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INVASIVE RODENTS ON ISLANDS
Mitochondrial DNA evidence for the spread of Pacific rats
through Oceania
Elizabeth Matisoo-Smith ÆJudith Robins
Received: 6 June 2008 / Accepted: 29 September 2008
ÓSpringer Science+Business Media B.V. 2008
Abstract In the 10 years since we published our
first full analysis of mitochondrial DNA (mtDNA)
variation in Rattus exulans as a means for tracking
human migration in Polynesia, we have extended the
commensal approach through time and space with the
use of ancient DNA (aDNA) and by analysing
samples from across the Pacific. Not only can
mtDNA phylogenies provide information regarding
population origins and paths of migration, they have
also provided information regarding degrees of
contact and interaction between islands. An important
extension of the R. exulans project is the creation and
on-going development of a genetic database for the
identification of Rattus species based on mtDNA
sequences. The phylogenetic analysis of sequences
from 18 species and 1 subspecies of Rattus thus far
have raised some questions regarding species iden-
tification and species distributions in the Pacific.
Keywords Rattus exulans Pacific prehistory
Ancient DNA
Introduction: the commensal model
In the mid 1990s a program developing a new genetic
model for understanding the human settlement of the
Pacific was undertaken at the University of Auckland
(Matisoo-Smith 1994; Matisoo-Smith et al. 1997,
1998). Given the concerns of indigenous peoples
about the use and study of human tissues at the time,
coupled with the recognised lack of genetic variation
in Polynesian populations (Hertzberg et al. 1989; Hill
and Serjeantson 1989), it was concluded that perhaps
an alternative method for identifying population
origins and tracking prehistoric human migration
patterns might be to use a proxy. Instead of studying
the genetic relationships of the people themselves, we
could trace their migration patterns by studying the
things that they carried with them in their colonising
canoes. The archaeological evidence strongly
suggested that Polynesians and their ancestors trans-
ported numerous plants and animals with them and
introduced those species to the islands of Remote
Oceania (Kirch 2000). If we could identify the genetic
relationships and track the origins of those plants and
animals around the Pacific, these might indicate the
immediate origins and the movement of the people
who carried them. Thus we began to develop and test
what we now refer to as the commensal model for the
human settlement of the Pacific (Matisoo-Smith 1994;
Matisoo-Smith et al. 1998).
In this paper we will review the development of
the R. exulans commensal model for tracking
E. Matisoo-Smith (&)J. Robins
Department of Anthropology and Allan Wilson Centre for
Molecular Ecology and Evolution, University of
Auckland, Private Bag 92019, Auckland, New Zealand
e-mail: e.matisoo-smith@auckland.ac.nz
123
Biol Invasions
DOI 10.1007/s10530-008-9404-1
prehistoric human migrations in the Pacific. We will
also discuss the projects that have been generated
from some of the methodological problems encoun-
tered in the commensal study, specifically the
development of species identification methods for
both modern and ancient Rattus samples. Finally, we
will briefly discuss the impact and possible applica-
tions of the results of these projects for island
conservation programs.
Rattus exulans and the commensal model
It is generally accepted that the first people to settle
the islands of Remote Oceania, or those islands east
of the main Solomon Island chain, were those
associated with the Lapita culture. These Lapita
people transported with them, in their canoes, dogs,
pigs, chickens and rats, and introduced them to the
pristine island environments they settled. Lapita
settlement resulted in the relatively rapid settlement
of islands as far east as Samoa and Tonga and it is
from these Lapita settlements that the ancestors of the
Polynesians originated. Polynesians continued to
transport the commensal animals throughout the
Polynesian triangle.
The first animal that was used to develop this
commensal model for Pacific settlement was the
Pacific rat, R. exulans,orkiore as it is known in New
Zealand. This rat was chosen for a number of reasons.
First, it was the most widely distributed of all of the
commensal animals that were transported by Pacific
peoples. R. exulans bones are found in early if not the
earliest archaeological layers throughout most islands
of Polynesia. They are also found in early layers of
most Lapita sites in both Near and Remote Oceania.
Extant populations are still found on most islands
across the Pacific, and since R. exulans are a different
species from those rodents introduced by Europeans
(Rattus rattus and Rattus norvegicus), they do not
interbreed with those later arrivals. Unlike the dogs,
pigs and chickens carried by Pacific peoples, that
have since interbred with European introduced ani-
mals, the R. exulans found on Pacific islands today
are the direct descendents of those rats introduced by
the early Pacific colonists. In addition, it appears that
they have not been transported in historic vessels and
therefore their distribution remains directly related to
prehistoric human dispersal.
Study of mtDNA variation in Polynesian
R. exulans
The first test of the commensal model involved the
study of mtDNA variation in extant populations of R.
exulans throughout Polynesia (Matisoo-Smith 1994;
Matisoo-Smith et al. 1998). Samples were collected
from Fiji, Samoa, New Zealand, the Cook Islands, the
Society Islands, the Marquesas, the Kermadecs, the
Chathams and Hawaii. A total of 94 samples were
analysed for variation in 432 base pairs (bp) of the
hypervariable control region within the mitochondrial
genome. The results of the analyses were remarkably
consistent with both archaeological data and oral
traditions. A central region encompassing the Soci-
eties and the Southern Cook Islands was identified
from which the other central East Polynesian popu-
lations were derived. Interestingly, the Marquesas did
not appear to be part of this central ‘‘homeland
region’’, yet the Hawaiian R. exulans populations
were clearly derived from those in both the Marque-
sas and the central homeland, which is consistent
with linguistic and archaeological models for Hawai-
ian origins. The R. exulans populations in New
Zealand also appeared to be the result of multiple
introductions, most likely from this central homeland
region. The Kermadec Islands seemed to have been a
stepping stone location for movements between New
Zealand and the central homeland as predicted by
Irwin (1992). The introduction of rats to the Chat-
hams was most likely the result of a single or very
limited number of voyages from a single location,
most likely the South Island of New Zealand
(Matisoo-Smith et al. 1998,1999).
Development of ancient DNA methods
Once it was shown that the commensal model for
tracking migrations through Polynesia did work, there
were a few more issues that needed to be addressed.
For example, while the mtDNA phylogenies sug-
gested that the New Zealand R. exulans were most
likely derived from both Cook Island and Society
Island populations, we could not identify the timing of
those introductions. In addition, since R. exulans are
no longer present on the North Island of New Zealand
(due to competition with European rodents), we did
not know for sure if the remnant R. exulans
E. Matisoo-Smith, J. Robins
123
populations, found primarily on the off-shore islands
around New Zealand, were truly representative of
those populations initially introduced to the mainland.
Similarly, other islands, such as Rapa Nui no longer
had extant populations of R. exulans, so our study was
limited. Luckily, the 1990s saw the rapid growth of
ancient DNA studies, and we were able to develop and
apply these methods to archaeological remains of
R. exulans (Matisoo-Smith et al. 1997).
R. exulans and chickens were the only two
commensal animals introduced to Rapa Nui and
R. exulans bones are found in large numbers through-
out early sites on the island. The potential impact of
this apparently large rat population on the native flora
of Rapa Nui, in particular on the Jubaea palm, has
recently been discussed by Hunt (2007) who suggests
that they may have contributed significantly to the
ecological collapse there that has received so much
attention (Diamond 2005). Unfortunately, mtDNA
analyses of the archaeological exulans bones were
unable to provide evidence as to the specific origin of
the canoes that first introduced them because all
belonged to the most common lineage (known as R9)
found throughout central East Polynesia (Barnes et al.
2006).
Analyses of archaeological remains allowed us to
further test the reliability of the commensal model in
numerous ways. Comparisons between archaeologi-
cal and extant mtDNA sequences in R. exulans from
the Chatham Islands indicated that there was little
variation in populations separated in time by
500 years or so, suggesting that there was little in
situ evolution taking place over the relatively short
periods of time represented in Polynesian prehistory
(Matisoo-Smith et al. 1999). This study also allowed
us to test Irwin’s (1992) ideas about island accessi-
bility and the implications of accessibility on the
number of R. exulans introductions to islands. It is
most likely that islands that were accessible would
receive more R. exulans introductions and therefore
would possess higher levels of mtDNA variation.
Similarly, islands that were isolated would receive
fewer introductions and thus would have rat popula-
tions with lower levels of variation. Our results were
consistent with this prediction. The R. exulans from
the Chatham Islands, which are located in the roaring
40s and are particularly difficult to reach safely
according to Irwin’s voyaging models, showed
almost no variation. The Kermadec Islands, on the
other hand, which Irwin argued were a stepping-stone
island for colonising voyages to New Zealand and
post-colonisation voyages between New Zealand and
Central East Polynesia, showed a much higher degree
of mtDNA variation in their R. exulans populations
(Matisoo-Smith et al. 1999). The lack of variation
identified in Rapa Nui rats was also indicative of a
limited number of introductions followed by relative
isolation of the island (Barnes et al. 2006).
Analyses of archaeological rat remains from New
Zealand also demonstrated what we assumed was a
likely situation—that there are ancient lineages in
archaeological samples which are no longer present
in extant R. exulans populations in New Zealand. We
found, for example, that the rats on the North Island
of New Zealand belonged to two major haplogroups,
whereas the rats from the South Island looked more
like the extant populations in that they belonged to
only one of those major haplogroups (Matisoo-Smith
et al. 2001; Matisoo-Smith 2002). The possible
absence or extinction of ancient lineages in extant
populations is a major problem facing many molec-
ular studies that focus exclusively on modern
populations to infer past behaviours or relationships.
Identifying more distant origins
The development and application of aDNA methods
to R. exulans remains also opened up the opportunity
to study the bigger question of the ultimate origins of
Polynesian populations and perhaps even the origins
of Lapita populations. With archaeological remains,
museum samples and additional tissue samples of
R. exulans from Near Oceania and Island Southeast
Asia we were able to study mtDNA variation across
time and space (Matisoo-Smith and Robins 2004).
One of the major surprises of this larger study was
that we were able to identify three distinct lineages of
R. exulans in the Pacific region—identified as Groups
I, II and III. The distribution of each of these
haplogroups was fairly well defined geographically:
Group I rats were found in the region spanning the
Philippines, Borneo and Sulawesi. Group II rats were
found from the Philippines through to New Guinea
and as far east as the Southeast Solomon Islands,
and perhaps further into Remote Oceania. Group III
rats were found almost exclusively in Remote
Oceania—including Vanuatu, New Caledonia, Fiji
Mitochondrial DNA evidence
123
and throughout both Polynesia and Micronesia. These
Group III rats, one might suggest, were most likely
dispersed as part of the Lapita expansion into Remote
Oceania. We were rather shocked, however, by the
fact that there appeared to be no Group III rats
anywhere in Near Oceania except from the island of
Halmahera in Wallacea. This was particularly sur-
prising given the accepted view linking the Lapita
dispersal in Remote Oceania to the earliest Lapita
settlements in the Bismarck Archipelago, in Near
Oceania.
We decided that the surprising lack of connection
between Near and Remote Oceanic lineages of
R. exulans could have three possible explanations.
First, the distribution could mean that those human
populations who introduced Group III rats to Remote
Oceania did not pass through Near Oceania, in which
case we had to seriously either reconsider our current
ideas about Pacific prehistory and the Lapita culture,
or we would have to reject the premise that R. exulans
were transported by the first colonists into Remote
Oceania. An alternative explanation, and one that
appeared to be much more likely given the archae-
ological and linguistic evidence linking the
colonisation of Remote Oceania with Near Oceania,
was that our sampling of populations within Near
Oceania was incomplete and that there were indeed
Group III rats in the region. This promulgated our
most recent research project which focuses on more
precise and directed sampling of R. exulans popula-
tions throughout Near Oceania, but particularly on the
most likely ‘‘Lapita target’’ islands in the Bismarck
Archipelago. In the last 2 years we have collected
both extant and archaeological R. exulans remains
from many islands including Manus, New Ireland,
Lihir, Tabar, New Hanover and some of the small
islands in the St. Matthias group. Interestingly, we are
now finding some overlap between Type II and Type
III R. exulans in Near Oceania which may help us
tease apart and better understand various episodes of
human migrations and rat introductions in the region.
Species identification
As part of this extended research focus on R. exulans
populations in Near Oceania and Island Southeast Asia
we encountered another difficulty which opened up a
new area of research for our group: the problem of
species identification. In Polynesia and throughout
most of Remote Oceania, there are a very limited
number of rodent species present. In Polynesia,
R. exulans was the only rat that was introduced
prehistorically. European ships later brought new
species, specifically Rattus rattus and Rattus norvegi-
cus and the house mouse (Mus musculus). These four
species are fairly easy to distinguish from one another
morphologically (Cunningham and Moors 1983,
McCormack unpublished data), though not always
with 100% reliability, particularly when only working
with skeletal remains. In western Micronesia, the
Reef/Santa Cruz Islands in the Southeast Solomons,
Vanuatu and Fiji, prehistoric voyagers introduced
other rat species in addition to R. exulans. Archaeo-
logical remains of the Asian rat, Rattus tanezumi
predate the appearance of R. exulans in western
Micronesia (Wickler 2004), and it appears that Lapita
canoes carried a New Guinea native rat, Rattus praetor
as far as Vanuatu and Fiji (White et al. 2000). The
islands of New Guinea and those of Southeast Asia of
course have numerous native rodent species and are in
fact the two most speciose regions for the genus Rattus
(Musser and Carleton 2005). It has been estimated that
there are between 11 and 14 native species of Rattus in
New Guinea with another five species introduced to
the region by humans (Musser and Carleton 2005;
Taylor et al. 1982). It is not surprising therefore that
with all of the additional possible species appearing in
both the archaeological record and as fresh tissue
samples, species identification was becoming a prob-
lem for our commensal studies. We therefore set out to
see if we could develop an mtDNA database to allow
us to reliably identify the rat species we were
collecting (Robins et al. 2007).
Our lab obtained DNA sequence from tissues of
118 rats which included 18 named species and 1 sub-
species of Rattus from Island Southeast Asia, New
Guinea, Australia and several Pacific Islands as
shown in Fig. 1 of Robins et al. (2007). We then
built a reference phylogeny using DNA sequence
from three regions of the mitochondrial genome,
d-loop, cytochrome band cytochrome oxidase I, and
developed a rat identification system similar to the
DNA Surveillance project designed for marine
mammal identification (Ross et al. 2003). The
phylogeny from the Bayesian partitioned likelihood
analysis (Huelsenbeck and Ronquist 2001) of the
concatenated sequences of all three regions of the
E. Matisoo-Smith, J. Robins
123
mitochondrial genome (approximately 2,000 bp in
total) resolved several well differentiated clades.
The phylogeny in Fig. 2 of Robins et al. (2007)
showed a major divergence that separated the rats of
Asia and Island Southeast Asia from those of New
Guinea and Australia and also resolved 16 well
supported clades. The term ‘‘nominal’’ species was
used for the rat identification as determined by the
collectors and or museums who provided us with the
tissue samples because these identifications were not
always consistent with the phylogenetic identifica-
tions. Nevertheless, 63% (10/16) of the clades had the
same nominal and phylogenetic identification and
these were largely compatible with the revised Rattus
taxonomy of Musser and Carleton (2005).
The inconsistencies between the nominal and the
phylogenetic species assignments were thought to be
due to a number of contributing factors: (1) The
complex and changing taxonomy makes species
assignment difficult and can result in name confusion,
e.g., Musser and Carleton (2005) list 49 synonyms for
R. exulans and over 80 for R. rattus; (2) The lack of
good morphological characters makes many rats
difficult to identify even from whole carcases. The
clade labelled exulans included all the R. exulans
samples and also, almost certainly because of misi-
dentification, one sample each of R. steini and
R. verecundus; (3) Some species appeared to be over
split, e.g., the clade labelled PNG I contained six
nominal species of native New Guinean rats, R. mor-
dax,R. niobe,R. novaeguineae,R. praetor,R. ruber
and R. steini all of which have in the past been
classified as subspecies of R. ruber (Taylor et al. 1982;
Musser and Carleton 2005); (4) Some species appeared
to be undersplit e.g., R. tanezumi samples fell into three
different clades although the singleton that was in the
clade labelled tiomanicus was probably misidentified.
One question that has often confused researchers is
the description and taxonomic status of R. tanez-
umi—specifically whether it is a subspecies of
R. rattus or indeed a distinct species. Musser and
Carleton (2005) identify seven groups within the
Rattus genus. One of these, the Rattus rattus group,
contains approximately 21 different species including
R. rattus and R. tanezumi. Within the species
R. rattus, two subgroups were identified based on
chromosome number: the Oceanian or European type
that has 2n=48 and the Asian type with 2n=42
(Yosida et al. 1974). It is this Asian type that Musser
and Carleton (2005) have designated R. tanezumi.
This Asian R. tanezumi is indigenous to Southeast
Asia, but it is also found in Japan, the Philippines,
Island Southeast Asia, New Guinea and several
Pacific islands mostly in Near Oceania and Microne-
sia, though it has been reported in Fiji (IUCN 2007).
The European/Oceanian variety, R. rattus, is believed
to have originated in India, reaching Europe by the
third century AD from where it was taken in sailing
vessels along the trading routes, around the world
(Innes 1990; Atkinson 1985). When R. rattus is
introduced to locations where R. tanezumi is already
present, R. rattus is generally only found around the
port areas. In the tree presented in Robins et al.
(2007) the European/Oceanian variety is most likely
represented by the rattus I clade (which includes
samples from New Zealand, Samoa, the Society
Islands and coastal New Guinea) and the Asian type
is represented by the tanezumi clade (made up of
samples from Japan, Hong Kong and Indonesia).
R. tanezumi is thought to be a complex; and Musser
and Carlton suggest a two taxon division is probably
appropriate. The two clades labelled tanezumi and
diardii, each containing a number of specimens, offer
support for this hypothesis (Robins et al. 2007).
It is clear that much more work needs to be done to
clarify a number of aspects of Rattus taxonomy, but
the sequence database we have built and the results of
our phylogenetic analyses demonstrate the value of
this approach not only for commensal studies and
understanding prehistory, but perhaps more impor-
tantly for ecological and conservation studies. The
identification of rat introductions to islands is
increasingly important as islands are now being
cleared of rats and set aside for bird conservation and
recovery programmes. Regular monitoring of these
islands is necessary in order to identify any possible
re-introductions. The ability to quickly identify either
trapped rodents or even rodent droppings found on
important rat-free islands can help identify the source
of that introduction. We have so far been able to
assist the New Zealand Department of Conservation
and other organisations by using our species identi-
fication database to help identify and in some cases
source the introduced rodents. The database and tree-
based species identification programme ‘What rat is
that?’ is now publicly available on-line as part of the
DNA surveillance project at http://www.dna-surveil
lance.auckland.ac.nz.
Mitochondrial DNA evidence
123
Conclusion
It has been nearly 15 years since we started working on
genetic variation in R. exulans and the value of the
commensal approach for tracking human presence on
and paths of migrations to Pacific islands has been
clearly demonstrated. A most interesting current and
future development for better understanding the
human settlement of the Pacific is the comparison of
mtDNA phylogenies of R. exulans and the other
Pacific commensal animals, the dog, pig, and chicken,
as well as commensal plants such as taro, sweet potato
and bottle gourds. Each of these commensal stories can
be telling us about various human activities and
voyages, all leading to a better understanding of
human mobility in Pacific prehistory. In addition much
will be illuminated by fully considering and compar-
ing the commensal genetic data with the rapidly
increasing human genetic data from Pacific and Island
Southeast Asian populations. We are already recogn-
ising through commensal studies that the history of
human settlement of the Pacific is much more complex
than some early models suggest (Matisoo-Smith
2007). Additional studies will most likely only add
to our appreciation of how complex that history was.
Perhaps the surprising additional benefit from the
development of the commensal model is the potential
use of the large amount of genetic data generated. As
many of the papers in this volume attest, the arrival of
rats on islands has had a significant negative impact
on the native flora and fauna. Understanding not only
the timing and sources of those past rodent introduc-
tions helps us to evaluate and document the impacts
of prehistoric human presence on islands. This in turn
may also allow us to model and manage island
biodiversity more effectively today and in the future.
The ability to quickly, efficiently and reliably identify
invasive rodent species and also potentially identify
the source population could be valuable for manage-
ment and conservation agencies in the Pacific and
many other island environments.
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