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Proc Biol Sci. Jan 22, 2009; 276(1655): 209–217.
Published online Sep 30, 2008. doi:  10.1098/rspb.2008.0959
PMCID: PMC2674344

The diverse origins of New Zealand house mice

Abstract

Molecular markers and morphological characters can help infer the colonization history of organisms. A combination of mitochondrial (mt) d-loop DNA sequences, nuclear DNA data, external measurements and skull characteristics shows that house mice (Mus musculus) in New Zealand and its outlying islands are descended from very diverse sources. The predominant genome is Mus musculus domesticus (from western Europe), but Mus musculus musculus (from central Europe) and Mus musculus castaneus (from southern Asia) are also represented genetically. These subspecies have hybridized to produce combinations of musculus and domesticus nuclear DNA coupled with domesticus mtDNA, and castaneus or musculus mtDNA with domesticus nuclear DNA. The majority of the mice with domesticus mtDNA that we sampled had d-loop sequences identical to two haplotypes common in Britain. This is consistent with long-term British–New Zealand cultural linkages. The origins of the castaneus mtDNA sequences widespread in New Zealand are less easy to identify.

Keywords: d-loop, hybridization, mitochondrial DNA, morphology, Mus musculus, phylogeography

1. Introduction

The house mouse (Mus musculus L.) originated in the north of the Indian subcontinent ca 0.5 Myr ago (Boursot et al. 1993), expanded its natural range into the Middle East, and diversified into three major subspecies: castaneus; domesticus; and musculus (Din et al. 1996), all intimate commensals. Thereafter, house mice were transported by people wherever they went (Pocock et al. 2005). They spread throughout Eurasia, starting in the Neolithic with the development of agriculture and permanent human settlements (Cucchi et al. 2005). Mus musculus domesticus colonized the Mediterranean basin and western Europe, musculus central and eastern Europe and northern Asia, and castaneus southern Asia; stable hybrid zones were formed where the subspecies came into contact (Boursot et al. 1993).

Since the earliest days of ocean-going navigation, commensal house mice have been carried on ships well beyond this Eurasian range. Mus musculus domesticus colonized north and south America, South Africa, Australia and Atlantic archipelagos such as Faroe and Madeira (Berry & Peters 1977; Boursot et al. 1993; Gündüz et al. 2001). Mus musculus musculus and Mus musculus castaneus reached several islands in the north Pacific such as Japan and the Hawaiian Islands (Wheeler & Selander 1972; Moriwaki et al. 1986).

The global colonization history of the house mouse has been complex, and much about it remains unknown. Here, we provide the first detailed investigation of mice on the archipelago the most distant from Eurasian source areas: New Zealand and its outlying islands in the south west Pacific.

The earliest humans to settle in New Zealand, in ca AD 1280 (Wilmshurst et al. 2008), were Polynesians migrating from islands which were, at that time, apparently mouse free (Worthy & Holdaway 1996; Steadman 2006). The origins of house mice in New Zealand are therefore generally assumed to be associated with the voyages of early European explorers and traders, facilitated by James Cook's first coastal chart of 1769–1770.

We have applied a genetic approach (Searle 2008) to study the colonization of New Zealand by house mice, using mitochondrial (mt) DNA sequences, nuclear molecular markers and morphology (external measurements, skull features and pelage coloration). The genetic diversity is striking: genetic contributions of all three subspecies of house mouse are present in New Zealand, deriving from different parts of Europe and from Asia. These subspecies have hybridized to create a genetic melting pot that illustrates graphically how easily humans can unwittingly transport and bring together highly divergent genetic forms of single species.

2. Material and methods

(a) Sample collection

We examined a total of 755 mice, representing 22 field localities in New Zealand (figure 1). Sub-samples were used for analyses of coat colour, external measurements, skull characters and molecular traits, as listed in appendices 1–3 in the electronic supplementary material.

Figure 1
Map showing house mouse collection localities in New Zealand and its outlying islands. The populations or groups of populations sampled for molecular analysis are labelled 1–17 (open circles on New Zealand; precise locations unknown on the outlying ...

(b) Molecular methods and analysis

Specimens for molecular analysis were stored frozen (−80°C) or in absolute ethanol. Genomic DNA was extracted by phenol : chloroform or with commercial extraction kits. Subspecies were distinguished from mtDNA and nuclear sequences, and mtDNA sequences were used to infer more specific source areas of the colonists.

The complete mt d-loop and flanking regions were amplified with the PCR primers and conditions as described in Gündüz et al. (2000) or with the primer pairs L15320/H15782 and L15735/H00072 of Prager et al. (1993). The fragments generated were sequenced in both directions using the same primers.

Sequences were aligned and edited using Sequencher v. 4.8 (Gene Codes Corp.). For all specimens we obtained sequences for the mtDNA region between positions 15363 and 16295 (933 bp) of Bibb et al. (1981). These were then truncated to a standard length of 853 bp, between positions 15424 and 16276, so that we could analyse our data together with the relevant sequences already in GenBank. Our sequences have also been deposited there (FM211632-FM211645). Both the new and previous sequences were readily classified according to subspecies M. m. domesticus, M. m. musculus and M. m. castaneus (e.g. Prager et al. 1996; Ihle et al. 2006).

The phylogenetic analysis of M. m. domesticus is the same as that reported in the companion paper (Searle et al. 2009) that provides the detailed results. The analysis involved all domesticus sequences from New Zealand together with all published sequences of the same subspecies. GenBank sequences M. m. gentilulus AF074545, AF074544; M. m. castaneus EF108342, AF088879, AJ286322 and M. m. musculus U47504, U47532 were used as outgroups, following Rajabi-Maham et al. (2008; M. m. gentilulus is a tentative Arabian subspecies described by Prager et al. 1998). We also followed Rajabi-Maham et al. (2008) in carrying out a Bayesian analysis, generating a 50 per cent majority-rule consensus phylogenetic tree with MrBayes (Huelsenbeck & Ronquist 2001) based on a GTR+I+Γ substitution model (selected by Modeltest v. 3.7: Posada & Crandall 1998) and with the following conditions: 30 per cent burn-in, 5 million generations, two runs of five chains and temperature of 0.2.

The phylogenetic analysis of M. m. musculus and M. m. castaneus comprised the relevant New Zealand sequences together with all other musculus and castaneus sequences available in the literature (with domesticus AJ286321 as outgroup). The Bayesian analysis involved the same substitution model and run conditions as for the domesticus tree. Previous d-loop phylogenies with these subspecies have used the neighbour-joining (NJ) and maximum-parsimony (MP) methods (Prager et al. 1996; Gündüz et al. 2000) and we adopted those approaches here as well. The NJ tree was also based on the substitution model selected by Modeltest with bootstrap values from 10 000 replicates. The MP analysis was conducted by heuristic search using the TBR swapping algorithm with 10 random repetitions. A 50 per cent majority-rule consensus tree was constructed with bootstrap values from 1000 replicates using 10 random repetitions for each replicate.

Nucleotide (π) and haplotype (h) diversities for the d-loop sequences were calculated according to Nei (1987) using MEGA v. 4 (Tamura et al. 2007) and Arlequin v. 3.0 (Excoffier et al. 2005), respectively.

Four nuclear molecular markers with fixed differences between M. m. domesticus and M. m. musculus were typed for 56 mice (Abpa, Btk, D11 cenB2 and Zfy2). Mus musculus castaneus acts either as domesticus (D11 cenB2) or as musculus (Abpa, Btk, Zfy2). Controls of known domesticus (from England), musculus (Czech Republic) and castaneus (Thailand) were used to check all markers identified in New Zealand material. The Abpa marker is a sequence within the androgen-binding protein alpha subunit, 10 cM from the centromere of chromosome 7, scored as in Dod et al. (2005). The Btk marker is defined as the presence or absence of the B1 insertion between positions 77329–77464 in the Bruton's agammaglobulinemia tyrosine kinase gene on the X chromosome, scored as in Munclinger et al. (2002). D11 cenB2 is a marker at the centromeric region of chromosome 11, typed according to the method of Lanneluc et al. (2004), but the reaction to detect musculus requires a higher annealing temperature of 64°C. The Zfy2 marker is defined as the presence or absence of an 18 bp deletion in the last exon of the Zinc finger protein 2 on the Y chromosome, scored on males (n=25) according to the protocol of Orth et al. (1996).

(c) Morphological analysis

Freshly collected mice of all ages were scored for dorsal and ventral coat colour using Munsell standard soil colour charts. Only fully grown adults of Lidicker's tooth wear classes 4 and above (illustrated in Ruscoe & Murphy 2005) were used to score other characteristics. Tail length was determined by the hanging tail method (Jewell & Fullagar 1966) and head and body length by subtraction from total length. Relative tail length was expressed as tail : body length ratio (TBLR). Skulls were scored for general skull shape, shape of the zygomatic plate, shape of the suture between the squamosal and parietal bones, and shape of the first lower molar, four features that distinguish M. m. domesticus from M. m. musculus in Europe (Marshall & Sage 1981; Kraft 1985). Skull morphology of M. m. castaneus is less well known, so was not separately classified.

3. Results

(a) MtDNA analysis

MtDNA haplotypes of all three subspecies of house mouse were found on the New Zealand mainland and its outlying islands (appendices 1 and 2 in the electronic supplementary material). At 11 of 17 localities sampled for our molecular analysis (figure 1), we obtained only domesticus sequences; at one, both musculus and castaneus sequences, and at five, only castaneus sequences. Altogether, 10 domesticus haplotypes were found in 82 mice, one musculus haplotype in two mice, and three castaneus haplotypes in 22 mice.

The New Zealand domesticus haplotypes were distributed in five places in the phylogenetic tree (figure 2a). Haplotypes domNZ.1–5 fit within a well-supported lineage (posterior probability of 0.96) best documented in Britain and Germany (Searle et al. 2009). Of the 55 mainland New Zealand house mice with domesticus mtDNA included in this study, 47 belonged to this lineage, as did the 16 specimens from Auckland Island and Macquarie Island (figure 1). Haplotype domNZ.4 that is identical to one of the common haplotypes found in Britain and Germany (BritIsl.5; Searle et al. 2009), was particularly numerous (45 mice) and widely distributed in New Zealand. Likewise, domNZ.1 is identical to a common Anglo-German haplotype (BritIsl.1; Searle et al. 2009) and is frequent (15 mice) and widespread in New Zealand (North and South Islands and outlying islands). Haplotype domNZ.3 (found in one location in New Zealand) is identical to U47432 (found in one location in Germany) and both become identical to a British haplotype (U47434 found in one location) when truncated for phylogenetic analysis.

Figure 2
Phylogenetic trees for (a) M. m. domesticus and (b) M. m. castaneus and M. m. musculus, after Bayesian analysis (see text). Trees show all house mouse haplotypes found in New Zealand together with all available haplotypes from GenBank. All posterior probabilities ...

Haplotypes domNZ.6–10 are distributed elsewhere in the tree (figure 2a). The haplotypes domNZ.9 and 10 found at Ruatangata and Ashburton are part of the ‘Orkney’ lineage that consists predominantly of house mice from Ireland and the extreme north of Britain, although domNZ.9 is actually identical to a sequence previously found in a mouse from Croatia (see Searle et al. 2009). One haplotype on North Island (domNZ.6, represented by two individuals from Taranaki) has an affiliation with continental Europe (northern Italy, Germany); domNZ.8 from Antipodes Island has the closest affinity with a haplotype from Spain; and domNZ.7 from Pitt Island is basal within the tree.

Considering all New Zealand specimens with domesticus mtDNA, the haplotype diversity (h±s.d.) is 0.66±0.05 and the nucleotide diversity (π±s.d.) is 0.0042±0.0010.

Figure 2b shows the phylogenetic tree for musculus and castaneus (a more detailed version is available in appendix 4 in the electronic supplementary material). The single musculus haplotype found in Wellington (figure 1) was identical to sequences previously described from central Europe (southern Germany, Austria and Croatia) and in the same weakly supported lineage (posterior probability of 0.74) as others from the same geographical region. This lineage was also identified with NJ and MP analyses with less than 50 per cent bootstrap support.

Mus musculus castaneus mtDNA haplotypes were found in southern parts of both North and South Islands (casNZ.1 and 3) and on Chatham Island (casNZ.2). The three New Zealand castaneus haplotypes all belong to the same well-supported lineage (posterior probability of 0.98), also present with high bootstrap support, 91 per cent and 92 per cent, in the NJ and MP trees, respectively. The two other sequences in this lineage were derived from Pakistan and Thailand.

(b) Analysis of nuclear molecular markers

Fifty-five out of 77 mice from all 12 mainland New Zealand localities used for mtDNA analysis (figure 1) were also typed for nuclear molecular markers (appendix 1 in the electronic supplementary material). The vast majority of mice could be scored as domesticus with these markers. This group includes the male mouse from Wellington with musculus mtDNA for which all four nuclear markers could be scored as domesticus, and 17 individuals with castaneus mtDNA (five from Wellington and three each from Dunedin, Borland, Grebe and southern Fiordland) for which three or four nuclear markers could be scored as domesticus, depending on whether the individuals were females (seven mice, three markers) or males (10 mice, usually four and sometimes three markers).

Only mice from Nelson Lakes National Park in northern South Island showed any definite nuclear genetic input from musculus and/or castaneus. Four came from Lake Rotoiti and two from Mount Misery, 20 km away (the two Nelson Lakes populations in figure 1). One male from Rotoiti had a castaneus- or musculus-specific Zfy2 product for the Y chromosome, but could be scored as domesticus for the X-chromosome marker and two autosomal markers. Four of the five females also had hybrid genomes. One from Rotoiti was heterozygous at the D11 cenB2 locus, having a musculus type allele and a domesticus/castaneus allele; two (one from each locality) were heterozygotes for a castaneus or musculus allele and a domesticus allele at the Btk locus on the X chromosome; and one from Mount Misery was homozygous for a castaneus or musculus allele at the Btk locus. At other markers these four females could be scored as domesticus, and one female from Rotoiti could be scored as domesticus at all loci.

(c) Morphological analysis

Pelage coloration was scored in a total of 277 fresh house mice from mainland New Zealand (appendix 3 in the electronic supplementary material). Dorsally, almost all were brown (32%) or dark brown (64%) with a few grey. Ventral colour ranged from white through grey to brown, most commonly pale brown (59%). The most frequent combination was a dark brown back and a pale brown belly (56%). Both this form and the variation around it are observed among domesticus from western Europe (Sage 1981). Mus musculus musculus more typically has a whitish belly (Boursot et al. 1993). Mus musculus castaneus tends to have an ochraceous tint (Marshall & Sage 1981), but that was not observed in any New Zealand mice. However, coloration is variable in all three subspecies and this character is not diagnostic.

More reliable as a discriminator between subspecies is relative tail length (musculus tends to have a smaller TBLR than the other two subspecies; Marshall & Sage 1981; Boursot et al. 1993). The New Zealand TBLR mean was 0.991 (range 0.67–1.30), compared with 0.872 (0.74–0.91) for musculus and 1.014 (0.87–1.20) for domesticus from continental Europe (Kraft 1985). The difference between the mean New Zealand and European values was significant for musculus (t163=−5.033, p<0.001) but not for domesticus (t166=1.888, p=0.061). There was significant local variation in TBLR values between the eight largest samples from New Zealand (figure 3; p<0.001, one-way ANOVA); all of them were significantly different in TBLR from European musculus, but none from domesticus.

Figure 3
Morphological characters of New Zealand house mice as illustrated with data from eight large samples (see figure 1 and appendix 1 in the electronic supplementary data). TBLR, tail : body length ratio. Skull scores 0–4 defined from ...

Each of the four features discriminating domesticus from musculus was scored in 549 skulls of New Zealand mice, as listed in appendix 1 in the electronic supplementary material. The distribution of these scores for the eight largest samples, plotted against TBLR in figure 3, was strongly skewed towards the reference values for domesticus (TBLR=1.014, skull score 0) as opposed to those for musculus (TBLR=0.872, skull score 4); the mean skull score was 0.661. However, the plots reveal deviation away from the domesticus morphology in samples from throughout the country, including places such as Pureora and Mana Island for which no genetic data are yet available.

4. Discussion

(a) Taxonomy of New Zealand house mice and evidence of hybridization

Our morphological and molecular data suggest that the house mice of New Zealand should be classified as the western European subspecies M. m. domesticus (see also Ruscoe & Murphy 2005). Most of the individuals examined were typed as domesticus on all criteria scored. However, there was also definitive evidence of the genetic presence of the other two subspecies as follows:

  1. we found mt d-loop sequences characteristic of south Asian M. m. castaneus on both North and South Islands and on one outlying island (Chatham) and
  2. we found mt d-loop sequences identical to central European M. m. musculus in one locality on North Island (Wellington).

Furthermore, based on the evidence from three out of four nuclear markers, non-domesticus genes were also present in most individuals at two separate locations in Nelson Lakes National Park on South Island and one of these mice carried a definitive musculus allele. Data on relative tail length were also consistent with a low level but probably widespread presence of elements of the musculus nuclear genome on both North and South Islands (figure 3). Generally the skulls of New Zealand mice were similar to European domesticus, but features characteristic of musculus were found at low frequency in many localities.

Considering the house mice collected on mainland New Zealand, it is important to emphasize that whenever there was either a musculus or castaneus element to the genome, there was also a domesticus element. Mainland New Zealand was dominated by domesticus; genomic contributions of the other subspecies were present only in hybrids.

Our results demonstrate that New Zealand is a genetic melting pot for house mice at the subspecies level. But the same is also true for the divergent lineages within the domesticus subspecies. Across the archipelago, we found four different domesticus mtDNA lineages plus a single basal haplotype (figure 2a), and at three localities (Ruatangata, Taranaki and Ashburton) two different domesticus lineages were present (figure 1). Hence, the nucleotide diversity (π) for domesticus mtDNA for our New Zealand material was relatively high at 0.0042. By contrast, the haplotype diversity (h) was relatively low at 0.66, largely because haplotype domNZ.4 was so abundant. The equivalent values for the Madeiran archipelago were π=0.0014 and h=0.90 (Gündüz et al. 2001). Continental domesticus populations tend to have higher values for both haplotype and nucleotide diversity. For example, Gündüz et al. (2005) estimated π=0.0084 and h=0.98 from 98 mice representing 48 localities in Turkey (see also Rajabi-Maham et al. 2008).

The interplay of divergent genomes within populations and individuals is of great theoretical interest (Arnold 2006). The house mouse in New Zealand offers particular opportunities for analysis, given the presence of genes of three different subspecies, multiple genealogical lineages within one of those subspecies, and the huge data resources available for genome studies of house mice (Mouse Genome Sequencing Consortium 2002). So, the house mouse in New Zealand is a potentially valuable model for future work on the fundamentals of genome interaction to contrast, for example, with mice from Japan, which show mixed musculus/castaneus genomes (Terashima et al. 2006).

(b) Colonization history of New Zealand house mice

Any account of the colonization history of house mice in New Zealand needs to explain (i) the dominance of M. m. domesticus belonging to mtDNA haplotypes with affinities to house mice from the British Isles (domNZ.1–5, 9–10), (ii) the presence of M. m. musculus based on morphology, nuclear markers and mtDNA (musNZ.1), the latter indicating central European affiliations, and (iii) the presence of M. m. castaneus mtDNA (casNZ.1–3) with a southern Asian affinity. Ships infested with mice have arrived throughout the 240-year European maritime history of New Zealand, so the following scenario needs to be viewed in that context.

In 1769, James Cook was the first of several European explorers to land in New Zealand; his expedition was followed by others from Britain, France and Spain (King 2003). The exploitation of the resources of New Zealand by European traders based at Sydney (then called Port Jackson, established 1788) began very early. The British East India Company was making use of New Zealand timber and flax by 1790 (King 2003), and sealers and whalers of different nationalities started working in New Zealand waters well before 1800 (Ross 1987; Smith 2002). Long before the beginning of organized colonization in 1840, New Zealand was already part of an extensive trading network also including ports in Europe, southern Asia and Australia (Ross 1987).

From the earliest days of European contact (Thomson 1922; King 2003), house mice began to exploit human settlements in New Zealand, as they do throughout the world (Boursot et al. 1993). In addition, the absence of close competitors (Cucchi et al. 2005) allowed house mice to live as non-commensals, and they are now found in natural habitat throughout New Zealand (Ruscoe & Murphy 2005). Shipwrecks and strandings in unpeopled areas were common (2300 shipwrecks along the New Zealand coast recorded since 1795: Ingram 2007), and provided additional opportunities for mice to reach remote areas. Indeed, the first record of house mice in New Zealand was on Ruapuke Island (figure 1) after the 1824 stranding and subsequent salvage of the Elizabeth Henrietta, an Australian brig bringing ‘British manufactures’ from Sydney to the Maori in exchange for flax (McNab 1908, p. 648). Mice were present at the port of Russell in the Bay of Islands (figure 1) in or before the 1830s (Guthrie-Smith 1969).

Most ships arriving in New Zealand during the early mid-nineteenth century came from Britain, and they usually called at Cape Town, Sydney and other Australian ports on the way (Jamieson 2001). The influx of settlers and their companion animals increased rapidly: 500 000 had arrived by 1881 (King 2003). In the first 50 years, 49 per cent of immigrants were from England and Wales, 24 per cent from Scotland, 19 per cent from Ireland, and the rest from Germany, Scandinavia, Poland, France and Italy (King 2003). The immigrant ships, their cargo, provisions and livestock and the subsequent close mutual trading links between Europe, Australia and New Zealand, provided decades of multiple opportunities for colonization by European mice resident in ports of origin and transit.

Asian mice could have reached New Zealand by one or all of at least three different routes: (i) between 1792 and 1820, indirectly with Sydney-based sealers and traders returning from the Canton fur market (Ross 1987; Smith 2002), (ii) after 1869, directly with Chinese gold miners from Canton (King 2003), or (iii) since the 1960s, on Asian fishing vessels after the restrictions on their use of New Zealand's ports have been lifted (Johnson 2004). Since 1985, ship rats (Rattus rattus) of the Asian karyotype have occasionally reached New Zealand with the Asian fleet (Innes 2005), and, presumably, so could Asian mice.

Given this history, we suggest the following scenario explaining the derivation of the contemporary house mice of New Zealand from different subspecies and source areas.

  1. Mus musculus domesticus from the British Isles. New Zealand was explored, exploited and settled very largely by people from the British Isles, directly or via Australia, so the predominant presence of house mice with a domesticus morphology and genome, and the widespread presence of seven mtDNA haplotypes (domNZ.1–5, 9 and 10) belonging to lineages found in the British Isles, are both consistent with documentary history. The fact that two of the most common and widespread haplotypes in New Zealand (domNZ.1 and 4) are the same as two of the most common and widespread haplotypes in Britain (BritIsl.1 and 5, respectively) makes the case even stronger. Not only do these haplotypes occur on North and South Islands, they are also found on Auckland and Macquarie Islands. Between 1770 and 1840, domNZ.1 and 4 and other haplotypes with close links to the British Isles had multiple opportunities to spread from Sydney, both to pre-colonial New Zealand and to Auckland Island, discovered in 1806, and Macquarie Island, discovered in 1810 (Clark & Dingwall 1985). Among the other haplotypes to arrive in New Zealand was domNZ.9. Although this haplotype is within the Orkney lineage, it has actually been recorded in Croatia rather than the British Isles and further studies are needed to establish the basis of this intriguing result.
  2. Mus musculus musculus from central Europe. The single musculus d-loop sequence from Wellington, identical to one recorded from Germany, Austria and Croatia, suggests a central European source. Wellington was one of the earliest settler ports (4000 immigrants by 1843: King 2003), and now, as New Zealand's capital city, hosts many resident members of the international diplomatic corps, providing ample opportunity for arrival of house mice of central European derivation. The occurrence of a musculus nuclear marker within Nelson Lakes National Park is also consistent with known history: the largest of the minority settler groups, the Germans, gathered in the Nelson district (King 2003).
  3. Mus musculus castaneus. The source area for the S Asian castaneus mtDNA haplotypes found in the southern parts of both South and North Islands (casNZ.1, 3) is ill defined, and offers no clues to their origin. Clearly, a more detailed phylogeny for castaneus would be desirable to make progress on this point. The mice of Chatham Island also have castaneus d-loop sequences, though a different haplotype (casNZ.2) from those recorded on the mainland. The ancestors of the Chatham Island mice could have got ashore in cargo from the 1853 wreck of the Randolph, an English barque trading from China to the Chathams via Melbourne (Ingram 2007). Additional colonizations might have come, either previously from the mainland (800 km west), or more recently via the numerous Asian fishing boats that now visit Waitangi, the main port on Chatham Island. It is notable that mice from nearby Pitt Island are characterized by a domesticus mtDNA haplotype (figure 1). This most likely reflects a differing colonization history but in this and other cases the possible involvement of lineage sorting (Avise 2000) cannot be discounted.

The scenario that we have developed is tentative, and cannot at this stage allow for the many unknown factors that complicate interpretation of the colonization history of New Zealand house mice, such as the influence of transit ports (e.g. in Australia) and transport within New Zealand itself. More information is needed both to test the interpretations that we suggest for the mainland and to attempt adequately to explain the distribution of mtDNA haplotypes on the outlying islands. However, mice are exceptionally pervasive commensals, so it is certain that the New Zealand archipelago has been ‘moused’ from all over the world, in the same way as it has been ‘peopled’.

Acknowledgments

We are extremely grateful to Kath Walker, Graeme Taylor and Alex McKillop for collecting mice from the offshore islands, to Tasmania Parks and Wildlife Service (Keith Springer) for the Macquarie Island specimens and to Pavel Munclinger for his advice and preliminary typing with nuclear markers. We also thank Alec Zwart for statistical help, Rhys Richards for advice on maritime history, Jaroslav Piálek and François Catzeflis for provision of samples of known subspecies, Fríða Jóhannesdóttir for drawing the trees and commenting on the manuscript, and Max Oulton for drawing the map. Funding was provided by the Universities of Waikato and York, and the Scientific and Technological Research Council of Turkey (TÜBİTAK). Part of this work was carried out using the resources of the Computational Biology Service Unit from Cornell University which is partially funded by Microsoft Corporation.

Supplementary Material

Appendices 1–4:

Figures and tables supporting paper

References

  • Arnold M.L. Oxford University Press; Oxford, UK: 2006. Evolution through genetic exchange.
  • Avise J.C. Harvard University Press; Cambridge, MA: 2000. Phylogeography: the history and formation of species.
  • Berry R.J., Peters J. Heterogeneous heterozygosities in Mus musculus populations. Proc. R. Soc. B. 1977;197:485–503. doi:10.1098/rspb.1977.0082 [PubMed]
  • Bibb M.J., Van Etten R.A., Wright C.T., Walberg M.W., Clayton D.A. Sequence and gene organization of mouse mitochondrial DNA. Cell. 1981;26:167–180. doi:10.1016/0092-8674(81)90300-7 [PubMed]
  • Boursot P., Auffray J.-C., Britton-Davidian J., Bonhomme F. The evolution of house mice. Annu. Rev. Ecol. Syst. 1993;24:119–152. doi:10.1146/annurev.es.24.110193.001003
  • Clark M.R., Dingwall P.R. Department of Lands and Survey, for IUCN; Wellington, New Zealand: 1985. Conservation of islands in the Southern Ocean: a review of the protected areas of Insulantarctica.
  • Cucchi T., Vigne J.-D., Auffray J.-C. First occurrence of the house mouse (Mus musculus domesticus Schwarz and Schwarz, 1943) in the western Mediterranean: a zooarchaeological revision of subfossil house mouse occurrences. Biol. J. Linn. Soc. 2005;84:429–445. doi:10.1111/j.1095-8312.2005.00445.x
  • Din W., et al. Origin and radiation of the house mouse: clues from nuclear genes. J. Evol. Biol. 1996;9:519–539. doi:10.1046/j.1420-9101.1996.9050519.x
  • Dod B., Smadja C., Karn R.C., Boursot P. Testing for selection on the androgen-binding protein in the Danish mouse hybrid zone. Biol. J. Linn. Soc. 2005;84:447–459. doi:10.1111/j.1095-8312.2005.00446.x
  • Excoffier L., Laval G., Schneider S. Arlequin 3.0 an integrated software package for population genetics data analysis. Evol. Bioinform. Online. 2005;1:47–50. [PMC free article] [PubMed]
  • Gündüz, İ., Tez, C., Malikov, V., Vaziri, A., Polyakov, A. V. & Searle, J. B. 2000 Mitochondrial DNA and chromosomal studies of wild mice (Mus) from Turkey and Iran. Heredity84, 458–467. (doi:10.1046/j.1365-2540.2000.00694.x) [PubMed]
  • Gündüz, İ., Auffray, J.-C., Britton-Davidian, J., Catalan, J., Ganem, G., Ramalhinho, M. G., Mathias, M. L. & Searle, J. B. 2001 Molecular studies on the colonization of the Madeiran archipelago by house mice. Mol. Ecol 10, 2023–2029. (doi:10.1046/j.0962-1083.2001.01346.x) [PubMed]
  • Gündüz İ, Rambau R.V., Tez C., Searle J.B. Mitochondrial DNA variation in the western house mouse (Mus musculus domesticus) close to its site of origin: studies in Turkey. Biol. J. Linn. Soc. 2005;84:473–485. doi:10.1111/j.1095-8312.2005.00448.x
  • Guthrie-Smith H. A. H. and A. W. Reed; Wellington, New Zealand: 1969. Tutira: the story of a New Zealand sheep station.
  • Huelsenbeck J.P., Ronquist F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. doi:10.1093/bioinformatics/17.8.754 [PubMed]
  • Ihle S., Ravaoarimanana I., Thomas M., Tautz D. An analysis of signatures of selective sweeps in natural populations of the house mouse. Mol. Biol. Evol. 2006;23:790–797. doi:10.1093/molbev/msj096 [PubMed]
  • Ingram C.W.N. Hodder Moa; Auckland, New Zealand: 2007. New Zealand shipwrecks: over 200 years of disasters at sea.
  • Innes J.G. Ship rat. In: King C.M., editor. The handbook of New Zealand mammals. Oxford University Press; Melbourne, Australia: 2005. pp. 187–203.
  • Jamieson, P. 2001 The taxonomic identification of the New Zealand house mouse. MSc thesis, University of Waikato, Hamilton, New Zealand.
  • Jewell P.A., Fullagar P.J. Body measurements of small mammals: sources of error and anatomical changes. J. Zool. 1966;150:501–509.
  • Johnson D. Hazard Press; Christchurch, New Zealand: 2004. Hooked: the story of the New Zealand fishing industry.
  • King M. Penguin Books; Auckland, New Zealand: 2003. The Penguin history of New Zealand.
  • Kraft R. Morphological characteristics and distribution of the house mouse Mus musculus musculus L., 1758, and Mus musculus domesticus Rutty, 1772 (Rodentia, Muridae) in Bavaria. Säugetierk. Mitt. 1985;32:1–12.
  • Lanneluc I., Desmarais E., Boursot P., Dod B., Bonhomme F. Characterization of a centromeric marker on mouse chromosome 11 and its introgression in a domesticus/musculus hybrid zone. Mamm. Genome. 2004;15:924–934. doi:10.1007/s00335-004-2397-x [PubMed]
  • Marshall J.T., Sage R.D. Taxonomy of the house mouse. Symp. Zool. Soc. Lond. 1981;47:15–25.
  • McNab, R. (ed.) 1908 Historical records of New Zealand, vol. 1. Wellington, New Zealand: Government Printer.
  • Moriwaki K., Miyashita N., Suzuki H., Kurihara Y., Yonekawa H. Genetic features of major geographical isolates of Mus musculus. Curr. Top. Microbiol. Immunol. 1986;127:55–61. [PubMed]
  • Mouse Genome Sequencing Consortium. Initial sequencing and comparative analysis of the mouse genome. Nature. 2002;420:520–562. doi:10.1038/nature01262 [PubMed]
  • Munclinger P., Božíková E., Šugerková M., Piálek J., Macholán M. Genetic variation in house mice (Mus, Muridae, Rodentia) from the Czech and Slovak Republics. Folia Zool. 2002;51:81–92.
  • Nei M. Colombia University Press; New York, NY: 1987. Molecular evolutionary genetics.
  • Orth A., Lyapunova E., Kandaurov A., Boissinot S., Boursot P., Vorontsov N., Bonhomme F. L'espèce polytypique Mus musculus en Transcaucasie. C. R. Acad. Sci. III Sci. Vie. 1996;319:435–441. [PubMed]
  • Pocock M.J.O., Hauffe H.C., Searle J.B. Dispersal in house mice. Biol. J. Linn. Soc. 2005;84:565–583. doi:10.1111/j.1095-8312.2005.00455.x
  • Posada D., Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics. 1998;14:817–818. doi:10.1093/bioinformatics/14.9.817 [PubMed]
  • Prager E.M., Sage R.D., Gyllensten U., Thomas W.K., Hübner R., Jones C.S., Noble L., Searle J.B., Wilson A.C. Mitochondrial DNA sequence diversity and the colonization of Scandinavia by house mice from East Holstein. Biol. J. Linn. Soc. 1993;50:85–122. doi:10.1111/j.1095-8312.1993.tb00920.x
  • Prager E.M., Tichy H., Sage R.D. Mitochondrial DNA sequence variation in the eastern house mouse, Mus musculus: comparison with other house mice and report of a 75-bp tandem repeat. Genetics. 1996;143:427–446. [PMC free article] [PubMed]
  • Prager E.M., Orrego C., Sage R.D. Genetic variation and phylogeography of central Asian and other house mice, including a major new mitochondrial lineage in Yemen. Genetics. 1998;150:835–861. [PMC free article] [PubMed]
  • Rajabi-Maham H., Orth A., Bonhomme F. Phylogeography and postglacial expansion of Mus musculus domesticus inferred from mitochondrial DNA coalescent, from Iran to Europe. Mol. Ecol. 2008;17:627–641. doi:10.1111/j.1365-294X.2007.03601.x [PubMed]
  • Ross J.O.C. Roebuck Society; Canberra, Australia: 1987. William Stewart: sealing captain, trader and speculator.
  • Ruscoe, W. A. & Murphy, E. C. 2005 House mouse. The handbook of New Zealand mammals(ed. C. M. King), pp. 204–221, 2nd edn. Melbourne, Australia: Oxford University Press.
  • Sage, R. D. 1981 Wild mice. In The mouse in biomedical research, vol. 1 (eds H. L. Foster, J. D. Small & J. G. Fox), pp. 39–90. New York, NY: Academic Press.
  • Searle J.B. The genetics of mammalian invasions: a review. Wildlife Res. 2008;35:185–192. doi:10.1071/WR07123
  • Searle J.B., et al. Of mice and (Viking?) men: phylogeography of British and Irish house mice. Proc. R. Soc. B. 2009;276:201–207. doi:10.1098/rspb.2008.0958 [PMC free article] [PubMed]
  • Smith I.W.G. Department of Conservation; Wellington, New Zealand: 2002. The New Zealand sealing industry: history, archaeology, and heritage management.
  • Steadman D.W. University of Chicago Press; Chicago, IL: 2006. Extinction and biogeography of tropical Pacific birds.
  • Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software v. 4.0. Mol. Biol. Evol. 2007;24:1596–1599. doi:10.1093/molbev/msm092 [PubMed]
  • Terashima M., Furusawa S., Hanzawa N., Tsuchiya K., Suyanto A., Moriwaki K., Yonekawa H., Suzuki H. Phylogeographic origin of Hokkaido house mice (Mus musculus) as indicated by genetic markers with maternal, paternal and biparental inheritance. Heredity. 2006;96:128–138. doi:10.1038/sj.hdy.6800761 [PubMed]
  • Thomson G.M. Cambridge University Press; Cambridge, UK: 1922. The naturalisation of animals and plants in New Zealand.
  • Wheeler L.L., Selander R.K. Genetic variation in populations of the house mouse, Mus musculus in the Hawaiian islands. Stud. genet. VII Univ. Texas Publ. 1972;7213:269–296.
  • Wilmshurst J.M., Anderson A.J., Highham T.F.G., Worthy T.H. Dating the prehistoric dispersal of Polynesians to New Zealand using the commensal Pacific rat. Proc. Natl Acad. Sci. USA. 2008;105:7676–7680. doi:10.1073/pnas.0801507105 [PMC free article] [PubMed]
  • Worthy T.H., Holdaway R.N. Quaternary fossil faunas, overlapping taphonomies, and palaeofaunal reconstruction in North Canterbury, South Island, New Zealand. J. R. Soc. NZ. 1996;26:275–361.

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