Multiple geographic origins of commensalism and complex dispersal history of Black Rats

Abstract

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.

Figure 1. Maps showing the global distribution of sampling localities.

Locality numbers refer to entries in Tables S1 and S2.

Figure 2. Phylogenetic tree produced with Bayesian Inference using MCMC.

The tips are labelled with codes that identify a unique combination of haplotype and locality (i.e. an identical haplotype only appears more than once if it was found at different localities). The full details for each tip code appear in Table S1. This tree also shows relationships outside of the Rattus rattus Complex. Numbers on nodes are Bayesian posterior probabilities.

Figure 3. Divergence time estimates for key diversification events in the Rattini and the Rattus rattus Complex.

Result of BEAST analysis using an uncorrelated lognormal relaxed-clock model and with HKY+I+G6 nucleotide substitution model on data partitioned by the three codon positions. MCMC analyses were run for 30,000,000 steps, with posterior samples drawn every 1000 steps after a burn-in of 3,000,000 steps. The general constant size coalescent model was used as tree prior. Divergence time estimates for labelled nodes A–E are shown in Table S3, References S1.

Figure 4. Geographic distribution and inferred dispersal episodes of the six lineages of the RrC.

(A). Global distribution of lineages I and II, showing inferred direction of movement of lineage I rats into the Middle East and from there, independently to Madagascar and Europe (and thence globally, as ship-borne emigrants). Note that lineage II is represented in South Africa and western USA. (B) Semi-schematic diagram showing the inferred natural ranges of each of lineages I–VI of the RrC, including the inferred ‘Sundaic’ sublineages of Lineage IV (hatched), which is fully congruent with the range of Lineage VI. Points of particular interest include: 1) extensive range overlap between lineages II and V (R. sakeratensis) in Thailand and central to southern Laos; 2) extensive range overlap between Lineages IV and VI (R. tiomanicus) on the Sundaic islands; 3) abutting or narrowly overlapping ranges of Lineages II and IV in central to southern Laos and Thailand; and 4) lack of evidence for natural range overlap among Lineages I–III prior to the onset of widespread habitat disruption and human-mediated dispersal. It is not clear whether the natural range of Lineage II included Taiwan or whether the natural range of lineage I included Sri Lanka. (C). Distribution in Asia of lineages I,II and IV showing inferred directions of prehistoric movement for each of lineage. Regional movement of Lineages II and IV has resulted in a broad zone of geographic overlap that includes Indonesia and the Philippines.

Figure 5. Population genetic analyses of lineage I of the RrC.

A) Median Joining Networks. On the left network, the observed haplotypes are identified by country of origin (country codes are: AU: Australia; BR: Brazil: FR: France; GU: Guinea; GY: Guyana; IN: India; IR: Iran; JA: Japan; MA: Madagascar; NZ: New Zealand; OM: Oman; PA: Papua New Guinea; SA: Samoa; SE: Senegal; SI: Society Islands; SO: South Africa; US: United States of America; VE: Venezuela); on the right network they are identified by haplotype number as listed in Table S2. In both networks, multiple codes or numbers within a single node signify an identical haplotype coming from more than one country or locality within a country. Haplotypes marked with an asterisk are short sequences and their position on the network was inferred from a separate network analysis that produced an otherwise identical topology; B) Pairwise mismatch analyses. Separate analyses were carried out for specimens derived from the inferred natural range of Lineage I on the Indian subcontinent (a–b) and for specimens belonging to the European Black Rat population and its global ‘ship rat’ derivatives (c–d). For each population, the mismatch distribution is compared with curves derived from coalescent simulations under contrasting models of stable (a,c) or fluctuating (b,d) populations.

Figure 6. Population genetic analyses of lineage II of the RrC.

A) Median Joining Network constructed as for Fig. 5. In the left network the observed haplotypes are identified by country of origin Country (codes as follows: BA: Bangladesh; CH: mainland China; CH_H: Hong Kong; ID_B: Indonesia (Bali Island) ; ID_J: Indonesia (Java Island); JA: Japan; JA_R: Japan (Ryukyu Archipelago); LA: Laos; MY: Myanmar; PA: Papua New Guinea; PH: Philippines; SO: South Africa; TA: Taiwan; TA_L: Taiwan [Lanyu, Orchid Island]); TH: Thailand; US: United States of America; VE: Venezuela; VN_N: Vietnam (northern); in the right network they are identified by haplotype number as listed in Table S1. In both cases, multiple codes or numbers within a single node signifies an identical haplotype coming from more than one country or locality within a country. Haplotypes marked with an asterisk are short sequences and their position on the network was inferred from a separate TCS analysis that produced an otherwise identical topology. B) Pairwise mismatch analyses, calculated as for Fig. 5. Separate analyses were carried out for specimens derived from the inferred natural range of lineage II on the Indochinese mainland (a–b) and for specimens belonging to each of sub-lineages IIA (c–d) and IIB (e–f) that derive mainly from areas of the western Pacific where archaeological evidence independently documents recent prehistoric introductions. For each population, the mismatch distribution is compared with curves derived from coalescent simulations under contrasting models of stable (a) or fluctuating (b) populations.

Figure 7. Population genetic analyses of lineage IV of the RrC.

A) Median Joining Network, constructed as for Fig. 5. In the left network the observed haplotypes are identified by country of origin [Country codes CA: Cambodia; ID_F: Indonesia (Flores Island); ID_L: Indonesia (Lombok Island); ID_J: Indonesia (Java); ID_S: Indonesia (Sulawesi); ID_W: Indonesia (Sumbawa Island); LA: Laos; PH: Philippines; SL: Sri Lanka; VN_S: Vietnam (southern)]; in the right network they are identified by haplotype number as listed in Table S1. In both cases, multiple codes or numbers within a single node signifies an identical haplotype coming from more than one country or locality within a country. Haplotypes marked with an asterisk are short sequences and their position on the network was inferred from a separate TCS analysis that produced an otherwise identical topology. B) Pairwise mismatch analyses for mainland Indochinese samples of Lineage IV, calculated as for Fig. 5. The inferred Sundaic sublineages are excluded from this analysis because the majority derive from islands where archaeological evidence independently documents recent prehistoric introductions. The mismatch distribution is compared with curves derived from coalescent simulations under contrasting models of stable (a) or fluctuating (b) populations.