Brown rat demography reveals pre-commensal structure in eastern Asia prior to expansion into Southeast Asia during the Song dynasty

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 due to European imperialist activity during the1600s-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 (Ne) size for this globally important pest species. We observed three range expansions from the ancestral population that produced the Pacific (~4.8kya), eastern China (diverged ~0.55kya), and Southeast (SE) Asia (~0.53kya) lineages. Our model shows a rapid range expansion from SE Asia into the Middle East then continued expansion into central Europe 537 years ago (1478 AD). We observed declining Ne within all brown rat lineages from 150-1kya, reflecting population contractions during glacial cycles. Ne increased since 1kya in Asian and European, but not 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 800-1550s 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, yet 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.