HTLV-II and the peopling of America

Map showing HTLV-II in Central Africa. Copyright © 2012 by Austin Whittall

Human T cell leukemia / lymphoma virus (HTLV) is found in four types numbered from one to four, they are closely linked to similar virus found among simians (STLV). Collectively, the HTLV groups and their STLV analogues are called “primate T-lymphotropic viruses” (PTLV).

In today’s post we will focus on the two main HTLVs (they are retrovirus that causes cancer and other disorders). The first of them is known as HTLV-I; it is closely related to a simian virus (STLV-I) and is considered an Old World virus, which has affected both humans and apes in Asia and Africa for milennia. [2]

The other type, HTLV-II is a cosmopolitan endemic illness among Intravenous Drug Users (IUD) all around the world. However, in 1990, it was unexpectedly discovered among an isolated group of American Indians, the Guaymi in Panama and a year later among other native Americans in the US. This came as quite a surprise which is difficult to explain how it could have appeared among separate Amerindian groups.

HTLV-II the American virus

Further research has established that HTLV-II is found among highly separated and often geographically isolated native American groups and this poses a problem because, highly influenced by the prevailing theories, nobody dates the arrival of HTLV-II type to America beyond the established 10,000 - 40,000 years ago that fits the orthodox temporal window for the Asian migration into the New World through Beringia.

As we mentioned above, HTLV-II, is prevalent all across the globe in intravenous-drug users (IUD), and the dispersal they caused is a very recent event. They surely picked up the infection sharing needles with Native Americans in the US, however the point of origin is not yed defined.

The interesting part is that prior to IUD dispersal, HTLV-II was only found in America, where two (actually three) subtypes can be found:

• HTLV-IIa is only found exclusively among some groups of American Indians such as the American Indian tribes of North, Central, and South America, including the Navajo and Pueblo in New Mexico and the Kayapo, Kraho, and Kaxuyana in Brazil. (this endemic Brazilian Amazonian subcluster is slightly different and have been designated as HTLV-IIc[1], it may differ due to a founder effect and is intimately linked to the original Paleo Indians who peopled the region.[10]
• HLTV-IIb is the other strain which is also found exclusively among Amerindians: Guaymi in Panama, the Wayu and Guahibo in Colombia, the Toba and Mataco in Argentina, and some Navajo and Pueblo in New Mexico. It is known as the “Paleo Indian strain” [7] [1]

As it was found among isolated Amerindian groups, and at high frequencies, initially the HTLV-II virus was thought to have originated in America. However, and this is another surprising fact, the virus is also present among Pygmies in Africa.

The fact that there are two reservoirs of HTLV-II, one in indigenous American populations and the other in African pygmies, groups which are as far apart within H. sapiens as one can find, is indeed a deep mystery.

The Pygmy connection: Africa

Besides infecting Pygmies, there is also an African simian virus very similar to HTLV-II that affects bonobos (a relative of the chimpanzees). This may indicate an African origin for the human virus, derived from the simian one. Furthermore, HTLV-IIb is found among Cameroonian Pygmy people but has very close phylogenetic relation with Amerindian HTLV-2b strains. [1].

The strains are “highly similar to each other (below 1% nucleotide divergence) , as well as to Amerindian HTLV-2b strains”[9]; a molecular clock analysis indicates that it has been endemic among the Bakola Pygmies for “a long time”.[9]

The HTLV-b strain has also been found in a non-Pygmy Gabonese family. If we cannot rule out some transoceanic contact with Paleoindians, then this virus must have originated in Africa [7]. We will look into this later (see below: Conclusions).

There is also another strain, HTLV-IId discovered among the Congolese Efe Pygmy (Bambuti Pygmies), a group which is not very admixed with other groups and are considered one of the oldest African people.[1]

So, we have two distinct groups of Pygmies infected with two different subtypes of HTLV-II, the Bambuti and the Bakola, each located at the extreme eastern and western points of the Pygmy territory. These are people which are completely different from their neighbors with whom they do not mix and have been separated from them for ten to twenty thousand years . Their isolation and lack of admixture means that they must be an ancient reservoir of the HTLV-II virus. [7]

The paper that deals with the Pygmy strain of HTLV-IId, [1], states that as the closest simian virus is found among the bonobos in Africa, the human strain must have originated there too, remained in Africa and, had the “longest independent evolution” among al HTLV-II strains. It goes on and says that the other two strains reached America on human hosts[1], in two different “waves” [7].

We will look into this assertion later (see below: Conclusions)

But, and this is an interesting question: How did HTLV-2 reach America? And why are there two varieties (“a” and “b”) found in America? There is no evidence of HTLV-II in Asia, the route upheld by orthodox science as the one taken by modern humans “Out Of Africa”, across Asia and through Beringia into America. I will try to answer both below.

To clarify the picture, the following figure, (from [10]) shows the different HTLV-II strains:

• HTLV-IIa (Amerindians) in Yellow
• HTLV-IIb (Amerindians) in Green. IUDs not shaded; cosmopolitan distribution
• HTLV-IIc (Amazonian strain) is shown in blue.

Pygmies are highlighted with an arrow, the “b” and “d” subtypes. And also an “a” type. Which I had not found mentioned in the bibliography.

From Fig 2 [10].

In America but not in Asia how can that be?

Assuming that the contemporary Asian descendants of the humans who peopled America had HTLV-II, a group of scientists [2] sampled 778 Siberians in 1993 at Tchoukotka and Sakhalin island and at other Northern Siberian populations. The sampling spanned a wide range of ethnic groups: Tchouktche, Nivkh, Evene, Yakoute, Eskimo, Russians, Dogen, Orok, Nganas, Evenke, Nenetse, and various other ethnic origins, surprisingly, not one of them was HTLV-II positive. A similar finding was reported by Neel et al. (1994) (sample n=473). [2]

Trying to explain this odd situation that defies the logic of the Beringian entry into America, the authors suggested several possible explanations:

• the sample did not cover groups that had the virus.
• A founder effect (population bottle neck that wiped out those carrying the original virus).
• The extant population contains only a small proportion of the ancient mongoloid group that peopled America (and had the virus).
• The virus disappeared due to a drop in transmission rate caused by (unexplained) cultural and / or environmental changes. [2]

The final and most likely probable cause given was that the current Siberians are not related to the group that peopled America and hence, don’t have the virus.[2]

In no other part of Asia has the HTLV-II virus been found with the exception of a single report of HTLV-IIa serological profiles in three Mongolian women, which was reported in a 1994 Annual Meeting of Virologists (W.W. Hall et al. 1994). [3]

However this finding was not printed later in any journal and, the author professor Hall, who is a world authority on HTLV-II, did not mention the issue again in the 18 years that have gone by since then.

Hall has recently studied HTLV infections in America and in Asia, his team was, of course, seeking the source of Amerindian HTLV, so knowing that Siberia showed no signs of the virus, “the researchers decided to go to Outer Mongolia” there “Hall's group found HTLV-I among remote peoples in Mongolia, but no HTLV-II. Not finding HTLV-II was significant, as it suggested an American origin [of the virus].” [4], a conclusion that is in contradiction with the Pygmy findings in Africa and the African origin of the virus.

Based on this evidence we can safely conclude that there is no clear proof available on the existence of HTLV-2-like viruses in modern Asian human and nonhuman primates.

So, how did the virus get to America without leaving any traces in modern Asian humans? Furthermore, HTLV-1 is present in Asia and also in America, so the human host who brought it into America managed to live on in Asia with it (in a future post we will take a look at HTLV-1 and the peopling of America). Why did HTLV-2 leave no traces in Asia?

Quick answer: it was not taken there by modern humans but by other now extinct hominids More below, see Conclusions.

It is a matter of Time and divergence

When comparing the different strains of virus, scientists look at the differences (nucleotidic divergence) and take it as an indication of how long they have evolved separately. The more differences, the longer they have been apart.

The divergence between HTLV-IIa and HTLV-IIb is about 4.8%. What can this tell us?

Since the internal divergence of HTLV-IIb between the different Amerindian groups varies from 0 to 0.4%, on an average 0.2%, and these people have been isolated for milennia, a very simple and straightforward calculation (and a very approximate one also) would allow us to calculate that the “a” and “b” strains have been apart for about (4.8/0.2 = 24) twenty four times longer. [7]

Of course, evolution rate may not be constant as time passes (accelerates, decelarates, stops and starts), it may vary along the nucelotide, quicker in some areas, slower in others. This is reflected in the range given for the evolutionary rate in the bibliography: evolutionary rate is estimated at 0.1 to 1% per 1000 years (a tenfold difference). Furthermore, it seems that it may even be lower in populations with predominantly vertical (mother-child) transmission such as Amerindians [8]

Virologists test their divergence estimates against “established” mileposts defined by anthropologists, take this example (from [11]):

”The relaxed molecular clock was calibrated with two independent molecular calibration points; 12,000 – 30,000 ya as confidence intervals for the origin of HTLV-2 as it migrated out of Africa and Asia and into the Americas via the Bering land bridge and 40,000 – 60,000 ya as confidence intervals for the origin of HTLV-1 in Melanesia as it became populated with people from Asia... The PTLV evolutionary rate assuming the global molecular clock model was estimated by using the divergence time of 40,000 – 60,000 years ago (ya) for the Melanesian HTLV-1 lineage (HTLV-1mel) and 12,000–30,000 ya for the most recent common ancestor of HTLV-2a/HTLV-2b native American strains..."[11]

But what if the clocks are based on incorrect temporal events? Say it was a pre-sapiens hominid who brought the HTLV-II into America long before the 12-30 Kya date? Or if HTLV-1 reached Melanesia in the blood of a H. erectus 1.8 million years ago?

Below are two different examples of the outcome of these divergence estimates and the dates of course differ

1. Divergence of the different HTLV and STLV virus [6]

This paper includes a Figure, shown below, in which the PTLV-1 and PTLV-3 human and simian viruses are intermingled, but the HTLV-2 and STLV-2 have lineages that are clearly separated from each other. [6] Does this reflect that there is no recurrent or repeated cross-infections between species in HTLV-2?

Note the split dates. The split between PTLV-3 and the other two happened between 947 and 632 Kya. HTLV-2 broke off from the simian STLV-2 some 192- 287 Kya, and it was about 579 to 867 Kya that PTLV-1 and PTLV-2 split apart.[6]

PTLV evolution times Fig. 8.2 from [6].

HTLV-II Divergence Tree. Fig 5 from [11].

2. Divergence of the different HTLV and STLV virus [13].

This paper includes several figures all similar (though the exact dates differed slightly) and we have taken one, shown above which depicts the different HTLV and STLV variants and their evolution. The branch lengths are proportional to “median divergence times” in years and the scale at the bottom shows 100,000 years.

It estimates the following dates in years BP: PTLV-4 split from PTLV-2 happened between 49,800 and 378,000 years ago. The PTLV-1 : 54,250 - 75,100 years, PTLV-2: 75,200 -128,600 years, and PTLV-3: 40,850 - 71,700 years.

The dates of examples 1 and 2 differ considerably, so it makes me wonder how reliable are these “clocks” and divergence times. Furthermore, since they are taking the entry date of modern humans into America (12- 30 Kya) as a benchmark to calibrate their clocks, I am even more doubtful about their reliability. As we will see below there is some discrepancy among specilists regarding the divergence dates.

Conclusions, Discussion and possible explanations

Having read all the facts and seen all the data we have to explain the following:

• A virus strain, HTLV-II with three subtypes “a”, “b” and “c” found basically in America (North and South)
• The same virus HTLV-II subtype “b” found among Gabonese and Bakola Pygmies.
• Another unique African strain “d” , apparently the most divergent and therefore ancient, among another group of Pygmies, the Efe or Bambuti.
• No virus (we exclude the recent dispersal by IUDs) anywhere else in the whole world.
• Similar virus in D.R. of Congo Bonobo simians in Africa suggesting an African origin.

First lets take a look at the African “b” Subtype “outliers” the Gabonese and the Bakola Pygmies.

Why are the IIb subtypes from America and the Pygmies so similar?

Long residence in isolated populations such as the Amerindians and the Pygmies should provoke a high level of genetic drift. But, the divergence within IDUs is higher than the one found among the reservoir populations! And “tree branch length of nearly all viral strains within the major groups are short, indicating only a few genetic differences are unique to each strain irrespective of origin.” [13].

This could be explained by “a recent origin of modern day HTLV-II with repeated episodes of intercontinental dissemination” [13] But this option can be discarded based on the unique diversity of subtype IId and STLV-II

But the extreme similarity between strains fouond in Colombia and Cameroon; and Chile and Gabon, show such a small divergence that [13] ”based on the rates of change from IVDU (Salemi et al. 1998a), yields a recent divergence time of 100–400 years ago for the transcontinental strains.”[13] (Below is a link to Salemi’s paper).

In an attempt to circumvent this contradiction some have proposed that coevolution between host and virus in isolated communities is different to the mutation rate of the virus when it enters a new host population such as IDUs (where it evolves faster). Thus mutation rate may be “mutation rate may be orders of magnitude different”[13] (slower) among Amerindians.

I think that the answer is much more simple and straightforward:

The Gabonese and Bakola HTLV-IIb source: Brazil

If we accept Salemi’s time frame of 100 – 500 years BP as the age of HTLV-IIb subtype, and ask ourselves if there is any link between Equatorial Africa and America through which the virus could have moved during that window, we can immediately answer: yes, there was a link: the Atlantic slave trade.

Of the 11 million Africans that were captured, enslaved and ferried across the Atlantic, about 3 to 5 million went to Brazil. This country held the largest slave population in the whole world. These Africans came from the Portuguese setlements in Africa: Mozambique, Angola, Cabinda, Guina Bissau, Cape Vert and other sites along the Gulf of Guinea. Gabon and Cameroon were providers of slaves too.

It is highly probable that the HTLV-IIb strain detected in Gabon, and virtually identical to the Amerindian strains may came from America: Gabon was a source of slaves for the Americas and a coastal settlement set up for this purpose in ths sixteenth century, taking slaves from deep inland and loading them on slave ships. Paradoxically it ended up as Libreville (Freetown), the current capital of Gabon, which housed freed slaves captured by the French navy in the 1840s and grew to become a settlement with freed slaves.[15]

The crew of slave ships could have easily become infected with Amerindian HTLV-II from prostitutes at the South American Ports (Brazil or elsewhere in Spanish America) where they unloaded their human cargo, and taken the virus back with them to Africa on their voyages to pick up more slaves or to trade with goods sent from Brazil to Africa. Similar horizontal transmission from sailors to African prostitutes at the Eastern African slave loading posts would have ensured transmission from one side to the other side of the Atlantic Ocean.

Could the infection have spread to the isolated Bakola Pygmies?

The Bakola Pygmies were not so isolated

The eastern Bakola Pygmies have interacted with the Bantu people along the coastal areas of Congo, Cameroon and Gabon for hundreds of years: ”In fact, unilateral marriage practicesin which Kwassio [ Bantu] men marry Bakola [Pygmy] women, and the children born from suchmarriage, have provided an opportunity for a spatial and temporal developmentof a long standing Bakola /Ngoumba relationship”. [16]

Marriage and the carnal relations it entails are a sure way for horizontal transmission of HTLV-II from coastal groups in touch with slave ship crews and inland Pygmy populations.

Wrap up: Therefore it is plausible therefore that American HTLV-II b subtype virus entred Gabon via slave ship crews and that prostitues in both America and Africa acted as infection routes: in America from Amerindians to sailors and in Africa from sailors to local population. These in turn through marriage infected the Bakola. The recent temporal window suggested for this virus subtype and the homogeinity among the viral strains in disparate locations are thus explained.

The Bambuti Pygmy “d” strain and bonobos

The “d” subtype is very interesting and there are two possible scenarios that can explain its great divergence from the Amerindian strains:

1. Recent origin: “it cannot be excluded that this yet unique HTLV-2 D strain could have been quite recently acquired from a a simian host, implying that its divergence does not reflect a long standing presence in the human host.”[12]. The text cited, speaks for itself. In other words, the apes infected the Bambuti pygmies recently

2. Ancient origin: it could be equally likely that the strain is very old among humans, as can be seen by its great divergence and is closer to the STLV-2 strains. This indicates an ancient origin in Africa.

What cannot be defined however is “whether the virus originated in the bonobo chimps and then infected humans, or if a common ancestor infected both humans and P. paniscus early within type II evolution”.[13]

This is interesting and we will look into it again below.

Why is it not found in Asia?

Quick answer: it was not taken there by modern humans but by other now extinct hominids. Lets elaborate on this:

The classic scenario for the dispersal of HTLV-II is the following: [13]

...type II viruses diverged from a common ancestor with other HTLV/STLV in Africa, and HTLV-II subsequently formed a minimum of three major lineages (IIa, IIb, IId) within Africa. With ancestral human migration events, subtypes IIa and IIb were carried into the New World and segregated among ethnic Amerindian tribes... [13]

This scenario requires two separate waves of ancestral humans taking the two different “a” and “b” varieties of HTLV-2 to America. Which, in my opinion is very complicated, especially since not one member of these waves remained in Asia with the HTLV-II virus in them.

The simple explanation is the following: PTLV-II originated in Africa and infected the bonobos and a group of hominids, perhaps Homo habilis, that preyed on them and got infected. The STLV-II adapted to these hominids and produced an ancestral HTLV strain.

Some of the infected H. habilis moved out of Africa and into Asia, taking the “proto IIC” (yes, “c”) with them. Others remained in Africa, and their HTLV-II would later evolve into the “IId” which died out elsewhere, but survived to infect the Bambuti humans. It is probable that H. habilis was preyed on by groups of H. erectus or other hominds, and that the last relict non “sapiens” hominids infected the Bambutis.

H. habilis bypassed Southern Asia and its simian inhabitants, which is why the Asian apes are not infected. They chose to live in the Caucasus. Their “Georgian” descendants must have pushed on, through an empty Siberia, across Beringia, into America, following their big megafaunal game. The few that remained behind disappeared without a trace and did not infect the hominids that would follow their steps. Or perhaps did, infecting Neanderthals, but since they passed away too, their HTLV-II is lost.

H. erectus who followed them later, chose a southern route (India, Indonesia, China and perhaps Australia), but they were not infected and did not take the virus with them. Perhaps they had HTLV-I, but we will look into that in another post.

Modern humans when they left Africa and entered Asia, were also free of HTLV-II, it remained in a backwater of Congo, tied up in the Bambuti Pygmies.

Modern humans lived in an HTLV-II free Asia!. That is why it has not been detected there.

The Georgians into America across Beringia 1.5 million years ago is a very ancient event, and it surely puts the “genetic clock” used to calculate divergence and evolution of viral strains in another setting. The dates divergence are very likely unreliable.

Highlight. There were no humans in Asia when H. habilis took a proto HTLV-IIa across Siberia and into America.

Cross-species transmission and the PTLV-II anomaly

STLV-1 strains have repeatedly infected human beings and this is the origin of the different subtypes of HTLV-1 found in Africa. The same can be said for the origin of HTLV-3. [11] The source of infection: hunting and eating monkeys, a horizontal prey-primate hunter transmission of a zoonotic infection, and intimate contact with the prey’s body fluids. [11]

Evidence of this is the more than 15 species of Asian and African apes are infected with HTLV-I, and 15 African ones with HTLV-III, your would expect a similar situation with HTLV-II, but no, it has not been detected in any wild apes in Africa, and has only been isolated in pygmy chimpanzees or bonobos (Pan pansicus) housed at the Yerkes National Primate Research Center in the USA but originally captured in the Democratic Republic of Congo [6] (where evidence of STLV-2 among wild bonobos has recently been sugested).[17]

So, beyond the bonobos, no STLV-II virus is found in Africa, this is very different to PTLV-I and III. Why?

The surprising thing is that STILV-II has been found in New World spider monkeys (Atles fusciceps) from Panama. [5] The authors of the paper that discoverd this, cautiously write: “There are several lines of evidence to suggest that the STLV-II isolate described here is a new simian retrovirus closely related to but distinct from HTLV-II...”. They continue and speculate: “New fossil evidence suggests that the time of origin of simian primates may be pushed back into the Paleocene period, which means that direct migration of simians between Africa and South America is more likely...”.

And finally: “HTLV-II infection may be endemic in certain New World aboriginal populations [...] since these Indian tribes are relatively isolated [the infection] may have arisen from close contact with primates....[5]

In other words: Ancient African apes had STLV-II, and that long ago,when South America and Africa were part of a Supercontinent, the virus was present in both groups. Later it evolved and infected Amerindian humans with HTLV-II. This is very unlikely (the similarity between African and American PTLV-II suggests one unique origin and dispersal out of Africa into America in more recent times than the Paleocene.

The more likely situation is that H. habilis entered America (which was free of PTLV-II), and that they infected the spider monkeys.

The Amazonian “IIc” anomaly: it is an ancient strain

We have mentioned at the beginning of this post that HTLV-IIc is included as a subcluster of IIa. What is interesting about “IIc” is that it has a very unusual feature, a protein encoded by its Tax gene (the virus contains this and other genes that modulate viral expression and play an important role in its pathogenesis) is similar to the one encoded by HTLV-IIb but is longer than that of type IIa. On the other hand its env (another gene) and LTR (gene expression control center) strongly resembles type IIa.

A possibility is that the long Tax gene is ancestral and was lost by the IIa subtype but was kept by IIc. Interestingly, the other “ancient” lineages of PTLV-II, the STLV-II and the “IId” variety also have long Tax genes. [13]

Point to remember The Amazonian “IIc” must therefore be older than “IIa” (which surely arose from it), and also older than “IIb”. It is probably as ancient as the “IId” found among the Bambuti Pygmies.

This is logical if you assume that H. habilis brought the proto HTLV-IIC with him into America. It evolved there isolated from the other “d” strain. And originated the “a” and “b” strains, the latter would then infect the newcomer H. sapiens when they reached America, and through them would later return to Africa in the blood of the slave ship crews to infect Gabonese and Bakola Pygmies.

Closing Comments

This has been a very long post, though I sincerely hope it was not a boring one!

What I tried to point out were two things: one, that a hominid other than us, modern humans could have brought HTLV-II into America long before the accepted date of entry (beyond 30 Kya) of humans into the New World. And two, that scientists take this date (30 Kya) as written in stone and calibrate their genetic clocks as well as build complicated theories to avoid going against it other, unconventional yet much more simple explanations such as the one mentioned above (early peopling of America by non-sapiens hominids.

Comments, suggestions, criticism is welcome

Sources

[1] Anne-Mieke Vandamme, et al. (1988). African Origin of Human T-Lymphotropic Virus Type 2 (HTLV-2) Supported by a Potential New HTLV-2d Subtype in Congolese Bambuti Efe Pygmies. J. Virol. May 1998 vol. 72 no. 54327-4340

[2] Gressain, Antoine, et al. (1996). Serological Evidence of HTLV-I But Not HTLV-II Infection in Ethnic Groups of Northern and Eastern Siberia. Journal of Acquired Immune Deficiency Syndromes & Human Retrovirology: 1 April 1996 - Volume 11 - Issue 4 - pp 413,414. Letters to the Editor.

[3]Hall, W. W., S. W. Zhu, P. Horal, Y. Furuta, G. Zagaany, and A. Vahlne., (1994). HTLV-II infection in Mongolia. Abstracts of the Annual Meeting of the Laboratory of Tumor Cell Biology, National Cancer Institute, Bethesda,Md.

[4] Clarie O’ Connell, (2007). UCD virus hunter travels the world seeking answers. Science Spin - January 2007

[5] Chen, Y. M. A., Y. J. Jang, P. J. Kanki, Q. C. Yu, J. J. Wang, R. J. Montali, K. P. Samuel, and T. S. Papas, (1994).Isolation and characterization of simian T-cell leukemia virus type II from New World monkeys. J. Virol. 68:1149–1157

[6] Alexander Voedvodin, Preston Marx, (2009). Simian Virology, Wiley-Blackwell. pp. 197.

[7] Antoine Gessain et al. (1995). Isolation and molecular characterization of a human T-cell lymphotropic virus type II (HTLV-II), subtype B, from a healthy Pygmy living in a remote area of Cameroon: An ancient origin for HTLV-II in Africa. Proc. Natl. Acad. Sci. USA. Vol. 92, pp. 4041-4045, April 1995.

[8] Angus G. Dalgleish. HIV and the New World Viruses pp 308+

[9] Philippe Mauclère (2011). HTLV-2B Strains, Similar to Those Found in Several Amerindian Tribes, Are Endemic in Central African Bakola Pygmies. Journal of Infectious Diseases. Published on behalf of Infectious Diseases Society of America. Volume 203, issue 9, pages 1316-1323

[10] Ethienne Lobato dos Santos et al., (2009). Molecular characterization of HTLV-1/2 among blood donors in Belém, State of Pará: first description of HTLV-2b subtype in the Amazon region Rev. Soc. Bras. Med. Trop. vol.42 no.3 Uberaba May/June 2009

[11] William M Switzer, et al., (2009). Ancient, independent evolution and distinct molecular features of the novel human T-lymphotropic virus type 4. Retrovirology 2009, 6:9 doi:10.1186/1742-4690-6-9.

[12] Thomas Leitner, Ed. The Molecular Epidemiology of Human Viruses. Chapter 7. Gessain A, Meertens L and Mahieux R. Molecular Epidemiology of Human T cell leukemia / lymohoma viruses Type 1 and Type 2...”. pp. 149.

[13]Jill Pecon Slattery, Genoveffa Franchini, and Antoine Gessain, (1999). Genomic Evolution, Patterns of Global Dissemination, and Interspecies Transmission of Human and Simian T-cell Leukemia/Lymphotropic Viruses. Genome Res. 1999. 9: 525-540

[14] Salemi M., Vandamme A.-M., Gradozzi C., Van Laethem K., Cattaneo E., Taylor G., Casoli C., Goubau P., Desmyter J., Bertazzoni U.(1998a) Evolutionary rate and genetic heterogeneity of human t-cell lymphotropic virus type II using isolates from European injecting drug users. J. Mol. Evol. 46:602–611.

[15] P. Hinks, John R. McKivigan,R. Owen Williams. Encyclopedia of Antislavery and Abolition, Volumen 2. pp. 432,

[16] Ngima Mawounga. (2001), The relationship between the Bakola and the Bantu poples of the coastal regions of Cameroon ...". Study Monographs, Suppl.26: 209-235, March 2001 209. pp. 214

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