Evolution of Homo sapiens in Asia: an alternative implication of the “Out-of-Africa” model based on mitochondrial DNA data

doi:10.4236/ns.2010.26072

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Vol.2, No.6, 571-575 (2010) Natural Science

http://dx.doi.org/10.4236/ns.2010.26072

Evolution of Homo sapiens in Asia: an alternative

implication of the “Out-of-Africa” model based on

mitochondrial DNA data

Hiroto Naora

Research School of Biology, The Australian National University, Canberra, Australia; [email protected]

Received 25 September 2009; revised 9 November 2009; accepted 14 January 2010.

ABSTRACT

Cann et al. [1] have claimed on the basis of mi-

tochondrial DNA (mtDNA) data that our direct

ancestral Homo sapiens evolved in the African

continent and spread to other continents, fol-

lowed by the total replacement of the indige-

nous population. Their “Out-of-Africa” model is

based on the assumption that mtDNA inheri-

tance is simply maternal. Recent findings sug-

gest the possibility that in between-population,

e.g. African and Asian, mating, the African pa-

ternal mtDNA was transferred to the egg cell of

an Asian together with Y-chromosomal DNA in

the human past. Considering that Y-chromos-

omal DNA and mtDNA sequences of African

origin coexist together with Asian X-chromos-

omal and autosomal DNA sequences in a cur-

rent Asian, the observations by Cann et al.

suggest the full/near full replacement of mtDNA

in the human past, but do not necessarily imply

the total replacement of indigenous populations

with African migrants.

Keywords: Out-of-Africa Model; Origin of Asian;

Paternal mtDNA Inheritance; mtDNA Transmission/

Recombination

1. INTRODUCTION

Evidence has accumulated that the Homo lineage origi-

nally appeared in Africa, followed by its successful glo-

bal expansion. The view of “Out-of-Africa” that our dir-

ect ancestral H. sapiens evolved in the African continent

and spread to other continents, has been popularly re-

ceived among researchers [1-8]. On the other hand, there

have been significant fossil records in non-African con-

tinents, supporting the “regional continuity” model [9].

This model claims that our direct ancestral H. sapiens

evolved locally in the widespread regions of major con-

tinents, e.g. Africa, Europe and Asia [10-12]. In fact,

morphological continuity in East Asian traits from East

Asian Homo erectus during the middle-late Pleistocene

transition can be seen in these fossil records [12-14].

However, most of these records have neither definitely

refuted nor supported one of the models for or against

the origin of H. sapiens, particularly in Asia. Further-

more, most genetic evidence, such as simulated dendro-

grams, genetic diversity and ancient DNA sequences can

argue for either model of human origin [15].

In 1987, a crucial observation was made by Cann et

al., who examined the human mitochondrial DNA (mt

DNA) diversity of globally dispersed populations. They

concluded that modern humans simply spread to other

continents, e.g. East Asia, from Eastern Africa around

200,000 years to 50,000 years (200 KY to 50 KY) ago,

followed by the total replacement of pre-inhabited in-

digenous populations [1,2]. The “Out-of-Africa” model,

reconstructed with mtDNA data, is primarily based on a

few assumptions. One of the key assumptions is that ani-

mal mtDNA does not undergo homologous recombina-

tion. This is because of past failure to observe the clear

cases of mtDNA recombination in natural populations.

However, recent findings have raised a new insight into

mtDNA inheritance and the behaviours of mtDNA in a

fertilised egg [16,17]. In this study, an attempt was made

to integrate the interdisciplinary information obtained in

the research fields, not only anthropology and mito-

chondrial genetics but also other areas, such as devel-

opmental biology, ecology and social sciences. A meta-

analysis of these findings has raised the need of careful

scrutiny in the interpretation of Cann et al. [1,2].

2. CRITICAL VIEW OF MITOCHONDRIAL

DNA INHERITANCE: STRICTLY

MATERNAL?

Two sibling bat species, European Myotis myotis and

newly migrated M. blythii to Europe from Asia, share

H. Naora / Natural Science 2 (2010) 571-575

572

multiple identical or very similar haplotype in mitocho-

ndrial genomes when they occur in sympasy. However,

they show a strikingly different pattern of nuclear DNA

diversity. On the other hand, allopatric M. blythii in Asia

possesses mtDNA divergent from those of two species in

Europe, postulating that the mtDNA of European M.

blythii has been replaced with that of M. myotis [18].

Similar mtDNA (full/near-full/partial) replacement has

been observed in a wide variety of other species in an

animal kingdom, for example, nematodes [19], molluscs

[20], insects [21], fishes [22] and mammals other than

bats, such as vole [23]. As opposed to the popular belief,

all of these observations suggest that paternal mtDNA

inheritance occurs widely in the animal kingdom. In fact,

paternal mtDNA inheritance has been observed even in

humans [24,25]. At present, no specific information has

been reported, which strongly favours the notion that

these human cases were really exceptional and that hu-

man mtDNA replacement, similar to the cases of Myotis,

has never taken place in evolution when two “sibling”

human populations met and lived in sympasy. Further-

more, evidence has shown that the segregation and

transmission of mtDNA sequences [26-28] play a crucial

role in the inheritance of human mitochondrial diseases

[16].

Molecular and cellular events at an early stage of fer-

tilisation would also provide us with more information

which we can not ignore the view of paternal mtDNA

inheritance in human. During the process of fertilisation

in mammals, up to 100 sperm mitochondria actually

enter an egg cell, together with the sperm head [17,29,

30]. However, these paternal mtDNAs are soon de-

stroyed by a selective elimination mechanism, including

ubiquitination of paternal mitochondria [30]. However,

the elimination mechanism in the fertilised egg cell is

not always highly stringent and fails to destroy all of the

inserted paternal mitochondria, causing paternal leakage

[30]. Such leakage was observed in mice progeny at a

frequency of around one in 10,000 [31]. An interesting

observation was that when “non-self” paternal mitochon-

dria—in terms of the population/subspecies/species, to

which the mating partner belongs—are inserted into the

egg cell, such as in the mating between cow and gaur,

these mitochondria are not eliminated and remain active

in the fertilised egg cell [30]. In the mating between two

inbred mouse strains, Mus musculus and M. spretus, a

similar escape of paternal mitochondria through the eli-

mination mechanism was observed as well [32]. These

leakages would lead to a heteroplasmic offspring and

thereby enhance the opportunity of transmission or re-

combination. It has been shown that human mitochon-

drial particles are fully equipped with the toolkits re-

quired for recombination [33-35]. Furthermore, each

mitochondrial organelle holds the mechanisms, leading

from heteroplasmy to the transmission of mtDNA [16,

28]. The detailed molecular mechanisms for paternal

mtDNA inheritance and replacement might differ from

one case to the other [36] and, at present, remain to be

examined in each case.

3. THE POSSIBLE FULL/NEAR-FULL

REPLACEMENT OF MTDNA

SEQUENCES IN THE HUMAN

PAST

It is highly likely that the anatomically modern humans

that originated in Africa were different from those who

inhabited in allopasy in the Asian continent for a long

evolutionary period [37]. Furthermore, different popula-

tions have differing variation in biological responses

[38]. Therefore, African migrants and indigenous inhab-

itants in Asia were likely to show different recognition

responses to the partner’s paternal mitochondria in their

“between-population” mating although they were sibling

and hybridisable. Thus, the ubiquitin-tagged paternal

mitochondria, which were inserted in the egg cell, would

not be subject to stringent mitochondrial elimination and

could survive in the fertilised egg cell, as seen in the

case of cow and gaur pairing [30]. There would be a

huge difference in recognition response between Palaeo-

lithic African migrant and inhabited Asians, who had

never exposed to Africans and thus much more paternal

(African) mtDNA molecules might had remained active

without any damages in Asian egg cells in their “betw-

een-population” mating. Since current human populati-

ons have already mixed each other in some degree, I bel-

ieve that much more African paternal mtDNA molecules

had survived in Palaeolithic Asian egg cells than those

we suspect in current “between-population” mating.

Most, if not all, of advocates for the “Out-of-Africa”

model based on mtDNA data often argue against the

alternative model of human origine on the following

basis: The alternative model has not based on the con-

clusive evidence showing the recombination/paternal

transmission of mtDNA in the human past. However, we

should realise that the “Out-of-Africa” model has been

standing on the shaky—recently much more shaky—

ground without any explicit and conclusive evidence,

showing that any recombination/paternal transmission of

mtDNA had not taken place in the human past. In fact,

Wilson [39] has mentioned that many puzzles have re-

mained between Y-chromosome and mtDNA data in the

conservative interpretation of the complex data in human

migration. In the present paper, I have already men-

tioned the new findings, which include the paternal

mtDNA behaviours in the fertilised eggs and the recom-

bination/paternal transmission of mtDNA in the wide

H. Naora / Natural Science 2 (2010) 571-575

573

range of animal kingdom. In fact, taking all of these new

findings into consideration, it is much more difficult to

prepare a reasonable explanation for the notion that a

series of the events, leading to the replacement of ma-

ternal mtDNA with the paternal DNA, had never taken

place in the human past. As already mentioned, the

transmission or recombination of mtDNA in the animal

kingdom has occurred more frequently and more widely

than we have previously suspected. Therefore, the lim-

ited human cases that have been currently reported so far

on the replacement of mtDNA should not be claimed

against the argument for the possible replacement events

in the human past.

Cann et al. [1] have shown that the mtDNA itself of

current humans in the Asian continent is really of Afri-

can origin. However, their claim that indigenous inhabi-

tants in Asia became completely extinct and were totally

replaced with African migrants is confusing. As will be

discussed in the next section, the present meta-analysis

shows that ironically, their result together with chromo-

somal DNA sequences can nicely account for the possi-

ble paternal mtDNA inheritance in the human past. Thus,

this novel view does not necessarily imply the extinction

of Asian indigenous inhabitants, followed by the total

replacement of the human population in Asia.

4. DISCUSSION AND CONCLUSION

The estimated ages of the most recent common ancestor

(MRCA) of Y-chromosomal DNA sequences, such as

several sites on SRY and YAP regions, were around 150

KY ago [40]. Current non-African men carry the M168

mutation, which arose in Africa during the period of 89

KY to 35 KY ago [41-43]. All of these sequences on

Y-chromosome were much younger than those (1,860

KY to 535 KY ago) of X-chromosomal DNA sequences,

e.g. gene coded for pyruvate dehydrogenase E1α [44]

and non-coding sequences Xq [45], and autosomal DNA

sequences, e.g. gene coded for β-globin [46] and non-co-

ding sequences on chromosome 22 [47]. It should be

noted that the MRCA ages of Y-chromosomal DNA

sequences roughly correspond to the time (200 KY-100

KY ago) of human migration to Asia and thus that the

Y-chromosomal and mtDNA sequences were likely to

arise in the ancestor who lived in Africa around < 200

KY ago [2]. On the other hand, the DNA sequences on

X-chromosome and autosomes could be traced back to

the era of H. erectus in Asia [10,48-50]. Therefore, these

results clearly suggest that the current Asians would be

the offspring of the hybrids resulting from the mating

between migrated Africans and indigenous Asian in-

habitants. However, it appears likely that African mi-

grants brought only African Y-chromosomal and mt D-

NA sequences to Asia [51] and most of Asian X-chro-

mosomal and autosomal DNA sequences remained in

the hybrid offspring. The most plausible scenario of the

event in Palaeolithic Asia would be as follows: In the

“between-population” mating, African Y-chromosomal

DNA entered an Asian egg cell, accompanying with his

mtDNA. The newly inserted paternal mtDNA remained

intact without any significant damage/elimination in the

fertilised egg cell and then formed heteroplasmy in the

hybrid. After a series of transmission or recombination

processes, the maternal mtDNA of Asian origin was

fully/near-fully replaced with the paternal (African)

mtDNA. Considering the possibility that the dilution-out

and/or selective sweep of African X-chromosomal and

autosomal DNA sequences might have occurred for

evolutionary advantage, the X-chromosomal and auto-

somal DNA sequences of Asian origin would tend to be

preserved more often and finally would be maintained as

a major component in the East Asian population [52].

Therefore, the male offspring, including a current Asian

male, would not necessarily be the direct descendant of a

replaced African, but would be the hybrid offspring

possessing the mitochondrial and Y-chromosomal DNA

sequences of African origin, together with Asian X-chr-

omosomal and autosomal DNA sequences. The seque-

nce data, if possible, of chromosomal DNA and mtDNA

of Palaeolithic Asian remains and the comparison with

those of current humans in different populations should

give a brighter view on this issue. The view raised in this

paper would open a new research field of biological in-

teractions, particularly in “between-population” repro-

duction in the human past.

5. ACKNOWLEDGEMENTS

I thank Prof. D. Clark-Walker (The Australian National University) and

Dr. A. Thorne (The Australian National University) for their critical

reading of the manuscript, and valuable suggestions and conversations.

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