Brown rat demography reveals pre-commensal structure in eastern Asia before expansion into Southeast Asia

Abstract

Fossil evidence indicates that the globally distributed brown rat (Rattus norvegicus) originated in northern China and Mongolia. Historical records report the human-mediated invasion of rats into Europe in the 1500s, followed by global spread because of European imperialist activity during the 1600s-1800s. We analyzed 14 genomes representing seven previously identified evolutionary clusters, and tested alternative demographic models to infer patterns of range expansion, divergence times, and changes in effective population (N _e) size for this globally important pest species. We observed three range expansions from the ancestral population that produced the Pacific (diverged ∼16.1 kya), eastern China (∼17.5 kya), and Southeast (SE) Asia (∼0.86 kya) lineages. Our model shows a rapid range expansion from SE Asia into the Middle East and then continued expansion into central Europe 788 yr ago (1227 AD). We observed declining N _e within all brown rat lineages from 150-1 kya, reflecting population contractions during glacial cycles. N _e increased since 1 kya in Asian and European, but not in Pacific, evolutionary clusters. Our results support the hypothesis that northern Asia was the ancestral range for brown rats. We suggest that southward human migration across China between the 800s-1550s AD resulted in the introduction of rats to SE Asia, from which they rapidly expanded via existing maritime trade routes. Finally, we discovered that North America was colonized separately on both the Atlantic and Pacific seaboards, by evolutionary clusters of vastly different ages and genomic diversity levels. Our results should stimulate discussions among historians and zooarcheologists regarding the relationship between humans and rats.

Figure 1.

Estimates of regional brown rat range expansions based on pairwise ψ statistics: (A) eastern Asia; (B) SE Asia and the Middle East; (C) Europe; (D) western Europe and the Expansion range; and (E) Russia, the Aleutian Archipelago, and Western North America. Lines show directionality from inferred source (pink) to sink (yellow) populations, whereas thickness was scaled to the Z-score when the absolute value was greater than five.

Figure 2.

Plot of change in effective population size (N_e) over time using MSMC2, where the x-axis is years before the present. Each evolutionary cluster was represented by a different color: eastern China, dark brown; SE Asia, light brown; Aleutian, orange; Western North America, yellow; Northern Europe, purple; Western Europe, light blue; and Expansion, medium blue.

Figure 3.

Inferred population tree topology and divergence times for the global expansion of brown rats. (A) The best-supported demographic model contained nine evolutionary clusters inclusive of two unsampled populations. The divergence times in generations and N_e are listed in Table 1. (B) Map of global sampling locations for the WGS demographic model in which evolutionary clusters were represented by different colors: Eastern China, dark brown; SE Asia, light brown; Aleutian, orange; Western North America, yellow; Middle East, gray-blue; Northern Europe, purple; Western Europe, light blue; and Expansion, medium blue.