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˜ring species™ (Cain, 1971). For Mayr (1942) such ˜circular overlaps™ perfectly
demonstrated the process of speciation. It is likely that the varying levels of
isolation, gene ¬‚ow and distance among human populations in the Pleistocene
generated geographical distribution patterns at particular times that were akin to
the ring species concept. For this reason it will be useful to explore this concept,
and its most recent developments in particular “ sympatric and parapatric speci-
ation “ a little further. In particular, I focus on the effects of gene ¬‚ow in prevent-
ing speciation. The Out-of-Africa vs Multiregional debate focuses on whether
there was isolation or gene ¬‚ow between Pleistocene human populations
(Hublin, 1998; Hawks & Wolpoff, 2001). Genetic exchange undoubtedly slows
down the rate of divergence of two populations (Irwin et al., 2001; Porter &
Johnson, 2002) but a more pertinent question is by how much? Recent specia-
tion models have highlighted the importance of local adaptation as a process that
Modern Human“Neanderthal problem 77

can oppose gene ¬‚ow leading to rapid population divergence to the level of full
species (Rice & Hostert, 1993; Johannesson, 2001). Even in cases of complete
sympatry, strong selection can eliminate gene ¬‚ow between populations lead-
ing to very rapid speciation (Gavrilets et al., 1998; Kondrashov & Kondrashov,
1999). Even though sympatric speciation is likely to be rare it appears a distinct
possibility in competitor-free, resource-diverse, environments (Dieckmann &
Doebeli, 1999; Filchak et al., 2000; Wilson et al., 2000) and minor changes
in the selective environment can cause population divergence (Danley et al.,
2000). According to Gavrilets et al. (1998), rapid speciation is also possible
without the need for extreme founder effects, complete geographical isolation
or selection for local adaptation. Short-term reductions in migration rate were
suf¬cient to produce signi¬cant and irreversible divergence and reproductive
isolation in just several hundred generations. Divergent selection pressures be-
tween populations can also lead to divergent sexually selected traits, if these
are favoured in different environments (Endler, 1992; Schluter & Price, 1993;
Schluter & Nagel, 1995; Irwin, 2000; Irwin et al., 2001; Johannesson, 2001).
Development, by providing a context for cryptic divergence in the allelic basis
of regulatory interactions and creating interspeci¬c incompatibilities, also in-
creases the probability of speciation even in cases of strong gene ¬‚ow (Porter &
Johnson, 2002). At the other end of the scale we have the classic allopatric spe-
ciation models in which geographically isolated populations can diverge due to
genetic drift even in the absence of strong divergent selective pressures but this
process will be severely curtailed in the presence of migration.
Irwin et al. (2001), in their review, concluded that the role of gene ¬‚ow in
preventing differentiation of the terminal forms of a ring species should be
highly dependent on whether initial substitutions were favoured everywhere or
only in parts of the species range. We can at least conclude that demonstration of
gene ¬‚ow in the case of sympatric or parapatric Pleistocene human populations
does not automatically preclude lineage divergence, or indeed even speciation.
Given the differences in spatial ecology between Neanderthals and Moderns,
that will become apparent in this book, we should not be surprised to observe
lineage separation in the presence of varying degrees of gene ¬‚ow as detected
by Templeton (2002).


Sympatry or allopatry?

The situation that arose in Europe and western Asia that concluded with the
extinction of the Neanderthals and the colonisation of the Moderns was not
exceptional, as we saw in the previous chapter. The pattern of extinction of
Neanderthals does not follow an east to west gradient as would be expected
78 Neanderthals and Modern Humans

if the Moderns arriving from the Middle East had replaced them. Instead,
Neanderthals became extinct across the mid-latitude belt from Portugal to
the Caucasus at about the same time (31“29 kyr) (Finlayson, 1999; Finlayson
et al., 2000a; Ovchinnikov et al., 2000; Zilhao, 1996; Smith et al., 1999; Chap-
ter 7). Populations that had occupied areas to the north, around the North
Eurasian Plain, became extinct earlier (by 40 kyr). This, together with the
long-established contemporaneity of Neanderthals and Modern Humans in the
Middle East for thousands of years (Bar-Yosef, 1998) questions the long-held
view that Moderns caused the Neanderthal extinction. The dating of a Javan
specimen, attributed to H. erectus, at 25 kyr (Swisher et al., 1996) indicates a
late persistence of archaic humans also in tropical South-east Asia. Since we
now know that Moderns had reached well into Australia by 50 kyr (Thorne et al.,
1999; Bowler et al., 2003), protracted geographical overlap between Moderns
and archaics must have been widespread. Questions that relate to reproductive,
ecological and behavioural interactions in areas of geographic overlap (sympa-
try) therefore assume a greater relevance. Because the European“Middle East-
ern region is the best documented, it is issues of Modern Human“Neanderthal
interactions that are receiving prominence. Sympatry would have been possible
if Neanderthals and Moderns had suf¬ciently different niches to permit ecologi-
cal isolation (Lack, 1971; Cody, 1974) or if numbers were such that populations
were below carrying capacity. Competition would only occur in situations in
which the populations were at carrying capacity and resources became limit-
ing. Differences in ecology may explain the long periods of sympatry (Mellars,
1996). Recent work suggests that Moderns and Neanderthals were ecologically
separated and had distinct habitat preferences (Finlayson, 1999; Finlayson &
Giles Pacheco, 2000). Improved resolution of climatic data is allowing greater
precision in linking ecological change with human behaviour (van Andel &
Tzedakis, 1998). The rapid changes during the late Pleistocene (Allen et al.,
1999) especially in zones of sharp ecological transition (Peteet, 2000) have clear
implications for the survival of populations, including hominids. The impor-
tance of temperate and tropical refugia is also being re-assessed and isolation in
cold-stage refugia (e.g. Iberia, southern Italy, Balkans) is re¬‚ected in distinctive
present-day patterns of genetic variation and subdivision among widely differ-
ent animals (Willis & Whittaker, 2000). The evidence increasingly points to the
Modern expansion and the Neanderthal extinction being the products of habitat
and resource change during the late Pleistocene, with southern refugia playing
a critical role in the outcome (Finlayson, 1999; Finlayson & Giles Pacheco,
2000). The degree of interaction between Moderns and Neanderthals would
have been minimised by ecological separation. Contact would be predicted to
be greatest where heterogeneous landscapes were close to the plains and would
therefore have been localised. So far the only case of apparent hybridisation, as
Modern Human“Neanderthal problem 79

we have seen, is the Lagar Velho child (Duarte et al., 1999; Zilhao & Trinkaus,
2002). The key is not whether hybridisation occurred but its effect on the hu-
man gene pool. Given the available genetic evidence (Krings et al., 1997, 1999,
2000; Ovchinnikov et al., 2000; Caramelli et al., 2003) it would seem that
such hybridisation must, at best, have been restricted to localised hybrid zones
(Hewitt, 1989). In the same way, the conditions required for competition
(Finlayson et al., 2000b) would not appear to hold given the low population
densities (Mussi & Roebroeks, 1996; Harpending et al., 1993) resulting from
the constantly and rapidly changing climate (GRIP, 1993; Allen et al., 1999).
Competition, like hybridisation, may have been a very local phenomenon with
no consequence to the Neanderthal extinction. It would be very informative to
have ecological data from South-east Asia where late H. erectus and H. sapiens
must have been sympatric for at least 25 kyr.


Genes

Studies of mitochondrial (mtDNA) and fossil (fDNA) Neanderthal DNA
(Krings et al., 1997, 1999, 2000; Ovchinnikov et al., 2000; Scholz et al., 2000)
indicate their genetic distinctness when compared to present-day humans. We
lack, however, a comparison with Modern Humans that were contemporary with
the Neanderthals (Wolpoff, 1998) although a recent comparison with 24 kyr-old
Modern Humans indicates a genetic discontinuity (Caramelli et al., 2003). In
any case these observations do not exclude the Multiregional model (Nordborg,
1998; Reletheford, 1999). The time of the last common ancestor of Modern
Humans and Neanderthals is now put within the time frame of 317“741 kyr,
possibly around 465 kyr (Krings et al., 1997, 1999; Ovchinnikov et al., 2000).
From the limited data available the provisional conclusion that may be drawn
about Neanderthal genetic diversity is that it was low, comparable to Mod-
erns, and much lower than for the great apes. Since Neanderthals had a larger
geographical range than the apes, it appears that the Neanderthals may have
expanded from a small population (Krings et al., 2000). If so, it would seem
that Neanderthals were similar to Moderns in demographic expansion charac-
teristics, low mtDNA and nuclear diversity in Moderns being equated to a rapid
population expansion from a small population (Jorde et al., 1998).
Many genetic studies in the 1980s and 1990s seemingly clari¬ed the ques-
tion of a single African origin (between 100 and 200 kyr) and the timing of
genetic differentiation of human populations around 100 kyr (Cann et al., 1987;
Vigilant et al., 1991). However, not all molecular clocks tick at the same rate
(Strauss, 1999) and there may even be variations in rate through time within
the same lineage. A number of studies now propose faster mutation rates than
80 Neanderthals and Modern Humans

conventionally accepted (Siguroardottir et al., 2000). Effects include a more
recent placing of the time of mitochondrial ˜Eve™ and of major Pleistocene
human population expansions (Excof¬er & Schneider, 1999). A study of the
haplotypes of the PDHA1 gene (that apparently has a steady mutation rate) on
the X chromosome threw the dating of Modern Human origins and the issue
of a single African origin wide open. Ingman et al. (2000), however, tested
and con¬rmed that human mtDNA lineages evolved at constant rates. Only the
D-loop did not evolve at a constant rate and was therefore unsuitable for dating
evolutionary events.
Harris & Hey (1999) found a ¬xed DNA sequence difference between African
and non-African samples and the age of onset of population subdivision was
around 200 kyr. This evidence supported earlier studies (Harding et al., 1997;
Hammer et al., 1998) that pointed to Asian ancestry older than 200 kyr that was
hard to reconcile with a unidirectional Out-of-Africa migration 100 kyr and the
total replacement of archaic populations in Asia. This message was reinforced
in another recent study (Reletheford & Jorde, 1999) that, while supporting a
major role for Africa in Modern Human origins, left the question of complete
African replacement open. In other words, it was not clear whether the gene
pool of Moderns was completely African or predominantly so (Jorde et al.,
2000). Recent high resolution studies using the Y-chromosome and of complete
mtDNA sequences appear to have strengthened the Out-of-Africa perspective
further (Ingman et al., 2000; Underhill et al., 2000; Richards & Macaulay, 2001)
but the question of complete replacement of all archaic human populations by
Moderns is still in doubt (Templeton, 2002).
The evidence is also pointing toward multiple dispersals from Africa. A study
of a 565-bp chromosome 21 region near the MXI gene, which is unaffected by
recombination and recurrent mutation, and con¬rmed by independent evidence
from a Y-chromosome phylogeny, suggests a series of distinctive range expan-
sions: a ¬rst one to Oceania via South Asia; a second one to east Asia and
subsequently north-east Asia and America; and a third mainly to Europe via
west and central Asia (Jin et al., 1999). This observation is consistent with
the view that aboriginal Australians and some Asians, in addition to Africans,
carry ancient DNA sequences (Harding et al., 1997; Stoneking et al., 1997;
Kaessmann et al., 1999). A population bottleneck appears to coincide with a
Eurasian colonisation from Africa, estimated to have occurred at 38.5 kyr and
no earlier than 79.5 kyr (Ingman et al., 2000). These observations point to an
early dispersal of Moderns into Asia via the Horn of Africa (Lahr & Foley, 1994;
Foley, 1998; Quintana-Murci et al., 1999; Kaessmann et al., 1999) around 120“
100 kyr, and a subsequent dispersal that included Europe between 60 and 40
kyr (Lahr & Foley, 1994; Underhill et al., 2000). Both dispersals originated in
eastern Africa (Quintana-Murci et al., 1999).
Modern Human“Neanderthal problem 81

The greater genetic diversity of African populations (Kaessmann et al., 1999)
has also been used as evidence of its greater age and, therefore, its function as
source (Tishkoff et al., 1996; Jorde et al., 1997; Harpending & Rogers, 2000).
Genetic diversity is not just a function of time (and distance from source) but also
of effective population size (Ingman et al., 2000) and the African population
size was indeed larger than in other parts of the world during recent human
evolution (Reletheford & Jorde, 1999).
The assumption that mtDNA is inherited by the maternal line alone has been
challenged as it appeared that mtDNA from the mother™s egg could recombine
with sperm-contributed DNA (Awadalla et al., 1999; Eyre-Walker et al., 1999;
Hagelberg et al., 1999). This potentially set the clock out and even questioned
the very existence of a mitochondrial ˜Eve™. Estimates of relatedness could be
affected because recombination would create a more genetically homogeneous
population through time than would otherwise be predicted so that differences
between more diverse ancient sequences and more homogeneous recent ones
would be exaggerated (Strauss, 1999). The mtDNA recombination idea has
been strongly challenged by Ingman et al. (2000) and Elson et al. (2001).
A recent study of 62 human population samples con¬rmed that the demog-
raphy of populations strongly affected genetic af¬nities, those not undergoing
demographic expansion showing increased genetic distances from other popu-
lations. Otherwise, genetic af¬nities closely matched geography (Excof¬er &
Schneider, 1999). The genetic study of population expansions (Excof¬er &
Schneider, 1999) may go some way towards focusing genetic research on re-
cent human evolution away from the ˜Out-of-Africa/Multiregional™ debate with
questions that will require multidisciplinary collaboration.
In a revision of the genetic evidence, Harpending & Rogers (2000) concluded
that the evidence in support of the Out-of-Africa model was far less clear than
it had been ¬ve years earlier. The issue of absence of evidence of a population
expansion in a number of gene loci was a particular problem and this issue has
been used by Hawks et al. (2000) to refute the Out-of-Africa model. For now,
balancing the available evidence, we can conclude that Africa, probably East
Africa, was the source area of Moderns. There were probably three major Out-
of-Africa expansions: one around 1.9 Myr; another one around 840“420 kyr,
that coincides with predictions of a demographic explosion around 500 kyr
(Aguirre, 2000) shortly after the emergence of the early archaic Modern form
in Africa (Brauer et al., 1997); and a third around 150“80 kyr (Templeton, 2002).
This third expansion may have involved an early phase, around 120“100 kyr,
to Oceania via the Horn of Africa and South Asia and a second phase, around
60“40 kyr, to East Asia (and eventually North America) and also into West
and Central Asia and from there into Europe. It is also likely that intermediate
periods saw varying degrees of isolation by distance. The degree to which these
82 Neanderthals and Modern Humans

dispersals involved complete replacement or, instead, some degree of inter-
breeding remains unresolved. The divergence of the Neanderthal and Modern
Human lineages around 465 kyr would be consistent with the second expansion
described above. We should not discard, either, the possibility that population
expansions were not always in the same direction and that ˜reversals™ would
have taken place probably in response to sudden, opposing, climatic trends that
were typical of the Pleistocene (Chapter 6).


Ecomorphology

There are many excellent texts that describe the morphological characteristics
of Neanderthals and Moderns (see, for example, Klein, 1999). For this reason I
will limit myself to highlighting and contrasting the major features of the two
forms and to discussing their functional signi¬cance. The particular features of
the Neanderthal morphology have been attributed to the gradual accretion of
characters during long periods of isolation in Europe and western Asia (Hublin,
1998). Some of the features that characterised the Neanderthals were present
in pre-Neanderthals (Arsuaga et al., 1997; Lebel et al., 2001) indicating that
they had been evolving independently in their geographical area for a long time.
Genetic drift is often considered a major factor in the evolution of the Nean-
derthals™ particular morphology even though there is no speci¬c evidence to
corroborate this assertion. On the other hand, a number of features are consid-
ered adaptive and are thought to re¬‚ect the particular environments exploited
by the Neanderthals. I will now summarise these features.
The Neanderthals were very robust, barrel-chested and exhibited muscular
hypertrophy. The hand™s morphology permitted a very powerful grip. Together
with strong and cortically thick leg bones these features suggest the ability
for endurance in use. The shafts of the phalanges of the foot may have been
adapted for prolonged movement over irregular terrain (Klein, 1999). The low
angle between the neck of the femur and the shaft is a characteristic of highly
active individuals (Trinkaus, 1993). A number of morphological features are
dif¬cult to interpret and this has led some authors to suggest that such features
had no functional signi¬cance (Klein, 1999). Some of these features may re¬‚ect
the highly mobile lifestyle of the Neanderthals (Chapter 5). These relationships
are, however, tentative. The longer and thinner pubis of Neanderthals when
compared to Moderns (Rosenberg, 1988; Dean et al.,1986) may re¬‚ect a longer
gestation period (Trinkaus, 1984) but this is disputed (Anderson, 1989; Rak,
1990; Stringer & Gamble, 1993). The precocity of Neanderthal children (Dean
et al., 1986; Trinkaus, 1986), along with a long gestation period, could reduce

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