Multiple Geographic Origins of Commensalism and Complex Dispersal History of Black Rats

et al. (2011) Multiple Geographic Origins of Commensalism and Complex Dispersal History of Black Rats. PLoS ONE 6(11): e26357. doi:10.1371/journal.pone.0026357 Multiple Geographic Origins of Commensalism and Complex Dispersal History of Black Rats Ken P. Aplin Hitoshi Suzuki Alejandro A. Chinen R. Terry Chesser Jose ten Have Stephen C. Donnellan Jeremy Austin Angela Frost Jean Paul Gonzalez Vincent Herbreteau Francois Catzeflis Julien Soubrier Yin-Ping Fang Judith Robins Elizabeth Matisoo-Smith Amanda D. S. Bastos Ibnu Maryanto Martua H. Sinaga Christiane Denys Ronald A. Van Den Bussche Chris Conroy Kevin Rowe Alan Cooper M. Thomas P. Gilbert, Natural History Museum of Denmark, Denmark The Black Rat (Rattus rattus) spread out of Asia to become one of the world's worst agricultural and urban pests, and a reservoir or vector of numerous zoonotic diseases, including the devastating plague. Despite the global scale and inestimable cost of their impacts on both human livelihoods and natural ecosystems, little is known of the global genetic diversity of Black Rats, the timing and directions of their historical dispersals, and the risks associated with contemporary movements. We surveyed mitochondrial DNA of Black Rats collected across their global range as a first step towards obtaining an historical genetic perspective on this socioeconomically important group of rodents. We found a strong phylogeographic pattern with well-differentiated lineages of Black Rats native to South Asia, the Himalayan region, southern Indochina, and northern Indochina to East Asia, and a diversification that probably commenced in the early Middle Pleistocene. We also identified two other currently recognised species of Rattus as potential derivatives of a paraphyletic R. rattus. Three of the four phylogenetic lineage units within R. rattus show clear genetic signatures of major population expansion in prehistoric times, and the distribution of particular haplogroups mirrors archaeologically and historically documented patterns of human dispersal and trade. Commensalism clearly arose multiple times in R. rattus and in widely separated geographic regions, and this may account for apparent regionalism in their associated pathogens. Our findings represent an important step towards deeper understanding the complex and influential relationship that has developed between Black Rats and humans, and invite a thorough re-examination of host-pathogen associations among Black Rats. - Funding: Funding support that allowed KA and AF to collect samples in Myanmar, Vietnam, Laos and Cambodia was provided by Australian Centre for International Agricultural Research (ACIAR - (http://aciar.gov.au/) and AusAID (http://www.ausaid.gov.au/), funding agencies of the Australian Government. Collecting by KA in Bangladesh was supported by Department for International Development(DfID) grants through the Poverty Elimination through Rice Research Assistance and Crop Protection Programme programmes. Y-PF was supported by grants from the National Science Council (http://web1.nsc.gov.tw/) and the Council of Agriculture (http://eng.coa.gov.tw/), Republic of China. AB was supported by DFID (project number R8190) and the European Commissions INCO-DEV programme (ICA4-CT2002-10056: Ratzooman - http://www.nri.org/ratzooman). CDs collecting in Guinea was supported by the European Commissions INCO-DEV programme (project TREATCONTROL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. The Black Rat (Rattus rattus; also known as House, Roof and Ship Rat) is the most widely distributed of all commensal animals and the most destructive of all animal pests. It is a remarkably adaptable species that plays multiple roles as a household pest [1], a destructive agricultural pest in cereal and vegetable crops, orchards and palm plantations [1,2], and a feral invader of natural habitats [3,4]. Huge effort is invested in pest control and feral eradication of the species, and there is growing interest in its role in numerous zoonotic disease cycles, including the ongoing threat posed by plague (Yersinia pestis) [5] and the emerging threats posed by bunyaviruses, leptospirosis and a range of bacterial typhus syndromes in particular [6,7]. Despite its obvious socio-economic significance, the Black Rat remains poorly understood from a taxonomic and evolutionary standpoint, and it remains almost entirely unstudied as a wild mammal within its natural range. Studies of chromosomes and blood proteins during the 1960s and 70 s identified patterns of geographic variation in the species [8], and subsequent genetic [9] and morphological work [10] encouraged discrimination of two weakly differentiated species R. rattus for European and Indian populations with a karyotype of 2n = 3840 and R. tanezumi for Asian populations with a 2n = 42 karyotype [11]. However, more recent regional studies of Black Rat mitochondrial DNA (mtDNA) [1213,14] identified patterns of genetic diversity that are not easily reconciled with this taxonomic arrangement. We undertook a global survey of mitochondrial DNA (mtDNA) of this important pest animal throughout its entire range. Our findings shed new light on the evolutionary history of Black Rats, including the geographic pattern of diversification and the direction and timing of prehistoric, historic and contemporary dispersals, and suggest a novel explanation for the exceptionally diverse zoonotic disease associations of this particular group of rats. Our findings also point the way forward to resolving the taxonomy of this problematic group of mammals. We obtained mitochondrial cytochrome b (cyt b) gene sequences from 165 individuals identified on morphological criteria as Black Rats, presumably representing either R. rattus or R. tanezumi. These were derived from 76 localities in 32 countries (Fig. 1; Tables S1, S2). To test the monophyly of Black Rats and to establish their relationships with other Rattus, we obtained cyt b sequences from seven other species of Rattus and species in four other closely related genera of the Tribe Rattini (Table S1). Phylogenetic analysis The Black Rat cyt b sequences fall into four well-supported lineages (designated IIV on Fig. 2). Three of these lineages (I III) comprise an exclusive, monophyletic assemblage of Black Rats designated Clade A on Fig. 2. However, the fourth Black Rat lineage (IV) belongs to a separate clade (designated B on Fig. 2) that otherwise includes rats coming from Thailand and Laos and identified as R. losea (Lineage V) and representatives of the Sundaic species R. tiomanicus and R. baluensis, which together comprise Lineage VI. The term Rattus rattus Complex (RrC) [15] is employed here for the smallest monophyletic unit that includes all of the typical Black Rats. The mtDNA tree topology suggests that t (...truncated)