Biological Journal of the Linnean Sociely (1990), 41: 13-25. With 2 figures
The house mouse progression in Eurasia: a
palaeontological and archaeozoological
approach
JEAN-CHRISTOPHE AUFFRAY, FLAVIE VANLERBERGHE AND
JANICE BRITTON-DAVIDIAN
Institut des Sciences de I‘Evolution, Universiti ScientiJique el Technique du Languedoc,
Place Eug2ne Bataillon, 34095 Montpellier Cedex 05, France
A palaeontological and archaeozoological survey has allowed us to establish the different steps in the
colonization of western Eurasia and northern Africa by the house mouse Mus rnusculus. After
successive immigration waves of the genus Mus into this zone from the late Pliocene to the upper
Pleistocene, the house mouse appeared and remained confined to the easternmost Mediterranean
Basin at the uppermost Pleistocene. The first progression of this species into the Mediterranean Basin
occurred in the Middle East from the Epipaleolithic to the Neolithic. Subsequently, this species was
found in the western Mediterranean Basin during the Bronze Age and in north-west Europe during
the Iron Age. I n comparison to this latter zone, north central Europe was colonized relatively early,
from the Neolithic to the Bronze Age which may, in fact, not only correspond to a much earlier
invasion of Europe by M. musculus musculus but also suggest that the distribution of this subspecies
extended much further west than it does nowadays, at a time when M . musculus domesticus was
restricted to the Mediterranean zone. This archaeological survey is in agreement with genetic data
which provide indications as to the speed, steps and pathways of progression of house mouse
populations in western Eurasia.
KEY WORDS:-Mus
invasions.
- Mus
musculus - palaeontology
-
archaeozoology - Pleistocene
-
Holocene
-
CONTENTS
Introduction . . . . .
From the origin of murids to the
Middle and upper Pleistocene in
Middle and upper Pleistocene in
Holocene . . . . . .
Acknowledgements
. . .
. . . . .
References
.
.
.
.
.
.
.
.
.
.
.
. . . . . . . . . . . . .
. . . . . . . . . . . .
. . . . . . . . . . . . .
lower Pleistocene . . .
Europe and northern Africa
the Middle East . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
13
. . 15
. . 17
. . 18
.
19
. . 22
.
23
INTRODUCTION
The study of the evolution of an animal group may be undertaken following
two complementary approaches: a ‘vertical approach’ used in palaeontology and
corresponding to the historical study of a group and a ‘horizontal approach’
followed by numerous fields of biology that compare subdivisions of a group in
order to reconstitute a phylogeny.
The genus Mus and especially the house mouse M . musculus has become a
successful model for the study of biological evolution. Geneticists and molecular
0024-4066/90/090013
+ 13 $03.00/0
13
0 1990 The Linnean
Society of London
J.-C. AUFFRAY E’T AL.
14
Mus musculus complex:
musculus musculus
Mus musculus domesticus
MUS
mj
spretus
Mus spicilegus
Mm macedonicus
Figure 1 . Distribution of extant species of Mus in West Eurasia and North Africa (modified from
Orsini, 1982 and Auffray el al., 1990).
biologists have recorded a succession of complete or incomplete speciation events
in this genus (Thaler, Bonhomme & Britton-Davidian, 1981; Bonhomme, 1986;
Bonhomme et al., 1984). Likewise, the systematic status of species and subspecies
present in West Eurasia and North Africa is now clearly established. If numerous
‘horizontal’ views of the evolution of this group are available, a ‘vertical’
approach, however, is much more difficult to establish, not only because the
mouse group is relatively recent and as such is poorly represented in
palaeontological remains, but also because several species of mice cannot always
be discriminated on a morphological basis in the fossil or subfossil material.
Brothwell attempted, in 1981, a history of the house mouse by successfully
introducing the use of archaeozoological data but, at that time, the systematics
of all the recent species of mice had not been determined.
The current systematic status considers that four species of mice occur in
western Eurasia and northern Africa (Fig. 1). Three are wild-ranged and live
independently of man, M . spretus, M . spicilegus and M . macedonicus, the latter
being often referred to as M . abbotti or M . spretoides (Britton & Thaler, 1978;
Bonhomme et al., 1983; Orsini et al., 1982, 1983). T h e fourth species is
commensal and subdivided into two subspecies, the long-tailed house mouse,
M . musculus domesticus, occupying the circum-Mediterranean area and western
Europe and the short-tailed house mouse, M . musculus rnusculus, present in
northern and continental Eurasia (for a review see Bonhomme, 1986).
HOUSE MOUSE PROGRESSION IN EURASIA
15
The biochemical study of several populations of M . m. domesticus of West
Eurasia and North Africa provides constructive information on the
differentiation patterns of this subspecies (Britton-Davidian, 1990). Indeed, this
study shows that populations from southern Europe (including France, Spain,
Italy and Greece) form a group very close in terms of the mean genetic distances
of Nei (0.04) and in which geographic distance is not correlated with genetic
distance. This indicates that house mice spread very rapidly all over the western
Mediterranean Basin and could account for the independence between
geographic and genetic distances. As one moves outward from this region
whether northward (Great Britain and Germany) or southward (Tunisia and
Algeria), mean genetic distances increase to 0.07-0.10. Finally, a welldifferentiated group is present in the Middle East (Egypt and Israel) showing
mean genetic distances between 0.10-0.15 to all of the latter. This could indicate
that the house mouse progressed slowly within the eastern Mediterranean Basin,
leading to the observed level of divergence.
The two genetically differentiated subspecies M . m. domesticus and
M . m. musculus are presently parapatric and interact along a narrow hybrid zone
extending across Europe from Denmark to Bulgaria (Yonekawa et al., 1982;
Ferris et al., 1983a, b; Boursot et al., 1984; Vanlerberghe et al., 1988a, b). The
secondary nature of this contact indicates that the house mouse probably
colonized Europe via two different pathways. However, the introgression
patterns of mtDNA variants and the fragmented position of the extant hybrid
zone in Denmark and northern Germany suggest that the initial hybridization
event between these two branches of M . musculus took place elsewhere on the
European mainland, a t a time when house mouse populations had not yet
reached the Jutland or Scandinavian Peninsulas. The advance of M . m. domesticus
from the south then probably induced an eastward retreat of M . m. musculus until
an equilibrium was established before M . m. domesticus populations reached the
Baltic Sea. From there, M . m. musculus mice with a nuclear-mitochondria1 hybrid
genome would have invaded the Scandinavian Peninsula (Gyllensten & Wilson,
1987).
The historical establishment of the extant distribution of these two subspecies
is one of the main problems that the present work will focus on. This work
reviews the available palaeontological and archaeological data, complemented
with the present day biological knowledge of the extant species of Mus, in order
to date and describe the colonization steps of mice in western Eurasia.
FROM T H E ORIGIN OF MURIDS TO T H E LOWER PLEISTOCENE
According to Jacobs (1982), Antemus is the oldest and most primitive murid
and is dated middle Miocene, 10 Myr. Fossils of Antemus have been found both in
the Potwar Plateau in Pakistan (Jacobs, 1982) and in the Li fossil locality in
Thailand (Jaeger et al., 1985). These findings suggest that south-east Asia is the
original area of distribution of murids.
Progonomys extinct species are the first representatives of the subfamily
Murinae Uaeger et al., 1985), to which belong, among others, the genera Mus
and Rattus. Progonomys appeared in the Early Valesian, again in the Potwar
Plateau Uacobs, 1982) and slightly later in western and southern Europe and
northern Africa (for a review see Jaeger et al., 1986). This genus is present during
16
J.-C. AUFFRAY E T AL.
the Valesian and the Turolian, that is, in the upper Miocene, in most of these
places (for a review see Cheylan, Michaux & Croset, in press), but the most
recent fossils have been found in Ammana, Algeria, between 9 and 8 M y r
Uaeger, 1977). Morphological comparisons suggested that the Mus morphotype
is closely related to, and derived from, an ancestral morphotype of Progonomys
(Jaeger et al., 1986). This explains why palaeontologists did not create an extinct
intermediate genus between Progonomys and Mus as they did for the lineage
leading to Apodemus (Thaler, 1986).
The first so-called Mus ( M .auctor) also comes from the Potwar Plateau in
Pakistan (Jacobs, 1982). This oldest Mus fossil is dated 7 Myr (Flynn & Jacobs,
1982) in the Turolian equivalent of Asia, late Miocene. According to
palaeontological data, the divergence between the Mus and Rattus lineages
occurred 12 to 8 Myr ago (Jacobs & Pilbeam, 1980; Jaeger et al., 1986).
Mus remained poorly represented in the Pliocene, 5 to 2 Myr. The genus was
noted in the Early Pliocene in the Kabul Basin in Afghanistan (Brunet et al.,
1980). Vereshchagin (1967) reported the occurrence of Mus represented by one
bone, in the Kosyakin Quarry locality in North Caucasus, U.S.S.R., dated lower
Pliocene on the basis of geological data and the composition of the fossil
complex. In East Africa Mus fossils found in the Hadar Formation, Ethiopia, are
dated 3 Myr and seem to be closely related to the recent Indian pigmy mouse
M . booduga formerly included in the subgenus Leggada (Sabatier, 1982). The
African and Indian pigmy mice are now considered as two different taxa on the
basis of biochemical genetics studies: the Indian pigmy mouse being now referred
to as M . booduga and the African pigmy mouse to the subgenus Nannomys which is
sufficiently different genetically to justify a genus rank (Bonhomme et al., 1984,
Bonhomme, 1986). O n the basis of the knowledge of these extant groups and
their distribution, the East African fossils of mice are probably more related to
the African Nannomys groups than to the Indian Leggada. Jaeger & Wesselman
(1976) also described a Mus (Leggada) in the Shungura Formation, Lake Rudolf
Basin, Ethiopia, dated the same.
Mus species from the upper Pliocene have been found around the Lake
Ichkeul, Tunisia (Jaeger, 1971), and M . haouzi in Jebel Melah, Tunisia, Jebel
Irhoud and Sidi Abdalah, Morocco Uaeger, 1975a).
At the end of the Pliocene, the genus Mus seems to have been well established
in two regions: south-east Asia and North Africa; the Nannomys group being more
representative of East Africa.
The lower Pleistocene distribution of the genus Mus is very similar to that of
the upper Pliocene: south Asia and East and North Africa. I n East Africa, Jaeger
(1977) describes in the rodent fauna of Olduvai, Tanzany, a mouse called
M . petteri, which is morphologically very isolated from all other recent African
species of mice. I n North Africa, fossils of Mus are found in Jebel Ihroud, Atlas,
Morocco Uaeger, 1970). This author considers these fossils as belonging to
M . haouzi Uaeger, 1975a), the same palaeontological mouse species as the one
occurring during the upper Pliocene from Jebel Melah, Morocco, thus possibly
indicating a continuous lineage of Mus in this region from the Pliocene to the
lower Pleistocene. However, as for the East African mice, the northern species
are very isolated from all the recent species Uaeger, 1975a).
In Pakistan, Jacobs (1982) continues to follow the Mus lineage in the Potwar
Plateau by describing Mus sp. fossils from Pabbi Hills dated Early Pleistocene.
HOUSE MOUSE PROGRESSION IN EURASIA
17
MIDDLE AND UPPER PLEISTOCENE IN EUROPE AND NORTHERN AFRICA
From the middle Pleistocene, fossils referred to as Mus become more common
around the Mediterranean Basin and in West Eurasia. This study will focus on
these areas.
First, in Morocco Mus remains are present in the middle Pleistocene at Sidi
Abdallah, Aim Mefta, Salk, Irhoud and in the upper Pleistocene a t Irhoud
Neandertal Uaeger, 197513). Jaeger (1975a) suggests that they represent
vicariant species of Mus, those of the uppermost levels being M . musculus. At the
time that Jaeger undertook these studies, the taxonomic status of the two
sympatric species of mice of the western Mediterranean Basin had not been
determined. I n fact, Jaeger considered that four extant species of Mus, including
M . musculus domesticus and M . musculus spretus, occurred in the Maghreb and did
not attempt to discriminate them in the fossil material.
Once the specific status of these sympatric mice M . musculus domesticus and
M . spretus was clearly established in southern France following the biochemical
survey by Britton & Thaler (1978), Darviche & Orsini (1982) developed
discriminative morphological parameters between these two species using
biochemically screened animals. Subsequently Orsini ( 1982) described these two
mice in northern Africa. Based on these works, Thaler (1986) considers that the
oldest fossils exhibiting M. spretus attributes in northern Africa occur in the
middle Pleistocene, suggesting that the divergence between M. spretus and
M . musculus lineages occurred at least 1 Myr ago and a t most 3 Myr ago-this
interval corresponds to the fact that the mammalian fauna of this region is
characterized by a high rate of extinction and reappearance by migration, and it
is not possible to determine which immigration wave corresponds to the first
specific ancestor of M. spretus (Thaler, 1986).
O n the other side of the Mediterranean Sea, in southern France, Chaline
(1971) found several fossils of Mus at Le Vallonet in two different layers a t the
transition lower/middle Pleistocene which is characterized as a semi-arid steppe
environment. Mus does not reappear in this region until the Holocene.
Eastwards, the presence of Mus is intermittent and often seems to be related to
climatic changes, this suggests that several immigration waves of Mus may have
occurred in Central Europe. I n Hungary (for a review see Janossy, 1986), the
genus Mus is evident from the middle Pleistocene onward. The oldest fossil of
Mus found there, M . musculus synanthropus, comes from Tarko and is dated
Biharian, c.-500 000; it corresponds to the first immigration wave of true mice
into the Carpathian Basin. Later, Mus (Budamys) synanthropus is noted in marly
layers of Vkrtesszolos, corresponding to the upper Biharian, Mindel. This is one
of only two cases showing the presence of Mus during glacial periods, the second,
during Riss, corresponding to Mus (Budamys) solymarensis recorded in the
Ordoglyuk cave of Solymar. At the interglacial period Mindel-Riss, Mus
remained in this region as M . m. synanthropus from the lower layers of Vdrhegyy in
Buda. The latest Pleistocene occurrence of Mus in this region dates from the
Riss-Wurm interglacial period which is characterized by a Mediterranean
climate: Mussp. from locality 6 and 9 of Siitto. Mus is no longer present in this
region during the Wurm.
Thaler (1986) considers that Pleistocene mice of the Pannonic basin do not
represent direct ancestors of the post-glacial fauna. We consider that the four
18
J.-C. AUFFRAY E l AL.
recent species of western Eurasia differentiated elsewhere than in Central
Europe.
Moving south from Hungary, Mus appears in Greece some time between the
middle and the late Pleistocene (Van de Weerd, 1973): the mouse fossils from
this period, Mussp., found in Varkiza, near Athens, are closely related to the
Hungarian fossils described by Janossy (1986). Mussp. is also noted at Chios
Island at the middle Pleistocene (Storch, 1975). According to Mayhew (1977)
the presence of Mus in Greece also explains its presence in Crete: the reduction of
sea barriers during periods of major land ice development in the middle and
upper Pleistocene allowed immigration of Mus to the island. Two types of Mus
were noted by Mayhew (1977), (1) M. batae from Stravos, Akrotiri Peninsula
from the middle and late Pleistocene, and (2) M . minotaurus in a “cave deposit
between Canea and Suda” locality and ten other localities of the northern
Cretean Coast, dated from Riss to the Holocene age.
At the end of the Pleistocene, Mus is no longer present in mainland Europe,
but may possibly occur as M. minotaurus in Crete and as M . spretus (or a close
ancestor) in northern Africa (see above).
MIDDLE AND UPPER PLEISTOCENE IN T H E MIDDLE EAST
In Cyprus, two morphotypes of Mus were noted by Boekschoten & Soondar
(1972), during the middle Pleistocene. Both forms were found in Cape Pyla,
South Cyprus and the largest one only at Kythraea, in an interglacial deposit of
Villafranchian.
Eastward, Vereshchagin (1967) notes the presence of the genus Mus in the
Caucasus in the middle and upper Pleistocene. For the latter period, Mus fossils
were recorded in the Binagady locality. Binagady mammals lived, according to
the author, in a dry steppe suggesting a climate somewhat cooler and more
humid than the present one. Vereshchagin correlates this period with the
Mousterian culture.
In the eastern Mediterranean Basin, the situation is much more precise and
instructive. Israel harbours many Pleistocene and Holocene localities rich in
mouse fossils, as do northern Africa and Hungary, allowing mouse lineages to be
followed through time. Two other advantages characterize this region: (1) a
parallel between the evolution of the mouse lineages and the cultural evolution
of man can be established and (2) the zone represents the first circumMediterranean step on the European colonization route of mice from their
original south Asian area of distribution.
The genus Mus is attributed to a fossil of Ubeidyia dated middle Pleistocene
(Tchernov, 1986). Later, the genus Mus becomes very frequent from the
Acheulean level until the Historical Age (Tchernov, 1984). A study on fossil
material in Israel allowed identification of the two recent species of mice present
in this region. The method was the same as that applied to the North African
M . spretus and M. musculus. It consisted of (1) establishing biochemically the
presence of two sympatric extant species, M. macedonicus and M. musculus
domesticus, in Israel, ( 2 ) the re-evaluation of discriminative morphological
parameters (Auffray et al., 1990) which had been determined for other regions,
Greece and Bulgaria (Orsini et al., 1983) and finally, (3) the discrimination of
fossil material based on the analogy with the recent material.
HOUSE MOUSE PROGRESSION I N EURASIA
19
The archaeological survey of Israeli material revealed that M . macedonicus
occurred from the Acheulean culture level until present in several localities,
Oum Qatafa, Qafzeh, Tabun and Hayonim. Mus musculus first appeared in the
Hayonim fossil locality (level B), that is during the Natufian culture (Auffray et
al., 1988). The Mus fossil of the middle Pleistocene Locality of Ubeidyia, which is
represented by a single tooth, could not be referred to either species. The house
mouse M . musculus appears in the Levant during the post-glacial period, that is
not before the uppermost Pleistocene.
According to the many biological reports on the distribution and ecology of
mice of the genus Mus, M . musculus (including all its subspecies, domesticus,
musculus, castaneus and bactrianus-for a review see Bonhomme, 1986) is the only
one to establish permanent commensal populations. I n Israel, the present
distribution and ecology of M . musculus domesticus and M . macedonicus is very clear:
M . m. domesticus is essentially commensal and M . macedonicus is mostly found in
environments unexploited by man. Syntopic zones are agricultural fields. That
competition exists between the two species in zones of sympatry is detected by
the fact that the house mouse, outside the sympatric area, that is, the
Mediterranean zone, shows a larger ecological range extending into unexploited
environment (Auffray ef al., 1990). Competition between these two mouse
species may well be at the origin of the commensalism of the house mouse.
Indeed, the first M . musculus in Israel is dated Natufian (Auffray el al., 1988)
which corresponds to the beginning of human seden tism, long-term occupational
sites, and to the earliest human dwellings (Valla, 1988). These earliest dwellings
in the Fertile Crescent could have provided a new ecological niche allowing the
house mouse to progress into this zone and thereby avoid competition with the
resident M . macedonicus.
Another discrimination of fossils based on recent species was performed by
Storch (1988) who described the arrival of M . macedonicus at the uppermost
Pleistocene of south-west Anatoly, Antalya locality.
I n conclusion, at the end of the Pleistocene, that is Wurm and the beginning of
by two
the post-glacial period, Mus is present in the Middle East-represented
species in Israel, the house mouse M . musculus, and a short-tailed wild-living
mouse M . macedonicus (Auffray et al., 1988), and represented only by the latter in
Anatoly (Storch, 1988).
HOLOCENE
At the uppermost Pleistocene, the occurrence of the house mouse is recorded
only in the eastern Mediterranean Basin, where it has just arrived. The few other
places of the circum-Mediterranean area where Mus was then present seem to be
occupied by other species of Mus, such as M . spretus (or a close ancestor) or
M . macedonicus (or a close ancestor). Therefore, the presence of the house mouse
in human occupational sites in the Israeli Natufian constitutes the first phase of
house mouse progression into Eurasia from the original eastern area of
distribution and the first record of its association with man.
From this date on, Mus reappears around the Mediterranean Sea. I t occurs
either in archaeological sites, where, according to the ecology of the extant
species, the specific status can certainly be considered as M . musculus or in
palaeontological sites where the specific denomination remains problematic.
J.-C. AUFFRAY E’T AL.
20
TABLE
1. Archaeological sites presenting Mus musculus from the Epipaleolithic in West Eurasia and
North Africa
Location
Hayonim, Israel
Time, period
Epipaleolithic
C.
Kirokitia,
Andreas-Kastro Cap,
Cyprus
Catal Huyiik, Turkey
10000 BC
Pre-pottery Neolithic
9000-8000 BC
Species
M . musculus appears
while M . macedonicus has
been present since the
Middle Pleistocene in the
Levant
Mus mllsculus
Reference
Auffray et al. (1988)
Le Brun et al. (1987) in
Vigne 1988a
Mus musculus
Brothwell (1981)
Mus musculus
Cordy & Stassart (1982)
Bronze Age 1750 BC
Twelfth Egyptian
Dynasty, c. 1700 BC
Bronze Age
1500-1300 BC
Bronze Age 1490 BC
Mus musculus
Mus musculus
Alcade-Gurt (1986)
Petrie (1891), Dixon (1972)
in Brothwell (1981)
Kordos (1978)
Bronze Age
1200-700 BC
Middle Bronze Age
Mus musculus
Vigne & Alcover (1985)
Vigne (1988a)
Brothwell (1981)
Mus musculus
Cristaldi & Federici (1980)
Bronze Age 700 BC
Discrimination between
Mus musculus and Mus
spretus has not been
possible
Mus musculus
Vigne & Alcover (1985)
Vereshchagin (1967)
Mus musculus
Brothwell (1981)
Kotsakis & Ruschioni
( 1984)
Vigne & Marinval-Vigne
(in press)
Reurner & Sanders (1984)
Vigne & Alcover (1 985)
Neolithic 6500-5650
BC
Place St-Lambert, Liege,
Belgium
La Garrotxa, Spain
Kahun and Buhen,
Egy Pt
Nagyoldal Shaft,
Hungary
Su Guanu Cave,
Sardinia, Italy
Bovenkarspel, Holland
Grotta Romagnano,
Trento, Italy
Es Pouas, Ibiza, Spain
Neolithic 4500-4300
BC
Mus musculus
Mus musculus
Pyatigor’e, Caucasus,
U .S.S.R .
Urartu Fortress, Kamir
Blur, Caucasus U.S.S.R.
Tortoreto, Teramo, Italy
Late Bronze Age
mid-1st millenium BC
Late Bronze Age
Iron Age
Mus musculus
Monte di Tuda, Corsica,
France
Bini Calaf, Menorca,
Spain
400
Mus musculus
S’illot, Majorca, Spain
400-150
Gussage All Saints,
England
Tornror, Island of
Oland, Sweden
Les Illettes, Alps, France
Pre-Roman Iron Age
Mus musculus appears
while Mus spretus appears
at Rafal Rubi site,
1500-1400 BC
Mus spretus and Mus
musculus appear together
Mlls musculus
Late Iron Age
Mus musculus
Lepiskaar (1980)
Gallo-Roman
0-300
AD 400-600
Mus musculus
De Roguin (in press)
BC
300 BC
BC
Vigne & Alcover ( 1985)
Corbet (1974)
AD
Vigne ( 1988b)
Abri du Casino, Island
M u sp.
of Zembra, Tunisia
Several undated appearances of the house mouse should be mentioned such as that in Malta, in the Cave of
Ghar Dalam (Storch, 1970) in which the house mouse was still not recorded in the “Apodemus layers” dated the
Bronze Age (Storch, 1974).
HOUSE MOUSE PROGRESSION I N EURASIA
WEST
AGE
4
b
21
EAST
Pr.
1000
1
-3000
I
-7000
Neolithic - Greece
fdS004OMl)
-8000
CYPRUS 0
0
Oldest M u remains in archaeological sites of West Eurasian
and N o h African regions
(7000Bc)
0 ISRAEL
-11ooo
Figure 2. Oldest Mus subfossils in archaeological sites reported for regions of West Eurasia and
North Africa.
We review chronologically the first appearances of the mouse in
archaeological sites of numerous west Eurasian regions, subsequent to its
appearance in the East Mediterranean Basin (Table 1). These data, summarized
in Fig. 2, allow the progression of this species in western Eurasia to be followed.
From c. 10 000 to 4000 BC, the house mouse occurred only in the Middle East,
where it was present during the Epipaleolithic in the Levant, in the
Pre-Neolithic of Cyprus, and the Neolithic of Anatolia. The house mouse arrived
in northern Europe as early as the end of the Vthmillenium in Belgium whereas
in Mediterranean (Spain, Italy and Mediterranean islands) and north central
Europe (Holland and Hungary), it only appeared in the Bronze Age and in
north-western Europe (France and Great Britain) in the Iron Age.
One can hardly conceive that the house mouse appeared 3 to 2 millenia earlier
in Belgium than in Mediterranean Europe on a route from the Middle East. This
discrepancy supports the existence of two separate colonization pathways from
an archaeozoological point of view. The explanation may be as follows: the
subfossils of Belgium have been found in a ribboned grave site; the so-called
ribboned civilization is a cultural extension of the Danubian Neolithic inflow
that diffused and/or progressed from the Middle Danube zone and from
southern Moravia. This cultural inflow coming from eastern Europe could have
favoured the progression of one branch of M . musculus from the north-west of the
Black Sea to northern Europe, that is, by a continental pathway.
However, the second branch which followed a Mediterranean route could not
be correlated with the extension of agricultural practices as the northern one
22
J.-C. AUFFRAY E T AL
was. The appearance of the house mouse in the Middle East preceeded
agricultural activities which have often been considered as the determining
factor in the spread of the house mouse. This suggests then that it is more the
building practices which, by creating new habitats, could have been the main
factor of invasion.
I n the same way, colonization of Mediterranean Europe which occurred at
the Bronze Age, that is, much later than the appearance of agriculture, suggests
that passive sea transport by man has also been a key factor. At that time,
extensive navigation became possible all over the western Mediterranean Sea
(Camps & D’Anna, 1980). Moreover, the early Bronze Age of western Europe
corresponds, in the East, to the beginning of the Aegean civilization and the
Middle Empire in Egypt. The birth of these progressive civilizations possibly
favoured an increase in sea trading but also modified its characteristics, for
example the kind and size of ships used, the number of passengers and the food
provisions taken aboard. From an archaeozoological point of view, it is in the
Bronze Age and in a very short time that the whole of western Mediterranean
Europe was colonized by the house mouse (see Fig. 2). The low genetic
differentiation within all southern European populations of M . m. domesticus
(Britton-Davidian, 1990) supports this hypothesis. Indeed, based on the
distribution of extant subspecies of M . musculus in Europe (Fig. l ) , we attribute
the continental pathway to M . m. musculus and the Mediterranean one to
M . m. domesticus.
Fossils of Belgium and Holland that are representative of the continental
inflow should then be attributed to M . m. musculus. However, M . m. domesticus is
the subspecies presently found in these two countries. This faunal substitution
could be explained by a retreat of M . m. musculus in the face of the progression of
M . m. domesticus, a retreat that is supported by the present distribution of the two
subspecies of the house mouse in Denmark and northern Germany and by the
mitochondria1 and nuclear genome patterns of the Danish mice (see
introduction).
According to palaeontological data the date of the contact between these two
subspecies depends on where it took place. It may have occurred at a very early
date in eastern Europe (Bulgaria, Greece) from the Epipaleolithic to the Bronze
Age, but certainly not later than the Bronze Age and probably closer to the Iron
Age in central and northern Europe.
This hypothesis on the colonization dynamics of Europe by the house mouse
based on archaeozoological data, is consistent with the genetical surveys of
extant mice. Confirmation of this hypothesis will be possible only by
morphological or morphometrical identification of the subfossil subspecific
status, enabling clarification, for instance, of whether Belgium and Dutch fossils
should be referred to M . m. musculus instead of M . m. domesticus as present.
Morphometrical discrimination between the two subspecies is already possible
on extant material, on the basis of cranial and mandibular measurements treated
by multivariate analyses (Gerasimov et al., 1990). Studies should now be
undertaken to determine the subspecific status on the most common fossil
material such as teeth.
ACKNOWLEDGEMENTS
The authors thank Franqois Bonhomme, Louis Thaler, Jean-Denis Vigne for
their very helpful comments on the manuscript.
HOUSE MOUSE PROGRESSION IN EURASIA
23
REFERENCES
ALCADE-CURT, G., 1986. Les faunes de rongeurs du Pl6istocine supdrieur et de I‘Holocine de Catalogne (Espagne) et
leurs signiJications pallookologiques el palloclimatiques. Unpublished Ph.D. Thesis, Ecole Pratique des Hautes
Etudes, Paris.
AUFFRAY, J. C., TCHERNOV, E. & NEVO, E., 1988. Origin of the commensalism of the house mouse
( M u s musculus domesticus) in relation to man. Comptes Rendus de I‘Acadlmie des Sciences, Paris, 307: 517-522.
AUFFRAY, J. C., TCHERNOV, E., BONHOMME, F., HETH, G., SIMSON, S. & NEVO, E., 1990.
Presence and ecological distribution of Mus musculus domesticus and Mus “spretoides” in Israel.
Circum-Mediterranean vicariance in the genus M u s . Zeitschriflfur Suugetierkunde, 55: 1-10,
BOEKSCHOTEN, G. J. & SONDAAR, P. Y., 1972. O n the fossil mammalia of Cyprus I & 11. Proceedings of
the Koninklijke Nederlandse Akademie uan Wetenschappen, Amsterdam, 75: 306-338.
BONHOMME, F., 1986. Evolutionary relationships in the Genus M u s . Current topics in Microbiology and
Immunology, 127: 119-124.
BONHOMME, F., CATALAN, J., GERASIMOV, S., ORSINI, P. & THALER, L., 1983. Le complexe
d’espkce du genre M u s en Europe Centrale et Orientale-I. GCnktique. zeitschrifl fur Suugetierkunde, 48:
78-85.
BONHOMME, F., CATALAN, J., BRITTON-DAVIDIAN, J., CHAPMAN, V. M., MORIWAKI, K.,
NEVO, E. & THALER, L., 1984. Biorhemical diversity and evolution in the genus M u s . Biochemical
Genetics, 22: 275-303.
BOURSOT, P., BONHOMME, F., BRITTON-DAVIDIAN, J., CATALAN, J., YONEKAWA, H.,
ORSINI, P., GERASIMOV, S. & THALER, L., 1984. Introgression diffkrentielle des gknomes nucltaires
et mitochondriaux chez deux semi-espkces europeennes de souris. Comptes Rendus de I’Acadlmie des Sciences,
Paris, 299: 691-693.
BRITTON, J. & THALER, L., 1978. Evidence for the presence of two sympatric species of mice (Genus
M u s L.) in southern France based on the biochemical genetics. Biochemical Genetics, 16: 213-225.
BRITTON-DAVIDIAN, J., 1990. Genic differentiation in M u s musculus domesticus populations from Europe,
the Middle East and North Africa: Geographic patterns and colonization events. Biological Journal of the
Linnean Society, 41: 27-45.
BROTHWELL, D., 1981. The Pleistocene and Holocene archaeology of the house mouse and related species.
Symposia of the zoological Society, London, 47: 1-13.
BRUNET, M., CARBONNEL, J. P., HEINTZ, E. & SEN, S., 1980. Premikres dkcouvertes de VertCbres dans
les formations continentales de Pul-e Charkhi, bassin de Kabul, Afghanistan; implications stratigraphiques.
Bulletin du Museum National d’Histoire Naturelle, Paris, 2: 277-285.
CAMPS, G. & D’ANNA, A,, 1980. Recherches sur les navigations prkhistoriques en Mkditerranke
Occidentale. In Actes de la Table Ronde d u Groupement d’IntkrCt Scientifique, Sciences Humaines sur
I’Aire MCditerrankenne, Nauigation et gem de M e r en Mlditerranle de la Prlhistoire ri nos Jours: 1-16. Paris:
Editions d u Centre National de la Recherche Scientifique.
CHALINE, J., 1971. La microfaune du Vallonet (A,-M.) et le problkme des corrtlations
micromacromammiferes a la limite Pltistockne inferieur-moyen. Bulletin du Musde d’Anthropologie Prlhistorique
de Monaco, 17: 65-69.
CHEYLAN, G., CROSET, H. & MICHAUX, J., in press. Of Mice and Men. Colloque International du Centre
National de la Recherche ScientiJique “Histoire des Inuasions”, Montpellier. Paris: Editions du Centre National de la
Recherche Scientifique.
CORBET, G. B., 1974. The distribution of mammals in historical times. I n D. L. Hawksworth (Ed.), The
Changing Flora and Fauna of Britain: 174-202. London & New York: Academic Press.
CORDY, J.-M. & STASSART, M., 1982. La faune omalienne de la Place Saint-Lambert (Liege). Notae
Praehistoricae, 2: 105-1 10.
CRISTALDI, M. & FEDERICI, R., 1980. Conseguenze storico-evolutive del commensalismo del topolino
delle case ( M u s musculus) con la specie umana. Unicopli Uniuersitaria, 68: 1-73.
DARVICHE, D. & ORSINI, P., 1982. Critkres de diffkrenciation morphologique et biomktrie de deux espkces
de souris sympatriques: M u s spretus et Mus musculus domesticus. Mammalia, 43: 205-2 17.
D E ROGUIN, L., in press. Donnkes historiques nouvelles sur la prksence du rat noir Raltur rattus (L.) en
Europe occidentale. I n M. Le Berre (Ed.), Actes du 22me Colloque International “L e Rongeur el I‘Espace”, Lyon
1989. Lyon.
FERRIS, S. D., SAGE, R. D., HUANG, C. M., NIELSEN, J. T., RITTE, U . & WILSON, A. C., 1983a.
Flow of mitochondrial DNA across a species boundary. Proceedings of lhe National Academy of Sciences, U . S . A . ,
80: 2290-2294.
FERRIS, S. D., SAGE, R. D., PRAGER, E. M., RITTE, U. & WILSON, A. C., 1983b. Mitochondria1 DNA
evolution in mice. Genetics, 105: 681-721.
FLYNN, L. J. &JACOBS, L. L., 1982. Effects of changing environments on Siwalik rodent faunas of northern
Pakistan. Paleogeography, Paleoclimatology, Paleoecology, 38: 129-1 38.
GERASIMOV, S., NIKOLOV, H., MIHAILOVA, V., AUFFRAY, J.-C., BONHOMME, F., 1990.
Morphometrical stepwise discriminant analysis of the five genetically determined European taxa of the
genus M u . Biological Journal of the Linnean Society, 41: 47-64.
GYLLENSTEN, U. & WILSON, A. C., 1987. Interspecific mitochondrial DNA transfer and the colonization
of Scandinavia by mice. Genetical Research, Cambridge, 49: 25-29.
24
J.-C. AUFFRAY ET A L .
JACOBS, L. L., 1982. Fossil rodents (Rhizomyidae & Muridae) from Neogene Siwalik Deposits, Pakistan.
Museum of Northern Arizona Press, Bulletin Series, 52: 1-103.
JACOBS, L. L. & PILBEAM, D., 1980. Of Mice and Men: Fossil-based divergence dates and molecular
“clocks”. Journal of Human Evolution, 9 : 551-555.
JAEGER, J. J., 1970. Dtcouverte au Jebel Ihroud des premikres faunes de rongeurs du Pltistockne inftrieur et
moyen du Maroc. Comptes Rendus de l‘Acadimie des Sciences, Paris, 270: 920-923.
JAEGER, J. J., 1971. Les micromammiferes du “Villafranchien” inftrieur du Lac Ichkeul (Tunisie): DonnCes
stratigraphiques et biogtographiques nouvelles. Comptes Rendus de l’Acadkmie des Sciences, Paris, 273: 562-565.
JAEGER, J. J., 1975a. Les Muridae (Mammalia, Rodentia) du Plioclne et du Pliistoclne du Maghreb. Origine;
Evolution; Donnies biogdographiques et palioclimatiques. Unpublished Ph.D. Thesis, University of Montpellier.
JAEGER, J. J., 1975b. The mammalian faunas and hominid fossils of the Middle Pleistocene of the Maghreb.
In K. W. Butzer & G. U. Isaac (Eds), After the Australopithecines: 399418. The Hague: Mouton Publishers.
JAEGER, J. J., 1977. Les rongeurs du Miockne moyen et suptrieur du Maghreb. Paleouertebrata, 8 : 1-164.
JAEGER, J. J. & WESSELMAN, H. B., 1976. Fossil remains of micromammals from the Omo group deposits.
In Y. Coppens, F. Clark-Howell, G. L. I. Isaac & R. E. F. Leakey (Eds), Earliest M a n and Environments in the
Lake Rudolf Basin. Stratigraphy, Paleoecology and Evolution: 35 1-360. Chicago: University of Chicago Press.
JAEGER, J . J., TONG, H. & DENYS, C., 1986. The age of Mus-Rattus divergence: paleontological data
compared with the molecular clock. Comptes Rendus de l‘Acadimie des Sciences, Paris, 14: 91 7-922.
JAEGER, J. J., TONG, H., BUFFETAUT, E. & INGAVAT, R., 1985. The first fossil rodents from Northern
Thailand and their bearing on the problem of the origin of the Muridae. Revue de Palkobiologie, 4: 1-7.
JANOSSY, D., 1986. Pleistocene Vertebrate Faunas of Hungary. Amsterdam: Elsevier Science Publishers.
KORDOS, L., 1978. Historico-zoogeographicaland ecological investigation of the subfossil vertebrate fauna of
the Aggtelek Karst. Vertebrata hungarica, 18: 85-100.
KOTSAKIS, T. & RUSCHIONI, E., 1984. I microvertebrati di un insediamento dell’Eti del Ferro presso
Tortoreto (Teramo, Italia centrale). Atti della Academia nozionale dei Lincei, S.8,76: 29C297.
LEPIKSAAR, J., 1980. Animal remains at Tornror. A study of a Thanatocoenosis (Late Iron Age to recent
times). Striae, 10: 3-41,
MAYHEW, D. F., 1977. The endemic Pleistocene Murids of Crete. Proceedings of the Koninklijke Nederlandse
Akademie van Wetenschappen, Amsterdam, 80 ( 3 ) : 182-199.
MILLOTE, J:P. & THEVENIN, A,, 1988. Les Racines de Europiens, des Origines aux Celtes. Le Coteau: Editions
Horwath.
ORSINI, P., 1982. Facteurs rigissant la ripartition des souris en Europe: Intirtt du modlle souris pour une apfroche des
processus ivolutifs. Unpublished Ph. D. Thesis, University of Montpellier 11.
ORSINI, P., CASSAING, J., DUPLANTIER, J.-M. & CROSET, H., 1982. Premikres donntes sur I’tcologie
des populations naturelles de souris, Mus spretus Lataste et M u s musculus domesticus Rutty, dans le midi de la
France. Revue d’Ecologie (Terre Vie), 36: 322-336.
ORSINI, P., BONHOMME, F., BRITTON-DAVIDIAN, J., CROSET, H., GERASIMOV, S. &
THALER, L., 1983. Le complexe d’espkces du genre M u s en Europe Centrale et Orientale. 11-Critkres
d’identification, rtpartition et caracttristiques tcologiques. zeitschrift fur Saugetierkunde, 48: 86-95.
REUMER, J. W. F. & SANDERS, E. A. C., 1984. Changes in the vertebrate fauna of Menorca in prehistoric
and classical times. zeitschrift fur Saugetierkunde, 49: 32 1-325.
SABATIER, M., 1982. Les rongeurs du site Pliockne a hominidCs de Hadar (Ethiopie). Paleovertebrata, 12 (I):
1-56.
STORCH, G . , 1970. Holozane Kleinsaugerfunde aus der Ghar Dalam-Hohle, Malta (Mammalia: Insectivora,
Chiroptera, Rodentia). Senckenbergianaa Lethaea, 51: 135-145.
STORCH, G . , 1974. Quartare Fledermaus-Faunen von der Insel Malta. Senckenbergianaa Lethaea, 55: 407-434.
STORCH, G., 1975. Eine mittelpleistozane Nager-Fauna von der Insel Chios. Senckenbergianaa Lethaea, 56:
165-1 89.
STORCH, G . , 1988. Eine jung-pleistozane/altholozane Nager-Abfolge von Antalya, SW-Anatolien
(Mammalia-Rodentia). zeitschrift fur Saugetierkunde, 53: 76-82.
TCHERNOV, E., 1984. Commensal animals and human sedentism in the Middle East. In J. Clutton Brock &
C. Grigson (Eds), Animals and Archaeolop - 3 : Early Herders and their Flocks, Series 202: 91-1 15. Oxford:
B.A.R. International Series.
TCHERNOV, E., 1986. Les mammiferes du PlCistocene inftrieur de la vallCe du Jourdain a Oubeidiyeh.
Mlmoires et Travaux du Centre Franfais de Jerusalem, 5: 235-350. Paris: Association PalCorient.
THALER, L., 1986. Origin and evolution of mice: an appraisal of fossil evidence and morphological traits.
Current Topics in Microbiology and Immunology, 127: 3-1 1.
THALER, L., BONHOMME, F. & BRITTON-DAVIDIAN, J., 1981. Processes of speciation and semispeciation in the house mouse. Symposia of the zoological Society, London, 47: 27-41.
VALLA, F. R., 1988. Les premiers stdentaires de Palestine. La Recherche, 199: 576-584.
VAN DE WEERD, A., 1973. Rodentia from two Pleistocene fissure fillings near Athens. Proceedings of the
Koninklijke Nederlandse Akademie van Wetenschappen, Amterdam, 76 ( 2 ) : 148-1 66.
VANLERBERGHE, F., BOURSOT, P., NIELSEN, P. & BONHOMME F., 1988a. Past and present
exchanges across the hybrid zone between M u s musculus domesticus and M . m. musculus in Denmark:
Comparative introgression of autosomal genes, mitochondria1 DNA and the Y chromosome. Genetical
Research, 52: 185-193.
HOUSE MOUSE PROGRESSION I N EURASIA
25
VANLERBERGHE, F., BOURSOT, P., CATALAN, J., GERASIMOV, S., BONHOMME, F., BOTEV, A.
& THALER, L., 198813. Analyse gknktique de la zone d’hybridation entre les deux sous-espPces de souris
Mus musculus domesticus et M u s musculus musculus en Bulgarie. Genome, 30: 427-437.
VERESHCHAGIN, N. K., 1967. The Mammals ofthe Caucasus. A History of the Evolution ofthe Fauna. Jerusalem:
Israel Program for Scientific Translation.
VIGNE, J . D., 1988a. Biogtographie insulaire et anthropozoologie des socittts nkolithiques mtditerrantenne:
htrisson, renard et micromammiferes. Anthropozoologica, 8: 3 1-52.
VIGNE, J. D., 198813. Donnkes prkliminaires sur l’histoire du peuplement mammalien de l’ilot de Zembra
(Tunisie). Mammalia, 52: 567-574.
VIGNE, J. D. & ALCOVER, J. A,, 1985. Incidence des relations historiques entre I’homme et l’animal dans la
composition actuelle du peuplement amphibien, reptilien, mammalien des iles de Mkditerrante
occidentale. Actes du IlO2me Congrh des Sociltis Sauantes, Montpellier 1985, Sciences 2: 79-91.
VIGNE, J. D. & MARINVAL-VIGNE M . C., in press. Chronologie du renouvellement faunique Holocene
des micromammiferes en Corse: premiPres donntes sur la faune du Monte di Tuda. In M. Le Berre (Ed.),
Actes du 2kme Colloque International “Le Rongeur et l‘Espace”, Igon (989. Lyon.
YONEKAWA, H., MORIWAKI, K., GOTOH, O., MIYASHITA, S., BONHOMME, F., HJORTH, J. P.,
PETRAS, M. L. & TAGASHIRA, Y., 1982. Origins of laboratory mice deduced from restriction patterns
of mitochondria1 DNA. Diferentiation, 22: 222-226.