from a captive GSN monkey (Prugnolle et al., 2011) in blue. Asterisks on branches indicate bootstrap values ≥ 80%; the scale bar represents 0.05 nucleotide substitutions per site. GenBank accession numbers for all sequences are listed in Supplementary Table S1.

Fig. 3

Evolutionary relationships of Hepatocystis parasites. A maximum likelihood tree of mitochondrial cytb sequences (201 bp) is shown. Hepatocystis reference sequences are shown in black, with their respective host species indicated in parentheses; newly derived sequences from greater spot-nosed monkey samples are highlighted in red (the number of sequences with the same haplotype is shown in parentheses). Asterisks on branches indicate bootstrap support values ≥ 70%; the scale bar represents 0.02 nucleotide substitutions per site. GenBank accession numbers for all sequences are listed in Supplementary Table S1.