List of Plasmodium species

List of Plasmodium species
Scientific classification
Domain: Eukaryota
Kingdom: Chromalveolata
Superphylum: Alveolata
Phylum: Apicomplexa
Class: Aconoidasida
Subclass: Haemosporidiasina
Order: Haemosporida
Suborder: Laveraniina
Family: Plasmodiidae
Genus: Plasmodium
Species

see text

The genus Plasmodium is a member of the order Haemosporidia. It is the largest genus within this order and currently consists of over 250 species. They cause malaria in many different vertebrates.

The species in this genus are entirely parasitic with part of their life cycle spent in a vertebrate host and another in an invertebrate host - usually a mosquito. Vertebrates infected by members of this genus include mammals, birds and reptiles.

Host range among the mammalian orders is non uniform. At least 29 species infect non human primates; rodents outside the tropical parts of Africa are rarely affected; a few species are known to infect bats, porcupines and squirrels; carnivores, insectivores and marsupials are not known to act as hosts.

The listing of host species among the reptiles has rarely been attempted. Ayala in 1978 listed 156 published accounts on 54 valid species and subspecies between 1909 and 1975.[1] The regional breakdown was Africa: 30 reports on 9 species; Australia, Asia & Oceania: 12 reports on 6 species and 2 subspecies; Americas: 116 reports on 37 species.

Diagnostic criteria of the order Haemosporida

Currently there are ~550 species recognised in this order organised into 17 genera.[2]

The diagnostic criteria of this family are:

Diagnostic criteria of the genus Plasmodium

Note

Mammalian erythrocytes do not possess a nucleus. Although it has been suggested that the nucleus was lost in the erythrocytes better to enable them to traverse capillaries evidence for this is lacking. It appears that this loss along with the mitochondria that the erythrocytes also lose may protect the erythrocytes against oxidative stress.[3]

Subgenera

The full taxonomic name of a species includes the subgenus but this is often omitted in practice. The full name indicates some features of the morphology and type of host species. Sixteen subgenera are currently recognised.

The avian species were discovered soon after the description of P. falciparum and a variety of generic names were created. These were subsequently placed into the genus Plasmodium although some workers continued to use the genera Laverinia and Proteosoma for P. falciparum and the avian species respectively.

The 5th and 6th Congresses of Malaria held at Istanbul (1953) and Lisbon (1958) respectively recommended the creation and use of subgenera in this genus. Laverinia was applied to the species infecting humans and Haemamoeba to those infecting lizards and birds. This proposal was not universally accepted. Bray in 1955 proposed a definition for the subgenus Plasmodium and a second for the subgenus Laverinia in 1958. Garnham described a third subgenus - Vinckeia - in 1964. Several additional subgenera have been created since. The currently recognised subgenera are listed below.

Asiamoeba Telford 1988
Bennettinia Valkiūnas 1997[4]
Carinamoeba Garnham 1966
Giovannolaia Corradetti, Garnham & Laird 1963[5]
Haemamoeba Grassi & Feletti 1890
Huffia Garnham & Laird 1963
Lacertaemoba Telford 1988
Laverania Bray 1958[6]
Novyella Corradetti, Garnham & Laird 1963
Nyssorhynchus Poinar 2005
Ophidiella Garnham 1966
Papernaia Landau et al 2010[7]
Paraplasmodium Telford 1988
Plasmodium Bray 1963 emend. Garnham 1964
Sauramoeba Garnham 1966
Vinckeia Garnham 1964

Classification criteria for subgenera

The current classification scheme was developed prior to the widespread use of DNA sequence based taxonomy and is based on host and morphological criteria. Plasmodium has since been shown to be paraphytic with the genera Haemoproteus and Hepatocystis (vide infra).[8] Revision of this genus will be undertaken once sufficient DNA sequence material is available.

This forthcoming reclassification project is not unique to this genus as DNA based taxonomy is revising many traditional groupings of protozoa.

The bird infecting taxa can be separated into two groups on the basis of the gametocytes: species with round gametocytes (Bennettinia, Haemamoeba) and species with elongated gametocytes (Giovanniola, Huffia and Novyella). The monophyly of the Bennettinia, Haemamoeba and Huffia subgenera was subsequently confirmed by molecular studies.[9] The other two genera were found to be paraphytic. The genera were then revised and a new subgenus - Papernaia - was created.[7]

Species with mammalian hosts

Laverania

Species in this subgenus infect higher primates (including man) and have characteristic sickle shaped female gametocytes.

The type species is Plasmodium falciparum.

Plasmodium

Species infecting higher primates other than those in the subgenus Laverania are placed in the subgenus Plasmodium.

The type species is Plasmodium malariae.

Vinckeia

Parasites infecting other mammals including lower primates (lemurs and others) are classified in the subgenus Vinckeia.

The type species is Plasmodium bubalis.

Species with avian hosts

Bennettinia

Schizonts contain scant cytoplasm, are often round, do not exceed the size of the host nucleus and stick to it. Gametocytes, while varying in shape tend to be round or oval, do not exceed the size of the nucleus and stick to it.

The type species is Plasmodium juxtanucleare.

Giovannolaia

Schizonts contain plentiful cytoplasm, are larger than the host cell nucleus and frequently displace it. They are found only in mature erythrocytes. Gametocytes are elongated. Exoerythrocytic schizogony occurs in the mononuclear phagocyte system.

The type species is Plasmodium circumflexum.

Haemamoeba

Mature schizonts are larger than the host cell nucleus and commonly displace it. Gametocytes are large, round, oval or irregular in shape and are substantially larger than the host nucleus.

The type species is Plasmodium relictum.

Huffia

Mature schizonts, while varying in shape and size, contain plentiful cytoplasm and are commonly found in immature erythryocytes. Gametocytes are elongated.

The type species is Plasmodium elongatum.

Novyella

Mature schizonts are either smaller than or only slightly larger than the host nucleus. They contain scanty cytoplasm. Gametocytes are elongated. Sexual stages in this subgenus resemble those of Haemoproteus. A white/blue globule is present in the cytoplasm. Exoerythrocytic schizogony occurs in the mononuclear phagocyte system

The type species is Plasmodium vaughani.

Papernaia

The gametocytes are elongated. The schizonts apically or lateroapically placed and are rounded or irregularly shaped. The host nucleus may be tilted.

The type species is Plasmodium polare

Species with reptilian hosts

Although over 3200 species of lizard have been identified as hosts to Plasmodium species, only 29 species of snakes have been. All snake infecting species are placed into the subgenus Ophidiella.

Asiamoeba

The schizonts and gametocytes are greatly disparate in size (4 to 15 times).

Carinamoeba

The schizonts are small and give rise to 8 or fewer merozoites. The gametocytes like the schizonts are small.

The type species is Plasmodium minasense.

Lacertaemoba

The schizonts are medium-sized and undergo 3 to 5 nuclear divisions. The gametocytes are medium-sized

Paraplasmodium

The schizonts are of medium size. Exoerythrocytic schizonts may be produced in both fixed and wandering host cells. The gametocytes are large. One species in this sub-genus is capable of merogony in a vector of the Lutzomyia genus.

Sauramoeba

Large schizonts giving rise to 12 or more merozoites. The gametocytes like the schizonts are large. The asexual stages tend to disappear from the lymphocytes once the gametocytes appear in the lymphocytes.

The type species is Plasmodium agamae.

Ophidiella

The species in this subgenus infect only snakes.

The type species is Plasmodium weyoni.

Species with unknown hosts

One species has been identified from Dominican amber - Plasmodium dominicum. The vertebrate host of this species is unknown but it seems likely that it may have been a bird.

Nyssorhynchus

The type species is Plasmodium dominicum.

Phylogenetics

Although the evolution of this genus has been studied by a number of authors, details are still being elucidated. A brief summary of the pattern that has emerged is as follows:

The most basal split in the genus is between the reptile/bird species and the mammalian species. The bird/reptile clade appears to be related to the genera Haemoproteus, Leukocytozoon and Polychromophilus. The genus Hepatocystis appears to have evolved from with the mammalian species clade. Within the mammalian species the subgenus Laverinia appears to be basal with the subgenus Plasmodium and the rodent species being sister clades. Hepatocystis appears to have diverged after the separation of the rodent species. The species infecting lemurs may belong in the subgenus Plasmodium instead of their current placement within the subgenus Vinckeia.

Within the subgenus Plasmodium, P. vivax groups with an Asian clade which appears to be rooted in Africa. P. malaria and P. ovale both belong to an African clade and are more closely related to each other than to P. vivax. Within the subgenus Laverinia P. falciparum and P. reichenowi form a clade while the other four known species form a second clade.

There are a number of additional species in these taxa that await full description so changes to the branching order are likely. However the overall arrangement outlined above seems to be supported by a number of studies by different authors and is unlikely to change. Given the recently recognised paraphytic nature of several of the taxa above, the introduction of new genera and possibly families in the near future seems highly likely.

Relations with other Haemosporidian genera

While most phylogenetic trees have tended to agree that Plasmodium has descended from Leukocytozoon or Haemoproteus like species a Bayesian phylogenetic reconstruction suggests that Plasmodium may be the ancestral genus that has given rise to Haemoproteus and other genera.[10] Further study in this area is required.

Another Bayesian analysis has suggested the following taxonomy: Mammalian Plasmodium and Hepatocystis are sister clades with Hepatocystis having evolved from within the genus Plasmodium; the bird and reptile species are intermixed and basal to the mammalian Plasmodium/Hepatocystis species; the reptilian/bird Plasmodium species are a sister clade to the genus Polychromophilus; Leukocytozoon and Haemoproteus and sister clades; the Leukocytozoon/Haemoproteus clade is a sister to the Parahaemoproteus clade; and the Parahaemoproteus/Haemoproteus/Leukocytozoon clade is a sister to the reptilian/bird Plasmodium/Polychromophilus clade.[10] This grouping is supported by previous results.[11]

A study of DNA sequences suggests that the genus is paraphytic with Hepatocystis being related to the mammalian species and Polychromophilus being related to the reptile species.[12] This study also supports the ancestor of Plasmodium being a Leucocytozoon like species and that Plasmodium is more closely related to the Haemoproteus - specifically the subgenus Parahaemoproteus - than to Leucocytozoon.

A paper by Blanquart and Gascuel[13] examined Plasmodium 84 mitochondrial sequences and included Hepatocystis, Haemoproteus and Leukocytozoon sequences. The results agree with the previous analyses showing that Hepatocystis, Haemoproteus and Plasmodium appear to be derived from a Leukocytozoon ancestor. Hepatocystis appears to be a sister group to the great ape-rodent clade with the lower primate clade being ancestral to all three. In terms of Plasmodium subgenera they suggest that the subgenus Plasmodium is ancestral to both Laverania and Vinckeia.

A study of parasites infecting bats found that the bats were infected by species of the genera Hepatocystis, Plasmodium, Polychomophilus and Nycteria.[2] A phylogenetic tree which included these genera along with Haemoproteus and Leukocytozoon species was examined. As before Leukocytozoon was basal in this tree. The next clade to diverge was that of the Haemoproteus species. The remaining genera lay within the currently established genus Plasmodium. The authors suggested that the origin of the Plasmodium/Hepatocystis clade was likely to have been in Africa.

Within this genus the first to diverge were the avian and reptile species. The next clade to diverge was that of the Polychomophilus species. This was followed in branching order by the Nycteria species. The subgenus Laverinia was the next to diverge followed by the subgenus Vinckeia. The crown of the tree was formed by the subgenus Plasmodium and the genus Hepatocytis. This tree did not support the inclusion of P. ovale in the subgenus Vinckeia but agreed with previous analyses suggesting that P. malaria is more closely related to the Asian clade than P. ovale is. Several of the bat infecting Plasmodium species appear to be related to the rodent species.

Bats appear to have evolved ~66 million years ago in Africa[14] which - assuming that the phylogenetic tree in Schaer et al is correct - places an upper limit on the date for the evolution of the mammalian species of Plasmodium.

Another study of the genera Leucocytozoon, Haemoproteus, Parahaemoproteus, Polychromophilus and Plasmodium found that Leucocytozoon occupied a basal position and that Polychromophilus and Plasmodium were sister clades.[15]

A study of Polychromophilus species found that this genus lies within the avian/reptile clade of Plasmodium species.[12]

A study of mitochondrial, plastid and nuclear genes of the species Plasmodium odocoilei suggests that this species is actually two species that dierged between 2.3 million years ago and 6 million years ago.[16]The phyogenetic tree suggests that the genus Nycteria belongs in a clade that contains the lizard and bird species, that Polychromophilus form a clade with P. odocoilei and that Hepatocystis species in bats forms a clade with the primate and rodent species. It also suggests that the closest relation to Plasmodium - other than Nycteria, Polychromophilus and Hepatocystis - is the subgenus Parahaemaproteus and that this sugbenus is more closed related to Plasmodium that to the genus Haemoproteus. This study suggests that the subgenus Vinkeia is now in need of revision.

Another paper suggests the transfer of the ancestor of Plasmodium from lizards to bats without passage via birds.[17]

A study of Nycteria suggests that Leukocytozoon is basal, followed by Heamoproteus.[18] The sister group to Plasmodium/Nycteria/Polychromophilus/Hepatocystis is Paraheamaproteus. Hepatocystis appears to be a derived clade arising from with the subgenus Plasmodium. Polychromophilius is more closely related to the bird/lizard group than to the mammal infecting species. Nycteria is the sister taxon to the genus Plasmodium.

Possible evolution

The evidence is suggesting the following evolutionary scenario: Plasmodium evolved from a Leucocystis like ancestor. This ancestor gave rise to the subgenus Parahaemoproteus. Both of these taxons infect birds. Plasmodium evolved from its Parahaemoproteus ancestor when it gained the ability to infect lizards. After this Plasmodium diverged into a mammal infecting clade and a bird/lizard infecting clade. Within the bird/lizard clade some species developed the ability to infect bats (Nycteria). Within the mammalian clade a number of species have develope the ability to infect bats (Hepatocystis). Since Haemoproteus evolved after the evolution of birds this would suggest that an upper limit for the evolution of this genus is approximately 66 million years ago. The Columbidae - hosts of the Haemoproteus species - evolved in South East Asia. It is posisble that this also was the origin of the genus Haemoproteus.

This upper limit may be further reduced. The genus Leucocytozoon is thought to have evolved in the Oligocene.[19] This would place an upper limit of 33.9 million years ago for the evolution of the genus Leucocytozoon. This is in agreement with an estimate of the time of the basal radiation of the genus Plasmodium.[20] This date of origin lies within the range of other estimates suggesting that it is plausible. This suggestion is supported by other analyses.[21]

Relations with non Haemosporidian genera

The Piroplasma are usually considered to be the closest relations to the Haemosporidians. Based on the evolution of their vectors (ticks) may have evolved ~300 million years ago.[22] The vectors of Babesia and Theileria - ticks - evolved 350 million years ago ± 23 million years ago.[23] The hard (Ixodidae) and soft bodied (Argasidae) ticks diverged 290 million years ago± 23 million years ago. The most likely place of origin of the ticks is Northern Gondwana and most probably within the region that now constitutes Eastern Africa.

A molecular Bayesian study of Babesia and Theileria species along with Plasmodium species suggests that Babesia and Theileria are sister clades and that they diverged from Plasmodium ~56.5 million years ago (95% credible interval: 86.9 million years ago - 28.2 million years ago)[24] The dating in this study used a date of 12.5 million years ago for the origin of the genus Plasmodium.[25] The authors also estimated that Theileria evolved 23.38 million years ago (95% crdibile interval 11.1 million years ago – 36.7 million years ago) and that Babesia evolved 25.7 million years ago (95% credible interval 12.8 million years ago–40.7 million years ago)

Another analysis suggests that Babesia and Theileria are more closely related to the adeleid species than to Plasmodium.[26]

An examination of sequences from Babesiidae, Cryptosporiidae, Eimeriidae, Plasmodiidae, Sarcocystiidae, Theileriidae, a Perkinsus species and 2 dinoflagellates suggests that Plasmodium and Cryptosporidium are sister taxa and that Hepatozoon is basal to them.[27]

Morrison has shown using molecular data that the Haemosporidia are nested within the gregarines and that this clade is distinct from the piroplasms.[28] This latter clade is a sister group of the coccidians.

Examination of the actin genes suggests that Plasmodium is more closely related to the coccidians than to the Babesia/Theileria clade.[29] It also suggests that Cryptosporium is basal in the Apicomplexa: this latter finding is consistent with other analyses.

Phylogenetic trees

A number of useful phylogenetic trees of this genus have been published:

Tree of Life website
American Museum of Natural History
PLOS site
Paper on Plasmodium
Paper on Plasmodium
Paper on Plasmodium
Paper on Plasmodium

From these trees it is clear that:

The bird and lizard species are intermixed as previously found.

An analysis of the rodent genera (Plasmodium berghei, Plasmodium chabaudi, Plasmodium vinckei and Plasmodium yoelii) suggests that these species may actually be species complexes.[32] The separation of P. chabaudi and P. vinckei has been estimated to be between 3 million years ago and 13 million years ago while that of P. berghei and P. yoelii has been placed at 1 million years ago and 6 million years ago.

A paper that included five unnamed lemur species suggested that P. ovale is more closely related to the lemur species than to the other primate ones.[21] It also suggested that the lemur/P. ovale clade is a sister clade of the rodent species. While this is consistent with the placement of the lemur and rodent species in the subgenus Vinckeia it is inconsistent with the current placement of P. ovale within the subgenus Plasmodium. This paper also supports a basal divergence within the mammalian species into the subgenus Laverinia and the others. The subgenera Plasmodium and Vinckeia with the exception of P. ovale appear to be sister clades.

Analysis of the apicoplast genes auggests that P. ovale is related to the rodent species.[33] This is consistent with its relationship with the lemur species in the subgenus Vinckeia.

Other analyses

Examination of the protease gene (SERA) in 18 species[34] has shown that the ancestral state had only a single gene and that gene duplications have occurred in the extant species. This paper confirms the groupings found elsewhere with an Asian clade. The rodent species seem to be more closely related to the Laverania subgenus than does the subgenus Plasmodium.

A deletion mutation of ~100 base pairs including part of the LS1 rRNA gene is found in the sequences of two African species - P. gonderi and an undescribed parasite taken from a mandrill - and 2 Asian species - P. cynomolgi and P. simiovale.[35] This mutation was not found in the other species examined (Leucocytozoon caulleryi, Leucocytozoon sabrazesi, P. bergei, P. chabaudi, P. falciparum, P. floridense, P. gallacium, P. fragile, P. juxtanucleare, P. knowelsi, P. mexicanum, P. reichenowi, P. relictum, P. simiae, P. vivax, P. yoelii and two unnamed Haemoproteus species.) These mutations are rare events and strongly suggests these species are related.

Another paper suggests that after the mammalian-reptile/bird species split that the subgenus Laverina is basal among the mammal species.[36] This study did not include mammalian infecting species other than primate and rodent species and for this reason Laverina may not be as basal as the study suggests. The remaining branching order is consistent with other analyses placing the rodent species as the first branch after the P. falciparum/P. reichenowi clade. It places P. malaria and P. ovale as being more closely related to each other than to P. vivax. This is consistent with the proposed Asian origin of P. vivax.

Although bird malaria species use a variety of mosquito vectors from the genera Aedes, Anopheles, Culex, Culiseta, Mansonia and Psorophora, all mammalian species use vectors only from the genus Anopheles.[37] This host switch seems to have been associated with a specialization with a particular genus of mosquito.

The ability to store haemozoin appears to have evolved only once in the common ancestor of Haemoproteus, Hepatocystis and Plasmodium.[37]

A study of the relationships between Haemocystis, Haemoproteus, Leucocytozoon and Plasmodium suggests that (1) Leucocytozoon is basal (2) Haemoproteus is a sister clade to the remainder (3) Parahaemoproteus is a sister to Plasmodium and (4) Haemocystis is nested within Plasmodium.[37] As before the bird/lizard species form a distinct clade.

In birds the Haemoproteus and Leucocytozoon species rarely change transmission area.[38] These parasites are restricted to one resident bird fauna over a long evolutionary time span and are not freely spread between the continents with the help of migratory birds. Lineages of the genus Plasmodium in contrast seem more freely spread between the continents. This suggests that the origin on the genus Plasmodium may have coincided with the ability to transfer between avian hosts more easily than the other genera.

Molecular clock estimates

All dates estimated so far using a molecular clock should probably be regarded with some suspicion given the existing disagreements between the various authors.

The branching order suggested by other analyses concurs with an analysis of the mitochondrial genes[39] This latter paper puts the divergence between the reptile-bird and mammal clades at 38.4 million years ago ± 3.2 million years ago (Mya). Other divergence times reported include

An estimate of the dates of evolution of several species[40] using the date of separation of the African species P. gonderi and the Asian clade at 10 million years ago gives estimates as follows:

Analysis of 45 single copy nuclear genes from eight species (P. berghei, P. chabaudi, P. falciparum, P. gallinaceum, P. knowlesi, P. reichenowi, P. vivax, P. yoelii) using several different phylogenetic methods suggest a divergence date between Theileria and Plasmodium between 294 million years ago and 314 million years ago.[41] Estimates of the mutation rates suggest a date of divergence between P. falciparum and P. reichenowi between 5 million years ago and 7 million years ago.

The estimated date of divergence between P. vivax and P. knowlesi was between 15 million years ago and 46 million years ago. This latter period coincides with the radiation of the Old World monkeys which these parasites infect. The date of divergences between P. berghei, P. chabaudi and P. yoelii was estimated to be between 34 million years ago and 25 million years ago. The main radiation of the rodent family Muridae occurred ~24 million years ago.

A paper based on the analysis of 22 nuclear genes suggests a radiation of malarial parasites within the Oligocene (34-23 million years ago).[20]

Another paper[39] examining the dates of evolution using the concatenated sequences of the cytochrome c oxidase III, cytochrome c oxidase I and cytochrome b genes - all from the mitochondrion - suggested the following dates for the evolution of the species examined (P. coatneyi, P. cynomolgi, P. falciparum, P. fieldi, P. fragile, P. gonderi, P. hylobati, P. inui, P. knowlesi, P. malariae, P. ovale, P. reichenowi, P. simiovale, P. vivax) was as follows:

Asian-African primate clade divergence: 12 million years ago-19 million years ago

Primate-rodent clade divergence: 15 million years ago-30 million years ago

Reptile/bird-mammal clade divergence: 20 million years ago-30 million years ago

An estimation of the date of evolution of this genus based upon the mutation rate in the cytochrome b gene places the evolution of P. falciparum at 2.5 million years ago.[25] The authors also estimated that the mammalian species of this genus evolved 12.8 million years ago and that the order Haemosporida evolved 16.2 million years ago. While the date of evolution of P. falciparum is consistent with alternative methods, the other two dates are considerably more recent than other published estimates and probably should be treated with caution.

Another paper which examined primate, rodent, lemur, bird and reptile species suggests that the genus originated between 30 million years ago and 50 million years ago.[21] The split between the reptile/bird and mammalian species occurred between 31.4 million years ago and 47.6 million years ago. The first division in the mammalian species was between Laverinia and the others species. The separation of P. falciparum and P. reichenowi was estimated to be between 3.6 million years ago and 7.9 million years ago. The bonobo strains of P. falciparum of were the closest relations to those of humans. This analysis grouped P. ovale with the lemur species and this clade as a sister clade to the rodent species. While this is consistent with the current placement of the lemur species with the rodent species in the subgenus Vinckeia, it is inconsistent with the current placement of P. ovale in the subgenus Plasmodium. The date of separation of P. ovale from the lemur species was estimated to be 25 million years ago and 35 million years ago and their date of divergence from the rodent species was dated to between 30 million years ago and 50 million years ago. The rodent species first diverged between 10 million years ago and 20 million years ago. P. atherui appears to be more closely related to the P. berghei/P. yoelli clade than to P. chabaudi. P. malariae evolved between 20 million years ago and 30 million years ago and is more closely related to P. vivax than to P. ovale. P vivax and P. cynomogli last shared an ancestor between 2.2 million years ago and 4.5 million years ago. The origin of the Asian clade was placed between 5 million years ago and 8.2 million years ago.

Another estimate of the dates of evolution[42] has proposed that the mammalian Plasmodium parasites originated over 64 million years ago and that split between P. falciparum and P. reichenowi occurred 3.0-5.5 million years ago.

Another study has placed the evolution of the subgenus Laverina between 3.09 million years ago and 22.93 million years ago.[43] The same paper estimated the P. billbrayi - P.gaboni split between 1.92 million years ago and 4.69 million years ago and the P. reichenowi - P. falciparum between 4.02 million years ago and 7.84 million years ago.

Bats evolved between 51.5 million years ago and 75.3 million years ago[44] Since it appears that the mammalian infecting Plasmodium species evolved from a bat infecting species, this estimate may provide an upper limit for the date of evolution of these species of Plasmodium. A larger study suggests that bats evolved 58.9 million years ago[45] This upper limit for the date of bat infecting parasites is consistent with the estimates of the dates of evolution of the mammalian infecting Plasmodium species.

The divergence of Old World monkeys and apes has been dated to 25 million years ago to 30 million years ago.[46][47] Since the subgenus Laverinia infects apes rather than monkeys, this date suggests an upper limit for the evolution of this subgenus. This date also places an upper limit on the date when the species infecting Old World monkeys evolved.

Laverania

Four species (P. billbrayi, P. billcollinsi, P. falciparum and P. reichenowi) form a clade within the subgenus Lavernia. This subgenus is more closely related to the other primate species than to the bird species or the included Leuocytozoon species. Both P. billbrayi and P. billcollinsi infect both the chimpanzee subspecies included in this study (Pan troglodytes troglodytes and Pan troglodytes schweinfurthii). P. falciparum infects the bonbo (Pan paniscus) and P. reichenowi infects only one subspecies (Pan troglodytes troglodytes). Caution has been raised about the adequacy of the description of these new species.[48]

A report of a new species that clusters with P. falciparum and P. reichenowi in chimpanzees has been published, although to date the species has been identified only from the sequence of its mitochondrion.[49] Further work will be needed to describe this new species, however, it appears to have diverged from the P. falciparum- P. reichenowi clade about 21 million years ago. A second report has confirmed the existence of this species in chimpanzees.[50] This report has also shown that P. falciparum is not a uniquely human parasite as had been previously believed. A third report on the epidemiology of P. falciparum has been published.[51] This study investigated two mitochondrial genes (cytB and cox1), one plastid gene (tufA), and one nuclear gene (ldh) in 12 chimpanzees and two gorillas from Cameroon and one lemur from Madagascar. Plasmodium falciparum was found in one gorilla and two chimpanzee samples. Two chimpanzee samples tested positive for Plasmodium ovale and one for Plasmodium malariae. Additionally one chimpanzee sample showed the presence of P. reichenowi and another P. gaboni. A new species - Plasmodium malagasi - was provisionally identified in the lemur. This species seems likely to belong to the Vinckeia subgenus but further work is required.

A study of ~3000 wild ape specimens collected from Central Africa has shown that Plasmodium infection is common and is usually with multiple species.[52] The ape species included in the study were western gorillas (Gorilla gorilla), eastern gorillas (Gorilla beringei), bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). 99% of the strains fell into six species within the subgenus Laverina. P. falciparum formed a monophyletic lineage within the gorilla parasite radiation suggesting an origin in gorrilas rather than chimpanzees.

It has been shown that P. falciparum forms a clade with the species P. reichenowi.[53] This clade may have originated between 3 million years ago and 10000 years ago. It is proposed that the origin of P. falciparum may have occurred when its precursors developed the ability to bind to sialic acid Neu5Ac possibly via erythrocyte binding protein 175. Humans lost the ability to make the sialic acid Neu5Gc from its precursor Neu5Ac several million years ago and this may have protected them against infection with P. reichenowi.

Another paper has suggested that the P. falciparum isolates found in apes are derived from humans and that P. falciparum and P. reichenowi diverged when humans and chimpanzees/gorillas did (between 5 million years ago and 7 million years ago).[54]

It is considered that P. falciparum in humans originated from a single transmission event and that the great apes do not represent a potential reservoir for on going transmission.[55]

The origin of P. falciparum in humans seems likely to have been from bonobos rather than gorillas or chimpanzees.[36]

Another estimate of the most recent common ancestor of the extant strains that has been published is 452,000 years ago.[56]

A review of this subgenus has been published[57] Based on the analysis of the cytochrome b gene the relationships in this subgenus appear to as follows: P. falciparum and P. reichenowi are sister species. Their closest relation is P. billcollinsi. P. gaboni and P. billbrayi are sister species whose closest relation is P. gora. P. gorb is more closely related to the P. falciparum/reichenowi/billcollinsi clade than the P. gaboni/billbrayi/gora clade. This putative taxonomy will need confirmation from other DNA studies. A second study seems to confirm this proposed grouping.[58]

The dates of the evolution of the species within the subgenus Laverania have been estimated as follows:[36]

Another estimate using the mutation rate (1.2 x 10−8 subsititutions/site/year) of the cytochrome b gene placed the spread of P. falciparum to humans at 365,000 years ago (95% credible interval: 112,000 to 1,036,000 years).[59]

Revised names have been proposed for the P. gora and P. gorb species - Plasmodium blacklocki and Plasmodium adleri respectively.[60] These names were chosen to honour the malariologists Saul Adler (1895–1966) and Donald Blacklock (1879–1953). It has also been proposed that the P. falciparum strains infecting gorillas should be renamed Plasmodium praefalciparum. This proposal appears to have been accepted.[58][61] The species P. billbrayi seems to be synonymous with earlier named P. gaboni.

Host-parasite relations:

It appears that P. falciparum has been introduced into South America on several occasions.[62] The extant strains fall into two clades - one northern and one southern. The most probable origin of these strains is Africa and it seems that they were introduced with the slave trade.

Analysis of 45 single copy nuclear genes from eight species (P. berghei, P. chabaudi, P. falciparum, P. gallinaceum, P. knowlesi, P. reichenowi, P. vivax, P. yoelii) using several different phylogenetic methods suggest a divergence data between 294 and 314 between Theileria and Plasmodium.[41] Estimates of the mutation rates suggest a date of divergence between P. falciparum and P. reichenowi between 5 million years ago and 7 million years ago.

Analysis of polymorphisms in the mitochondrial[63][64] genes suggests a sub Saharan origin for P. falciparum with separate colonisations of Southeast Asia and Oceania. Given the distributions of the other members of Laverinia it seems likely all the known members of this subgenus originated in Africa.

Plasmodium

Colobine and macaque monkeys migrated from Africa into the Eurasian continent 10 and 6 millions of years ago respectively and became the ancestors of the extant Asian Old World monkey species.[65] Asian Old World monkey malaria parasite species infect both colobine and macaque monkeys. The existing divergence between the Asian and African clade of this subgenus seems likely to have been caused by intercontinental allopatric speciation along with that of their hosts.

Malaria parasites of the lemurs are not traditionally grouped with the subgenus Plasmodium being placed rather within subgenus Vinckeia. This classification may not be correct.[66] Based on an analysis of the mitochondria, these parasites seem to group with the others infecting primates. The origin of the primate infecting species (excluding those in the Laverina subgenus) may date back to the Eocene - a time when the primate radiation began. This analysis also suggests that the species infecting gorillas and humans may have originated in chimps.

Plasmodium: Asian clade

At least nine species belong to the 'Asian' clade of Plasmodium. These species include Plasmodium coatneyi, Plasmodium cynomolgi, Plasmodium fieldi, Plasmodium fragile, Plasmodium inui, Plasmodium hylobati, Plasmodium simiovale, Plasmodium simium and Plasmodium vivax.

As a rule (with the noticeable exception of P. knowesli), the Asian species have a 72-hour intra erythroctytic life cycle.

Analysis of the merozoite surface protein in ten species of the Asian clade suggest that this group diversified between 3 and 6.3 million years ago - a period that coincided with the radiation of the macques within South East Asia.[67] The inferred branching order differs from that found from the analysis of other genes suggesting that this phylogenetic tree may be difficult to resolve. Positive selection on this gene was also found.

In an analysis of the SSU rRNA gene it was found that all Asian simian Plasmodium species have a single S-type-like gene and several A-type-like genes.[68] A 50 residue insertion in the V7 variable region near the stem 43 is shared exclusively by the S-type like sequences of the Asian simian Plasmodium species and the S- and O-type sequences of P. vivax. This is consistent with their shared ancestry.

Plasmodium vivax may have originated in Asia and the related species Plasmodium simium appears to be derived through a transfer from the human P. vivax to New World monkey species in South America. This was proposed in a study of howler monkeys near São Paulo, Brasil.[69]

Another paper has suggested an African origin for P. vivax.[70]

Time to most recent common ancestor

P. vivax appears to have evolved between 45,000 and 82,000 years ago from a species that infects south east Asian macques.[71] This is consistent with the other evidence of a south eastern origin of this species. A second estimate put the earliest date of the evolution of P. vivax at 265,000 years.[72]

An estimate of the date of origin of P. vivax has placed it at 768,000 years ago.[56]

An estimate of the time of origin of P. vivax based on nuclear genes suggests that it originated between 232,228 to 303,030 years ago.[73] It may have appeared in India between 79,235 and 104,008 years ago.

A study of P. vivax in the Americas suggests that the strains in Venezuela and northeastern Brazil diverged from the others ~30,000 years ago.[74] This separation may have occurred before the parasite was introduced into South America.

The most recent common ancestor of the extant P. knowlesi strains has been estimated to have appeared 257,000 (95% credibility interval 98,000–478,000) years ago.[40] P. knowlesi underwent a rapid population growth between approximately 30,000 and 40,000 years ago. This era follows the growth in the human population in this area (~50,000 years ago).[75]

Branching order

P. coatneyi and P. inui appear to be closely related to P. vivax.[30]

P. vivax and P. knowesli appear to have diverged 25–30 million years ago.[54]

P. gonderi appears to be basal in this clade.[76] This is consistent with its African distribution rather than the mainly Asian distribution of the other species in this group.

Several of the 'Asian' clade - Plasmodium coatneyi, Plasmodium cynomolgi, Plasmodium fragile, Plasmodium inui, Plasmodium fieldi, Plasmodium hylobati, Plasmodium inui, Plasmodium knowlesi and Plasmodium simiovale and an African species Plasmodium gonderi - have a single S-type-like gene and several A-type-like genes. It seems likely that these species form a clade within the subgenus Plasmodium.

The 'Asian' species form a clade with P. simium and P. vivax being clearly closely related as are P. knowseli and P. coatneyi and P. fragile;[76] similarly P. brazillium and P. malariae are related. P. hylobati and P. inui are closely related. P. fragile and P. gonderi appear to be more closely related to P. vivax than to P. malariae.

An analysis of four apicoplast genome-encoded genes (small subunit rRNA, large subunit rRNA and caseinolytic protease C) of nine 'Asian' species (P. coatneyi, P. cynomolgi, P. fieldi, P. fragile, P. hylobati, P. inui, P. knowlesi, P. simiovale and P. vivax) and the African species P. gonderi suggests that P. coatneyi and P. knowlesi are closely related and that P. fragile is the species most closely related to these two.[77] Also P. vivax and P. cynomolgi appear to be related.

The pattern emerging from this data suggests that the ancestor of P. gonderi and the 'Asian' clade (P. coatneyi, P. cynomolgi, P. fieldi, P. fragile, P. hylobati, P. inui, P. knowlesi, P. simiovale and P. vivax) infected a primate host - perhaps the ancestor of the extant rhesus monkey - and migrated with its vertebrate host from Africa to Asia via the Middle East. The Asian branch then gave rise to several clades - P. fragile-P. coatneyi/P. knowlesi, P. hylobati/P. inui and P. cynomolgi - P. simium/P. vivax. P. fieldi, P. simiovale and P. vivax appear to be relatively early diverging species within this clade.[76] P. fieldi and P. simiovale appear to be each other's closest relations.

A summary of the currently understood branching order is as follows:

This branching order may have to be revised as more data becomes available. The timing of these events is still rather uncertain.

The African species P. georgesi appears to be a close relation of P. gondori.

Another paper suggests that P. coatneyi and P. knowlesi are sister species while P. hylobati and P. inui are also sister species.[36] This analysis supports the grouping of P. fieldi and P. semiovale as sister species with their closest relation being P. cynomogli. It also agrees with previous analyses that place P. simium and P. vivax as sister species. It also agrees that P. gondori is the African species most closely related to the Asian clade.

This branching order may have some difficulties. A deletion of the LS1 rRNA gene of P. gonderi P. cynomolgi and P. simiovale has been reported.[35] This mutation was not found in the other species of this group that were examined - P. fragile, P. knowelsi, P. simiae and P. vivax. These mutations are rare and suggest a relationship between the first three species to the exclusion of the others.

Host relations

P. cynomolgi, P. inui and P. knowlesi infect primates of the genus Presbytis.

P. cynomolgi, P. fieldi, P. inui, P. knowlesi and P. semiovale infect primates of the genus Macaca.

P. georgesi and P. gondori infect primates of the genus Cocerebus.

P. gondori infects primates of the genus Mandillus.

Additional species

Within the 'Asian' clade are three unnamed potential species. One infects each of the two chimpanzee subspecies included in the study (Pan troglodytes troglodytes and Pan troglodytes schweinfurthii).[51] These appear to be related to the P. vivax/P. simium clade.

A new species - yet to be formally described - has been reported from orangutans (Pongo pygmaeus) in Indonesia.[21] This species was identified from mitochondrial DNA in the blood of the hosts. It appears to be related to the other members of the Asian clade.

Another as yet unnamed species likely to belong to this group has been identified in the mandrill (Mandrillus sphinx).[35]

Plasmodium: African clade

The species infecting Old World monkeys (subgenus Plasmodium) seem to form a clade.

P. ovale is more closely related to P. malariae than to P. vivax.[76]

Plasmodium ovale has recently been shown to consist of two cocirculating species - Plasmodium ovale curtisi and Plasmodium ovale wallikeri.[78] These two species can only be distinguished by genetic means and they separated between 1 million years ago and 3.5 million years ago. A second estimate has placed the separation of these species at 4.5 million years ago (95% confidence interval 0.7-7.7 Mya)[76]

P. ovale, based on an analysis of the apicoplast genome, appears to be related to the rodent species suggesting an ancestral host switch.[33]

One paper has reported a strain of malaria in a chimpanzee with a mitochondrial sequence identical to that of P. ovale and a second closely related to it.[79] It seems likely as has been proposed earlier that P. ovale may have an animal reservoir.

Two unnamed potential species infect the bonbo (Pan paniscus) and these are related to the P. malariae/P. brazillium clade.

The species P. gonderi appears to be the closest relation to the Asian clade.

Plasmodium malariae

Plasmodium malariae has been considered to be closely related to Plasmodium brasilianum and Plasmodium rhodiani. These species may be a single species with multiple hosts.[80] Because the number of strains that have examined to date remains small, retirement of the brasilianum and rhodiani species names to junior synonym status should probably be delayed.

Rodent species

Although the branching order among the mammalian clades has not yet been determined the branching order in the rodent infections species has been studied.[32][81] The rodent parasites (P. berghei, P. chabaudi, P. vinckei and P. yoelii) seem to form a distinct clade. P. berghei and P. yoelii appear to be sister species as do P. chabaudi and P. vinckei. The separation dates between P. berghei and P. yoelii has been estimated to be 4.5 million years ago (95% credibility interval 2.5 - 6.0); that between P. chabaudi and P. vinckei has been estimated to be 9 million years ago (95% credibility interval 5.5 - 12.6); and that between the P. berghei/P. yoelii and P. chabaudi/P. vinckei clades to be 12.5 million years ago (95% credibility interval 9.0 - 17.5). These estimates are consistent with those from another paper that included a number of primate infecting species.[39]

P. atheruri appears to be the sister species of P. vinckei.[8]

Notes

A recently (2009) described species (Plasmodium hydrochaeri) that infects capybaras (Hydrochaeris hydrochaeris) may complicate the phylogentics of this genus.[82] This species appears to be most similar to Plasmodium mexicanum a lizard parasite. Further work in this area seems indicated.

Unlike other eukaryotes studied to date Plasmodium species have two or three distinct SSU rRNA (18S rRNA) molecules encoded within the genome.[68] These have been divided into types A, S and O. Type A is expressed in the asexual stages; type S in the sexual and type O only in the oocyte. Type O is only known to occur in Plasmodium vivax at present. The reason for this gene duplication is not known but presumably reflects an adaption to the different environments the parasite lives within.

It has been reported that the C terminal domain of the RNA polymerase 2 in the primate infecting species (other than P. falciparum and probably P. reichenowei) appears to be unusual[83] suggesting that the classification of species into the subgenus Plasmodium may have an evolutionary and biological basis.

It is known from many written historical sources that P. vivax malaria was endemic in the wetlands of England from the 1500s until the 20th century.[84] It is suspected that this disease was introduced by the Romans sometime before 400 AD. It seems likely that it remained endemic in these areas at least up to 1000 AD.

A study in Senegal of 25 strains isolated there suggests that P. falciparum underwent a major (60-fold) population expansion of ~20,000-40,000 years ago.[85]

A population study based on isolates from several countries suggests that distinct clustering of continental populations - Africa, Southeast Asia and Oceania - has occurred.[86] Within these grouping there has been some further clustering - West Africa versus East Africa, Thailand versus Cambodia. No distinction was identified between isolates from Mali and Burkina Faso.

Host range

Because of the number of species parasited by Plasmodium further discussion has been broken down into following pages:

Criteria used for speciation

The vertebrate host is the first criterion used for speciation and may be sufficient alone to determine the subgenus as in Ophidiella and Vinckeia. The morphological features of the parasite itself most commonly used to describe a species include the number of pigment granules, the degree of encirclement of the host nucleus, the size of the parasite, the degree of host nucleus displacement and the degree of host cell enlargement.

List of species

Plasmodium accipiteris
Plasmodium achiotense
Plasmodium achromaticum
Plasmodium acuminatum
 Plasmodium adleri
Plasmodium aegyptensis
Plasmodium aeuminatum
Plasmodium agamae
Plasmodium alaudae
Plasmodium alloelongatum
 Plasmodium anasum
Plasmodium anomaluri
Plasmodium arachniformis
Plasmodium ashfordi
Plasmodium atheruri
Plasmodium audaciosum
Plasmodium auffenbergi
Plasmodium aurulentum
Plasmodium australis
Plasmodium attenuatum
 Plasmodium azurophilum
Plasmodium billbrayi
Plasmodium billcollinsi
Plasmodium balli
Plasmodium bambusicolai
Plasmodium basilisci
 Plasmodium beaucournui
Plasmodium beebei
Plasmodium beltrani
Plasmodium berghei
Plasmodium bertii
Plasmodium bigueti
 Plasmodium bioccai
Plasmodium biziurae
 Plasmodium blacklocki
Plasmodium booliati
Plasmodium bouillize
Plasmodium brodeni
Plasmodium brasilianum
Plasmodium brumpti
Plasmodium brygooi
Plasmodium bubalis
Plasmodium bucki
Plasmodium buteonis
Plasmodium caloti
Plasmodium capistrani
Plasmodium carmelinoi
Plasmodium cathemerium
Plasmodium caucasica
Plasmodium cephalophi
 Plasmodium cercopitheci

Plasmodium chabaudi
Plasmodium chiricahuae
Plasmodium circularis
Plasmodium circumflexum
Plasmodium clelandi
Plasmodium cnemaspi
Plasmodium cnemidophori
Plasmodium coatneyi
Plasmodium coggeshalli
Plasmodium coluzzii
Plasmodium colombiense
Plasmodium columbae
Plasmodium cordyli
Plasmodium corradettii
 Plasmodium coturnixi
 Plasmodium coulangesi
Plasmodium cuculus
Plasmodium cyclopsi
Plasmodium cynomolgi bastianelli
Plasmodium cynomolgi ceylonensis
Plasmodium cynomolgi cynomolgi
Plasmodium dherteae
Plasmodium diminutivum
 Plasmodium diploglossi
Plasmodium dissanaikei
Plasmodium dominicana
Plasmodium dorsti
Plasmodium draconis
Plasmodium durae
Plasmodium egerniae
Plasmodium elongatum
Plasmodium eylesi
Plasmodium fairchildi
Plasmodium falciparum
Plasmodium fallax
Plasmodium fieldi
Plasmodium fischeri
Plasmodium foleyi
Plasmodium formosanum
Plasmodium forresteri
Plasmodium floridense
Plasmodium fragile
Plasmodium gaboni
Plasmodium gabaldoni
Plasmodium garnhami
Plasmodium gallinaceum
Plasmodium gemini
Plasmodium georgesi
Plasmodium ghadiriani
Plasmodium giganteum
Plasmodium giovannolai

Plasmodium ginsburgi
Plasmodium girardi
Plasmodium globularis
Plasmodium gologoense
Plasmodium golvani
Plasmodium gonatodi
Plasmodium gonderi
Plasmodium gracilis
Plasmodium griffithsi
Plasmodium guangdong
Plasmodium gundersi
Plasmodium guyannense
 Plasmodium heischi
Plasmodium hegneri
Plasmodium hermani
Plasmodium heroni
Plasmodium heteronucleare
Plasmodium hexamerium
Plasmodium hispaniolae
Plasmodium hoionucleophilum
Plasmodium holaspi
Plasmodium holti
Plasmodium homocircumflexum
Plasmodium homopolare
Plasmodium huffi
Plasmodium hydrochaeri
Plasmodium hylobati
Plasmodium incertae
Plasmodium icipeensis
Plasmodium iguanae
Plasmodium inopinatum
Plasmodium inui
Plasmodium japonicum
Plasmodium jeanriouxi
Plasmodium jefferyi
Plasmodium jiangi
Plasmodium josephinae
Plasmodium joyeuxi
Plasmodium juxtanucleare
Plasmodium kempi
Plasmodium kentropyxi
Plasmodium knowlesi knowlesi
Plasmodium knowlesi edesoni
Plasmodium koreafense
 Plasmodium lacertiliae
Plasmodium lagopi
Plasmodium lainsoni
Plasmodium landauae
Plasmodium lemuris
Plasmodium lenoblei
Plasmodium lepidoptiformis
Plasmodium lionatum
Plasmodium lophurae
Plasmodium loveridgei
Plasmodium lucens
Plasmodium lutzi
 Plasmodium lygosomae

Plasmodium mabuiae
Plasmodium mackerrasae
Plasmodium mackiei
Plasmodium maculilabre
Plasmodium maior
Plasmodium majus
Plasmodium malagasi
Plasmodium malariae
Plasmodium multivacuolaris
Plasmodium marginatum
 Plasmodium matutinum
 Plasmodium megaglobularis
Plasmodium megalotrypa
Plasmodium melanoleuca
Plasmodium melanipherum
 Plasmodium merulae
Plasmodium mexicanum
Plasmodium michikoa
Plasmodium minasense
Plasmodium minuoviride
 Plasmodium modestum
Plasmodium mohammedi
Plasmodium morulum
Plasmodium multiformis
Plasmodium narayani
Plasmodium necatrix
Plasmodium neusticuri
Plasmodium nucleophilium
Plasmodium octamerium
Plasmodium odocoilei
Plasmodium ovale curtisi
Plasmodium ovale wallikeri
Plasmodium pachysomum
Plasmodium paddae
Plasmodium papernai
Plasmodium parahexamerium
Plasmodium paranucleophilum
Plasmodium parvulum
Plasmodium pedioecetii
Plasmodium pelaezi
Plasmodium percygarnhami
Plasmodium pessoai
Plasmodium petersi
 Plasmodium pifanoi
Plasmodium pinotti
Plasmodium pitheci
Plasmodium pitmani
Plasmodium polare
Plasmodium polymorphum
Plasmodium pulmophilium
 Plasmodium pythonias
Plasmodium quelea
Plasmodium reichenowi
 Plasmodium relictum
Plasmodium reniai

Plasmodium rhadinurum
Plasmodium rhodaini
Plasmodium robinsoni
Plasmodium rousetti
Plasmodium rousseloti
Plasmodium rouxi
Plasmodium sandoshami
Plasmodium sasai
Plasmodium saurocaudatum
Plasmodium schwetzi
Plasmodium sergentorum
Plasmodium scelopori
Plasmodium scorzai
Plasmodium semiovale
Plasmodium semnopitheci
Plasmodium silvaticum
Plasmodium simium
Plasmodium simplex
Plasmodium smirnovi
Plasmodium snounoui
Plasmodium stellatum
Plasmodium stuthionis
Plasmodium tanzaniae
Plasmodium tenue
Plasmodium tejerai
Plasmodium telfordi
Plasmodium tomodoni
Plasmodium torrealbai
Plasmodium toucani
Plasmodium traguli
Plasmodium tranieri
Plasmodium tribolonti
Plasmodium tropiduri
Plasmodium tumbayaensis
Plasmodium tyrio
Plasmodium uilenbergi
Plasmodium uluguruense
Plasmodium uncinatum
Plasmodium unalis
Plasmodium uzungwiense
Plasmodium watteni
Plasmodium wenyoni
Plasmodium vacuolatum
Plasmodium valkiunasi
Plasmodium vastator
Plasmodium vaughani
Plasmodium vautieri
Plasmodium venkataramiahii
Plasmodium vinckei
Plasmodium vivax
Plasmodium volans
Plasmodium voltaicum
Plasmodium wenyoni
Plasmodium yoelii
Plasmodium youngi
Plasmodium zonuriae

Unnamed species

At least one species has been isolated from the mandrill (Mandrillus leucophaeus) that awaits full publication. It is currently known as Plasmodium sp. DAJ-2004.

At least one species related to P. ovale appears to be present in chimpanzees. It is known only from a DNA sequence and awaits description.

P. vivax strains can be separated into two distinct types depending on the organisation of the A and S rRNA genes.[87] A gene conversion occurred in an Old World strain and this mutated strain give rise to a new calde of parasites in the New World. The Old World strains were subsequently re introduced - possibly via the slave trade - and these are related to the monkey parasite P. simium. The specific name Plasmodium collinsi has been proposed for the New World strains but this has not yet been accepted.

A second mutation is present in the ORF 470 gene of the plasmid in the New World P. vivax strains. This protein is highly conserved. In the Old World strains of P. vivax and its relations a valine is present. In the New World strains this residue has been replaced by an isoleucine (G -> A in the first codon position).

Two separate strains of P. vivax can be identified on the basis of the circumsporozoite protein (CSP) gene.[88] Both of these alleles can be found in P. simium and they occur both in the New and Old Worlds. This suggests a complex history of transmission across the world and between species.

Another as yet unnamed species was isolated from humans in Madang, Papua New Guinea in 1993.[89] This species differed immunologically and genetically from then generally recognised species infecting humans. Additional isolates of this putative species were also found in Sepik also in Papua New Guinea, Brazil, Indonesia and Madagascar.[90] The circumsporozoite protein of this species appears to be identical to that of Plasmodium semiovale. At least two species of mosquito Anopheles deaneorum and Anopheles oswaldoi appear to be capable of transmitting this parasite.[91] These reports have not gone unchallenged and the status of this putative species is unclear at present.[92]

Species grouped by subgenus

This listing while currently incomplete will be updated when the relevant information becomes available.

Asiamoeba
Bennetinia
Carinamoeba
Giovannolaia
Haemamoeba
Huffia
Lacertamoeba
Laverania
  • Plasmodium adleri
  • Plasmodium billbrayi
  • Plasmodium billcollinsi
  • Plasmodium blacklocki
  • Plasmodium falciparum
  • Plasmodium gaboni
  • Plasmodium reichenowi
Novyella
Nyssorhynchus
  • Plasmodium dominicum
Ophidiella
Papernaia
Paraplasmodium
Plasmodium
Sauramoeba
Vinckeia

Species subsequently reclassified into other genera

The literature is replete with species initially classified as Plasmodium that have been subsequently reclassified. With the increasing use of DNA taxonomy some of these may be once again be classified as Plasmodium. This appears increasing likely as it has been shown that Hepatocystis and Polychromophilus appear to lie within the genus Plasmodium.

The following species have been classified into the genus Hepatocystis:

The following species have been classified into the genus Haemoemba:

The following species has been classified into the genus Garnia:

The following species has been classified into the genus Fallisia:

The following species has been classified into the genus Polychromophilus:

Species now considered to be junior synonyms

P. osmaniae and P. shortii are currently considered to be junior synonyms of P. inui.

P. inconstans is now regarded as a junior synonym of P. relictum.

Species of dubious validity

The following species that have been described in the literature are currently regarded as being of questionable validity (nomen dubium).

  • Plasmodium adunyinkai
  • Plasmodium bitis
  • Plasmodium bowiei
  • Plasmodium brasiliense
  • Plasmodium brucei
  • Plasmodium bufoni
  • Plasmodium caprea
  • Plasmodium carinii
  • Plasmodium causi
  • Plasmodium chalcidi
  • Plasmodium chloropsidis
  • Plasmodium centropi
  • Plasmodium danilweskyi
  • Plasmodium divergens
  • Plasmodium effusum
  • Plasmodium fabesia
  • Plasmodium falconi
  • Plasmodium gambeli
  • Plasmodium galinulae
  • Plasmodium herodiadis
  • Plasmodium leanucteus
  • Plasmodium malariae raupachi
  • Plasmodium metastaticum
  • Plasmodium moruony
  • Plasmodium periprocoti
  • Plasmodium pinorrii
  • Plasmodium ploceii
  • Plasmodium struthionis
  • Plasmodium taiwanensis

References

  1. ↑ Ayala S.C. (1978). "Checklist, host index, and annotated bibliography of Plasmodium from reptiles". J. Eukaryot. Microbiol. 25 (1): 87–100. doi:10.1111/j.1550-7408.1978.tb03874.x.
  2. 1 2 Schaer J, Perkins SL, Decher J, Leendertz FH, Fahr J, Weber N, Matuschewski K (2013) High diversity of West African bat malaria parasites and a tight link with rodent Plasmodium taxa. Proc Natl Acad Sci USA
  3. ↑ Zhang ZW, Cheng J, Xu F, Chen YE, Du JB, Yuan M, Zhu F, Xu XC, Yuan S (2011) Red blood cell extrudes nucleus and mitochondria against oxidative stress. IUBMB Life 63(7):560-565. doi:10.1002/iub.490.
  4. ↑ Valkiunas G. (1997). Bird Haemosporidia. Institute of Ecology, Vilnius
  5. ↑ Corradetti, A.; Garnham, P. C. C.; Laird, M. (1963). "New classification of the avian malaria parasites". Parassitologia 5: 1–4.
  6. ↑ Bray R. S. (1958) Studies on malaria in chimpanzees. VI. Laverania falciparum. Am. J. Trop. Med. Hyg. 7(1):20–24
  7. 1 2 Landau I, Chavaite JM, Peters W & Chabaud A (2010) The sub-genera of avian Plasmodium. Parasite 17: 3-7
  8. 1 2 Santiago-Alarcon D, Outlaw DC, Ricklefs RE, Parker PG (2010) Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove. Int J Parasitol 40(4):463-70. doi: 10.1016/j.ijpara.2009.10.003
  9. ↑ Martinsen ES, Waite JL & Schall JJ (2007) Morphologically defined sub-genera of Plasmodium from avian hosts: test monophyly by phylogenetic analysis of two mitochondrial genes. Parasitology 134: 483-490
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