Several recent papers, including one in BMC Evolutionary Biology, examine the colonization history of house mice. As well as background for the analysis of mouse adaptation, such studies offer a perspective on the history of movements of the humans that accidentally transported the mice

Gabriel, Sofia I

Jones, Eleanor P

Jóhannesdóttir, Fríða

Searle, Jeremy B

English

PubMed

Sofia I Gabriel

Fríða Jóhannesdóttir

Eleanor P Jones

Jeremy B Searle

Springer - Publisher Connector

Commensals of humans are likely to share the human 
global distribution. Being easily noticed, and surviving 
and reproducing well in environments that humans 
create, they also include some of the most favored model 
organisms. A prime example of this is the house mouse, 
Mus musculus, which is both the ‘classic’ mammalian 
model organism and a globally present commensal. 
Through its association with humans, the house mouse is 
even found in the remotest archipelagos, such as 
Kerguelen, a group of sub-Antarctic islands with a mean 
summer temperature as low as 8°C. It is the mouse 
populations inhabiting this inhospitable place that are the 
focus of a study by Hardouin et al. in BMC Evolutionary 
Biology [1].
With all the genomic tools available, there is currently a 
scramble to study the genetics of adaptation in house 
mice. What better place to study that than Kerguelen? 
Here, human occupancy is restricted to the few inhabi-
tants of a research station on the main island (Grande 
Terre). The mice on these islands live outdoors in extreme 
conditions and, in contrast to the typical seed-eating of 
house mice elsewhere, they feed primarily on inver-
tebrates. To understand the adaptations for this excep-
tional lifestyle, it is important to know something about 
the history of the mice. In particular: where did the mice 
come from? Is it a genetically mixed population? Is the 
population young or old? Hardouin et al. [1] investigated 
all these questions for Kerguelen house mice which belong 
to the western subspecies, Mus musculus domesticus.
The Kerguelen study
Hardouin et al.’s study [1] involved 437 mice from 
Kerguelen, an unprecedented coverage for the analysis of 
colonization history of such a small area. They found 
remarkable consistency in the mitochondrial DNA 
(mtDNA) sequences on Grande Terre and most of the 
surrounding small islands, suggesting that these 
populations are the product of a single relatively recent 
colonization (ultimately deriving from Europe). This fits 
with the recorded discovery of the archipelago in 1772 
(by a Frenchman called Kerguelen-Trémarec) and settle-
ment by mice either at the time or with subsequent 
human arrivals. Two of the other small islands in the 
archipelago (Cochons and Cimetière) may have been 
colonized in a second, separate introduction, as their 
mice belong to a different mtDNA lineage (also ultimately 
European). Over the archipelago as a whole there was no 
evidence of within-island heterogeneity in terms of 
mtDNA lineage. This is surprising given the large number 
of ships carrying mice that would have visited the islands 
(coming from many different places and therefore 
carrying mice of many different mtDNA lineages). These 
results are consistent with other data [2] suggesting that 
mouse populations are resistant to secondary invasion by 
females (mtDNA is a maternally inherited marker). 
Presumably, newly arriving females coming into an 
established population are generally unable to survive or 
gain mates, and in consequence do not contribute to the 
population’s gene pool. All of this means that mtDNA 
may be a very good marker for initial colonization by 
house mice within a given area.
Studies on European mice
The association of Mus musculus domesticus with 
humans in a European context has long been studied by 
zooarcheologists, and genomic tools are now being 
deployed to study adaptation in some of these European 
populations. With regard to colonization history, there is 
much zooarcheological evidence on the progression of 
Abstract
Several recent papers, including one in BMC 
Evolutionary Biology, examine the colonization history 
of house mice. As well as background for the analysis 
of mouse adaptation, such studies offer a perspective 
on the history of movements of the humans that 
accidentally transported the mice.
Colonization, mouse-style
Sofia I Gabriel1, Fríða Jóhannesdóttir2, Eleanor P Jones3 and Jeremy B Searle*2
See research article: http://www.biomedcentral.com/1471-2148/10/325
CO M M E N TA RY  Open Access
*Correspondence: jeremy.searle@cornell.edu 
2Department of Ecology and Evolutionary Biology, Cornell University, Corson Hall, 
Ithaca, NY 14853-2701, USA 
Full list of author information is available at the end of the article
© 2010 Gabriel et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons 
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any 
medium, provided the original work is properly cited.
Gabriel et al. BMC Biology 2010, 8:131 
http://www.biomedcentral.com/1741-7007/8/131
mice from their site of first commensalism with humans 
in the Near East through the Mediterranean region, 
providing a good test on the match between mtDNA 
sequences and the historical record. Gratifyingly, Bon-
homme et al. [3] have identified a discontinuity in mtDNA 
lineages that fits very well with the two phases of mouse 
colonization of the Mediterranean revealed by zoo-
archeologists (Figure 1). The eastern Mediterranean was 
colonized by mice during the Neolithic when they were 
first able to exploit stored grain. However, the western 
Mediterranean could not be colonized by house mice until 
the Iron Age (Figure 1), when settlements reached a suffi-
cient size for the house mice not to be outcompeted by 
local mice living outdoors, and when seafarers such as the 
Phoenicians carried cargoes of sufficiently large size to 
inadvertently transport house mice [3,4].
Studies by ourselves and others have looked at the 
mtDNA lineages of house mice in northern Europe. A 
different lineage from those typically seen in Mediter-
ranean Europe has been found further north in the area 
between Britain and Germany [2,5]. The mouse mtDNA 
again matches a regional sphere of influence of Iron Age 
people [6], and, unlike other mouse mtDNA lineages, it 
appears that this Anglo-German lineage did not arrive in 
northern Europe by an overland route; instead it probably 
came along the Atlantic coast (Figure 1).
Figure 1. Maps showing possible colonization routes taken by the western house mouse Mus musculus domesticus, based on mtDNA 
evidence. Neolithic (starting 12,000 years ago): colonization restricted to the eastern Mediterranean close to where this subspecies first became 
commensal [3]. Iron Age (starting 3,000 years ago): colonization westwards along the Mediterranean and then into north-west Europe by 
overland and coastal routes [3,5]. Viking Age (around 1,000 years ago): movements around the periphery of north-west Europe and colonization of 
Scandinavia and Madeira [2,5,7,8]. (The colonization of Scandinavia may have been earlier [7].) Recent history (a few hundred years ago): mice were 
taken substantial distances from western Europe, including to Kerguelen [1]. The dashed line shows the location of the hybrid zone between the 
subspecies M. m. domesticus and M. m. musculus.
Viking Age
Neolithic Iron Age
Recent history
Gabriel et al. BMC Biology 2010, 8:131 
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Page 2 of 3
mtDNA studies suggest another pulse of detectable 
mouse colonizations during Viking times (Figure 1). Like 
the Phoenicians, the Vikings were impressive seafarers, 
carrying substantial cargoes ideal for stowaway mice, and 
there are mtDNA signals of maritime colonization events 
[2,5,7,8].
How did Mus musculus domesticus get from Europe to 
Kerguelen? This subspecies had been in the right place at 
the right time to make use of the first storage of grain by 
Neolithic humans in the Fertile Crescent in the Middle 
East, and to adapt to changing human cultural practices. 
Good fortune struck again when the subspecies found 
itself in western Europe at the time that British, Dutch, 
French and Iberian seafarers were ‘discovering’, exploiting 
and taking settlers to the rest of the world. Kerguelen-
Trémarec and his crew may have been the first humans 
to see the archipelago that now bears his name, but the 
colonization route of the first mice to arrive there is still 
uncertain, although their starting point was certainly 
western Europe (Figure 1).
Mice as a proxy for human history
It is intriguing how far the linkage between human 
history and mouse history may go. Jones et al. [8] found a 
correlation between mouse genetic diversity and human 
population size (proportional to amount of mouse 
habitat) in discrete areas of the Faroe Islands in the 
north eastern Atlantic Ocean, another archipelago where 
house mice have been studied. This supports the expec-
tation that the population genetics (in terms of genetic 
response to population expansions and contractions) of 
house mice is likely to reflect rather closely the popu-
lation genetics of humans.
We have been considering how the history of humans 
impacts on the genetics of the house mouse, but that can 
be turned around. If the history of house mice is so 
intimately determined by humans, then the genetics of 
house mice may be useful to answer human historical 
questions; for example, the details of human affiliations 
in the Iron Age are sometimes imprecise - might house 
mice be able to indicate associations between Iron Age 
people from different geographical areas? House mice are 
equivalent to an artifact that an archeologist discovers 
and uses to determine human colonization or trading 
routes. The provenance of the mice is established from 
their DNA sequence and that is a very powerful tool, 
given its extraordinary information content. Not only can 
the DNA sequence help to establish the source of the 
mice found in a particular place but it can be used to date 
the original colonization and subsequent population 
history (including secondary colonizations), following 
approaches used for human DNA (see, for example [9]). 
However, it is clear from all the recent papers considered 
here [1,3,5,7,8] that archeogenetics using house mice is at 
an early stage, and that, in particular, calibrations to 
generate an accurate mouse mtDNA molecular clock are 
urgently needed. Hardouin et al. [1] comment that, for 
the mtDNA region analyzed, they found a much higher 
mutation rate than suggested by previous studies. Further 
work should follow up this finding and also use other 
subspecies to globalize the opportunities for applying 
mice as a proxy to study humans, following the lead of 
another recent paper [10].
Acknowledgements
SIG was funded by the scholarship SFRH/BD/21437/2005 from Fundação para 
a Ciência e a Tecnologia (Portugal), FJ and JBS by Cornell University (USA) 
and EPJ by the Carl Trygger Foundation (Sweden). We are grateful to Angela 
Douglas for her comments on the manuscript.
Author details
1CESAM - Centre for Environmental and Marine Studies, Departamento de 
Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, 1749-016 
Lisbon, Portugal. 2Department of Ecology and Evolutionary Biology, Cornell 
University, Corson Hall, Ithaca, NY 14853-2701, USA. 3Population Biology 
and Conservation Biology, Evolutionary Biology Centre, Uppsala University, 
Norbyvägen 18 D, SE-752 36 Uppsala, Sweden.
Published: 26 October 2010
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doi:10.1186/1741-7007-8-131
Cite this article as: Gabriel SI, et al.: Colonization, mouse-style. BMC Biology 
2010, 8:131.
Gabriel et al. BMC Biology 2010, 8:131 
http://www.biomedcentral.com/1741-7007/8/131
Page 3 of 3


Colonization, mouse-style

Abstract Several recent papers, including one in BMC Evolutionary Biology, examine the colonization history of house mice. As well as background for the analysis of mouse adaptation, such studies offer a perspective on the history of movements of the humans that accidentally transported the mice. See research article: http://www.biomedcentral.com/1471-2148/10/325</p

Searle Jeremy B

Jones Eleanor P

Jóhannesdóttir Fríða

Gabriel Sofia I

Directory of Open Access Journals

BMC Biology

Crossref

Several recent papers, including one in BMC Evolutionary Biology, examine the colonization history of house mice. As well as background for the analysis of mouse adaptation, such studies offer a perspective on the history of movements of the humans that accidentally transported the mice.SIG was funded by the scholarship SFRH/BD/21437/2005 from Fundação para a Ciência e a Tecnologia (Portugal), FJ and JBS by Cornell University (USA) and EPJ by the Carl Trygger Foundation (Sweden)

Searle, Jeremy B.

eCommons@Cornell

Auffray J-C: First occurrence of the house mouse (Mus domesticus Schwarz & Schwarz,

Excoffier L: Statistical evaluation of alternative models of human evolution.

Genetic differentiation of the house mouse around the Mediterranean basin: matrilineal footprints of early and late colonization. Proc Biol Sci

H: Detection of recombinant haplotypes in wild mice (Mus musculus) provides new insights into the origin of Japanese mice.

Iron Age communities in Britain: an account of England, Scotland and Wales from the seventh century BC until the Roman conquest. 4th edition.

Jóhannesdóttir F: Of mice and (Viking?) men: phylogeography of British and Irish house mice. Proc R Soc B

Searle JB: A characterization of the charismatic Faroe house mouse. Biol J Linn Soc,

Searle JB: Norwegian house mice (Mus musculus/domesticus): Distributions, routes of colonization and patterns of hybridization. Mol Ecol,

Searle JB: The expansion of the house mouse into North-western Europe. J Zool,

Tautz D: House mouse colonization patterns on the sub-Antarctic Kerguelen Archipelago suggest singular primary invasions and resilience against re-invasion.

http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2964602

Colonization, mouse-style

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