- The genome of Plasmodium berghei
- Reinvestigating the status of malaria parasite (Plasmodium sp.) in Indian non-human primates
- Research on alternative methods
This second perspective is particularly valuable wherever there are not obvious phylogenetic concordances between host species and their parasites. Plasmodium phylum Apicomplexa, family Plasmodiidae is a group of vector-borne parasitic protozoa that are better known by the handful of species that cause malaria in humans. The global health importance of human malarias, however, overshadows the extraordinary diversity in this genus represented by more than described species parasitizing many vertebrate hosts including rodents and nonhuman primates Garnham ; Coatney et al.
Of particular interest are those Plasmodium found in nonhuman primates and their relationships to the extant human malarias Ayala et al. Less attention, however, has been given to the evolutionary processes leading to the staggering diversity observed in primate malarial parasites Hayakawa et al. Although the hypothesis of adaptive radiation is appealing for parasites, such processes are not easy to study in any group of organisms, parasitic, or free-living. Furthermore, apparent patterns of accelerated evolution could be consistent with many other processes, if they are observed at broad time and geographic scales Glor These species are part of a monophyletic group that exhibits extraordinary phenotypic diversity, and its radiation is connected with the origin of the human parasite Plasmodium vivax Escalante et al.
This group includes species that are zoonotic Singh et al.
The genome of Plasmodium berghei
In addition, this clade is found in a defined geographic region that shares a common geologic history with many parasite species exhibiting overlapping host ranges the host species utilized by a parasite species and spatial distributions Coatney et al. Here, we report new data on the diversity of Plasmodium species infecting macaques and orangutans at two study sites in Borneo and analyze them together with previously reported data Hayakawa et al. We find several lineages that suggest new parasite species in this biodiversity hotspot.
Among those, we report divergent sympatric lineages in orangutans as well as evidence of parasite population genetic structures determined by geographic isolation. We also present evidence suggesting that the diversification rate of the Southeast Asian parasites is accelerated relative to other Plasmodium clades e.
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Thus, taking into consideration the apparent accelerated rate of evolution in this monophyletic group and that many species share multiple hosts, we hypothesize that Plasmodium species diversity in Southeast Asia was driven, at least in part, by the history of the host species utilized by these parasites. However, determining whether such rapid diversification was adaptive in nature will require additional evidence beyond the observation of accelerated evolution. In this study, we characterized the diversity of nonhuman primate malarias found in blood sampled from one population of Pongo pygmaeus morio and two populations of Macaca nemestrina and Macaca fascicularis from Sabah, Malaysian Borneo.
Table 1 describes the diversity of nonhuman primate malarias found in one population of orangutans P o. Blood smears were collected and some of the samples were positive by microscopy; however, the quality of the smears did not allow us to identify the parasites beyond the genus level. Thus, we relied on molecular diagnostics for species identification. All blood samples from 15 pig-tailed macaques M. We were able to generate 34 parasite mitochondrial genomes mtDNA for different Plasmodium parasites, 16 from M. However, we were unable to obtain complete mtDNA sequences for several positive M.
Regardless of the relatively small sample size, we found the same six Plasmodium species P. Figure 1 shows a Bayesian phylogenetic analysis of a combined set of nearly complete mitochondrial genome sequences including those generated in this and several previous studies supplementary table S1 , Supplementary Material online. We used the African parasite P. Overall, this phylogeny is similar to those obtained in previous studies Pacheco et al.
Of particular interest is a lineage that was present in both macaque species which shares a recent common ancestor with P. This Plasmodium species is divergent from the other species in that clade and does not appear to belong to either P. Specifically, the divergence between Plasmodium sp. This result may indicate that both species of macaques harbor a new Plasmodium species. In addition, we found Hepatocystis sp. Phylogenetic tree of Plasmodium species based on complete mitochondrial genomes. Bayesian and ML methods yielded identical topologies and so only the Bayesian tree is shown.
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The values above branches are posterior probabilities together with bootstrap values in bold as a percentage obtained for the ML tree see Materials and Methods. Macaque parasites from Borneo are labeled in blue and Plasmodium species from orangutans are labeled in red. Numbers of individuals with each parasite are shown.
The outgroup is indicated by the gray branches. Of the 38 orangutans sampled for this study, 23 were positive Three samples had low parasitemia and the PCR did not yield bands that would allow us to clone them. Unfortunately, although positive blood smears were available, these were not of sufficient quality to determine whether these parasites coincide with any of the Plasmodium species previously described in orangutans by Garnham and Peters et al.
We generated 30 parasite mitochondrial genomes from the remaining 20 samples; these haplotypes belonged to three different lineages A—C, fig. The phylogenetic analysis showed that two of these lineages A and B form a monophyletic group and share a common ancestor with P. Lineage C is at the base of a monophyletic group that includes P. Specifically, P. The average distance between the haplotypes belonging to lineages A and B in orangutan malarias 0. On the other hand, the average distances between clades A and C 0. These results suggest that the haplotypes identified in figure 1 as A—C may belong to three different species.
Clade A includes haplotypes described previously in a different population of orangutans Pacheco et al. In the case of P. These lineages belong to one of the two clades fig. Indeed, the average genetic distance among these four P. It is also worth noting that the divergence of these two clades of P. In addition to mtDNA genomes, phylogenetic analyses were also performed separately on data from several macaque and orangutan parasites using nuclear genes encoding two major antigens: Apical membrane antigen-1 AMA-1; fig. Despite the smaller number of species for which data is available, the phylogenies estimated from these two loci are largely compatible with previous studies using genes encoding merozoite antigens MSP Pacheco et al.
In particular, in both phylogenies we observe that several of the orangutan malaria lineages form a monophyletic group sharing a common ancestor with the macaque parasite, P. One difference between the phylogenies generated using either mtDNA or these two antigen-encoding genes is in the relative position of P. This is not surprising considering that the position of P. Although in the mitochondrial tree this lineage is located within the clade that includes the three orangutan lineages and P. This discrepancy could have three different explanations.
First, because the mitochondrial and nuclear loci are unlinked, there could be random differences in the genealogies of these loci. Second, this could be due to diversifying- or frequency-dependent selection acting on the antigen loci. Finally, this could be an artifact of our inability to generate antigen sequences for all of the taxa included in the mitochondrial tree. Indeed, because we were unable to generate any sequences of ama-1 that can be unambiguously assigned to mtDNA clade C, the position of P.
Bayesian phylogenetic tree of Plasmodium species based on the gene encoding AMA Clone numbers are shown. Clade numbers are shown and not necessarily correspond to clades A—C fig. For more details see Result section. The outgroup is indicated by the gray branch. In the case of ama-1 , we were able to obtain sequences for P. The genetic polymorphism of ama-1 per species is reported in the supplementary table S2 , Supplementary Material online. The ama-1 allele found in this study for P. Again, the undescribed Plasmodium sp. On the other hand, we only were able to generate msp-1 42 sequences for P.
The genetic polymorphism per species for msp-1 42 is reported in supplementary table S3 , Supplementary Material online. Overall, using these additional msp-1 42 sequences, we recovered the same topology that was previously reported for this antigen Pacheco et al. Phylogenetic-based analyses provide some insight into the role of selection at these two loci Pond et al.
S1 , Supplementary Material online. Furthermore, many of the nodes that may correspond to host switches also have significant uncorrected sequential likelihood ratio tests LRTs.
A similar pattern emerges from msp-1 42 where this method identifies four lineages that appear to be under episodic diversifying selection supplementary table S4 and fig. A median joining network of 41 Plasmodium mtDNA haplotypes isolated from orangutans from Borneo is depicted in figure 4.
As expected, the three clades identified in the mtDNA tree were clearly separated in the haplotype network. Furthermore, clade A itself colored in green contains two genetically differentiated populations light green: Sabah; dark green: Kalimantan and indeed the fixation index F ST between these two populations is high 0. In another context, the Venn diagram depicted in figure 4 shows the number of orangutans with mixed infections of Plasmodium. At least 10 of the 20 orangutan samples harbored mixed infections with parasites from two distinct clades, but none was found to be simultaneously infected by all three species.
Venn diagram of mixed infections and median joining network of Plasmodium sp. Branch lengths are proportional to divergence and node sizes are proportional to total haplotype frequencies. Figure 5 shows a median joining network for the 16 P. In addition, we also identified a divergent P.
The mitochondrial genome phylogeny was used to estimate the ages of the major clades of South Asian primate malarias under three different calibration scenarios fig. S2 , Supplementary Material online. See supplementary fig. S2 , Supplementary Material online, for the node numbers.
As expected, there is extensive overlap among the Crls obtained under the three different scenarios used for calibration. When the phylogeny is calibrated by assuming that the Asian and African primate parasites split in the same time frame that their hosts became geographically isolated 6— The split between P. Furthermore, clades A and B diverged approximately 1. On the other hand, the common ancestor of the orangutan Plasmodium lineages in clade C appears to have existed between 3. Timetree of the divergence of malarial parasites from Borneo, Sabah.
Divergence times were estimated with BEAST using the most inclusive scenario based on the minimum divergence of Macaca and Papio using fossils 6— Times are shown in Ma. The numbers of the nodes described in table 3 are provided and depicted with an orange dot. N ote. Node numbers are listed in supplementary figure S2 , Supplementary Material online. See Materials and Methods for more details. Previous phylogenetic studies have indicated that P. In this study, the age of the most recent common ancestor of P.
Visual inspection of the Plasmodium phylogeny fig. In fact, this hypothesis is consistent with the results obtained when we used the program MEDUSA to compare different birth—death models on a sample of 50 trees describing the relationships between the Plasmodium species known to infect mammalian hosts table 4 and supplementary fig. S3 , Supplementary Material online.
In every case, the corrected Akaike information criterion AICc calculated by MEDUSA was minimized by a two component birth—death model with accelerated branching within the clade of Asian macaque-infecting parasites. Although in five cases the reduction in AICc was too small to reject a simpler model with homogeneous birth and death rates across the entire tree, in the remaining 45 cases, the two-component model was identified as the best-fitting model by the stepwise selection procedure implemented in MEDUSA table 4.
Maximum likelihood ML estimates of the branching and extinction rates within the two-component models suggest that the parasites infecting Asian macaques have speciated approximately three to four times more rapidly than the other lineages contained in the tree. Furthermore, these differences appear to be almost entirely due to changes in the branching rate rather than the extinction rate.
Indeed, in every case the extinction rate was estimated to be less than 0. The change in branch length distribution is inferred to occur between nodes nd1 and nd2 see supplementary fig. S3 , Supplementary Material online, for ML with labeled nodes. The evidence ratio is shown under the column labeled evidence.
The exponential exp and variable rates v. Although there has been increasing awareness of the importance of parasitic organisms for biodiversity Poulin , most studies continue to focus on the harm caused by parasites to their hosts Nunn and Altizer and pay relatively little attention to the role of parasites as intrinsic elements of an ecosystem. Although host evolutionary history is considered a major driver in parasite speciation Poulin et al.
However, a common framework that encompasses host-range and different forms of geographic speciation is still a work in progress Huyse et al. Malarial parasites and other Apicomplexa allow such basic issues to be addressed since there is an overall knowledge of their basic biology and their species diversity. Here, we start to explore the relative importance of geography and host diversity and evolutionary history in the observed pattern of speciation of a diverse monophyletic group of parasites with overlapping geographical distributions.
Although we are far from understanding the complex evolutionary history of the nonhuman primate malarias in Southeast Asia, this study unveils several interesting patterns. First, we found that the two sympatric macaque species found in Borneo share the same set of Plasmodium parasites.
Thus, even with limited data, we do not observe evidence of host specificity. This result is perhaps surprising when we consider that the two Macaca species probably diverged 4—5 Ma Tosi et al. Second, we did not observe that populations of P. This observation suggests that transmission of this multihost parasite occurs frequently between host individuals belonging to different species, at least on the time scale resolved by mtDNA.
Third, our results indicate that some of the parasite populations are geographically structured within the island of Borneo. This is evidenced by the orangutan parasites from clade A fig. This result is expected and simply reflects the spatial distribution of the host population. The most important finding concerning the orangutan malarias is that there are multiple sympatric clades of Plasmodium. The phylogenetic relationships between lineages C and A and B in a clade that also includes the gibbon parasite P. However, because we have only limited data on parasites from gibbons, the direction of such host switches cannot currently be established.
Nevertheless, P. Asian ape parasites, thus far, have only been found in single host species, despite multiple sampling efforts Coatney et al. In contrast, P. Thus, it seems interesting that a parasite clade with many species with apparently high host specificity in Asian apes has given rise to a generalist parasite with a broad host range. In the case of orangutan malarias, the occurrence of such sympatric lineages within a host could be the result of sympatric speciation, secondary contacts between originally isolated host populations with divergent parasite lineages, or secondary acquisition via host switches as has been proposed in avian parasites Ricklefs Although we cannot rule out the possibility of sympatric speciation, the life cycle of malarial parasites involving sexual reproduction in the mosquito vector makes it likely that different parasite lineages infecting the same host species in the same area will frequently mate.
Under these conditions, sympatric speciation is expected to occur only if there is very strong selection promoting divergence and reproductive isolation Gavrilets ; Giraud et al. For this reason, we believe that our data are best explained by scenarios involving secondary contacts.
Indeed, the two lineages, A and B, shared their most recent common ancestor 1—2 Ma, a time frame that lies within the demographic history of the extant orangutans, a genus that evolved under complex climatic and geographic events that changed the connectivity of its populations Nieberding et al. Finally, our data suggest that speciation has occurred at an elevated rate within the group of malaria parasites that infect Southeast Asian nonhuman primates table 4. This rate seems to be 3—4 time faster than in the other groups included in this study e. Furthermore, we found no evidence of a significant extinction rate in the sampled species of mammalian malarias.
Although this inference is contingent on the assumption that we have sampled all extant Plasmodium species infecting mammalian hosts, we obtained qualitatively similar results when we repeated the MEDUSA analyses but specified that the lemur parasite clade contained an additional three species that have not yet been sequenced.
Indeed, there are partial mtDNA sequences that suggest the existence of three such species unpublished data. It is also important to highlight that additional sampling of nonhuman primates in Southeast Asia may increase the number of species contained within this clade e. This aspect is far more complex to address. Here, we have found some evidence for episodic selection in two proteins involved in the invasion of the red blood cell.
Considering the number of proteins that participate in the invasion of the red blood cell, these two antigens only provide a first glimpse of the many molecular adaptations that have presumably emerged in this group of parasites. This is already evident when we consider that some parasites like P. In addition, there is an extraordinary diversity of life history traits in this group Coatney et al.
At this stage, we can only speculate that such phenotypic diversity may allow the coexistence of multiple species by reducing competition. Indeed, we observed a relatively high number of mixed infections in this study table 1. Nevertheless, all this phenotypic diversity and variation at antigen-encoding genes reported here supplementary table S2 and S3 , Supplementary Material online and elsewhere emerged in a relatively short period of 3—4 Ma Pacheco et al.
In summary, contrary to previous studies, the evidence does not suggest that host switches have played a central role in the diversification of this group of parasites. On the one hand, we find no evidence of host specialization in the macaque parasites. In particular, we did not observe differentiation of P. On the other hand, although the orangutan parasites do appear to be host specific, phylogenetic analyses suggest that at least two of these lineages have diversified within orangutans.
The two lineages that do appear to have originated via host switches are P. We hypothesize that the host ranges of these parasite species underwent several historical changes as result of each host species demographic history that affected their population densities and spatial distributions. Importantly, this notion of a host range evolutionary dynamic does not assume that parasites affected their hosts' speciation or distribution e. However, host—parasite antagonisms could be part of the parasite evolutionary dynamics as suggested by the observation of episodic selection in the antigens included in this investigation.
Although hypothesizing adaptive radiation is tempting in light of the rapid diversification of host species, we are unable to draw such a conclusion in this case due to the confounding effects of biogeographical processes. Overall, elucidating the relative importance of adaptive radiation and biogeographical processes is a matter of great importance. Understanding the evolutionary dynamic of the host ranges in parasite speciation will provide valuable information about the origin of the observed biodiversity of parasites.
The island of Borneo is considered a biodiversity hotspot Meijaard and Nijman Just in the state of Sabah 73, km 2 in the northern portion of Borneo , there are more than ten species of nonhuman primates. Approximately 11, Eastern Bornean orangutans P o.
An unknown number of Sundaland pig-tailed macaque M. S4 , Supplementary Material online. Following a 6-month quarantine period, orangutans are taught how to transverse the forest and forage for food. Following extensive health inspections, these animals are eventually relocated or released into the surrounding forest. To facilitate public education and generate operational funds, the public is allowed to view two daily feedings of the free-ranging animals Ambu It is approximately 30 km north of Kota Kinabalu, surrounded by hectares of tropical forest, and contains an Orangutan Education Centre, part of the Rasa Ria Nature Reserve and home to four orangutans at the time of sampling.
Like SORC, the public is allowed to view two daily feedings of the animals. This included 34 orangutans P o. For sampling purposes, all but one orangutan the largest male were manually restrained for clinical inspection and sample collection. None of these animals was injured or febrile at the time. Respiration and heart rate were monitored while anesthetized. For the macaques and orangutans alike, blood was collected from the femoral vein using standard venipuncture technique with sterile, single-use Vacutainer productions Beckton-Dickson.
All the samples were collected in July and November No animal was sampled more than once. Permission to conduct all research in Sabah was granted by the Sabah Wildlife Department, and all animal handling was done by trained staff of the Sabah Wildlife Department. Both strands for all the cytb fragments were direct sequenced, using an Applied Biosystems capillary sequencer, and identified as Plasmodium using BLAST Altschul et al. Three loci were amplified from malaria positive samples. First, we amplified approximately 5, bp of the parasites mitochondrial genomes mtDNA. These two malarial antigens are essential in the invasion of the host red blood cell and have been widely studied Chesne-Seck et al.
As in the case of the mtDNA, there is a rich data set on these antigens that facilitates species identification. Infection tends to be low grade but may be persistent and remain as source of parasites for humans for some time. Like P. In spite of its admittedly poor transmission to chimpanzees given its discontigous spread, it is suspected that P.
If this is actually the case, the host seems likely to be a primate. A report has been published suggesting that P. It has been recently shown that P. These species are Plasmodium ovale curtisi and Plasmodium ovale wallikeri. Plasmodium knowlesi has a natural reservoir in the macaques of Southeast Asia, and was only in identified as being transmissible to humans.
Interrelatedness - The evolution of these species is still being worked out and the relationships given here should be regarded as tentative. This grouping, while originally made on morphological grounds, now has considerable support at the DNA level. Many species of Plasmodium which infect primates have been divided into subspecies. Examples are listed below:.
Most if not all Plasmodium species infect more than one host: the host records shown here should be regarded as incomplete. It has been proposed that the species P. New World monkeys of the family Cebidae : P. Old World monkeys of the family Cercopithecidae : P.
Gibbons of the family Hylobatidae : P. Orangutans Pongo : P. Gorillas and chimpanzees: P. From Wikipedia, the free encyclopedia. This section contains an enumeration of examples, but lacks a general overview of its topic. You can help by adding an appropriate introductory section.
Reinvestigating the status of malaria parasite (Plasmodium sp.) in Indian non-human primates
Editing help is available. March J Parasitol. Am J Trop Med Hyg. Brumpt 2eme note. Transmission de Plasmodium schwetzi a l'homme" [Study of Plasmodium schwetzi E.
Research on alternative methods
Transmission of Plasmodium schwetzi to man]. The Lancet Global Health. Bibcode : PNAS.. PLoS Pathog. Acta Trop. Int J Parasitol. Dec Emerg Infect Dis. Malar J. Bibcode : PLoSO