The origin of the German cockroach, Blattella germanica, is enigmatic, in part because it is ubiquitous worldwide in human-built structures but absent from any natural habitats. The first historical records of this species are from ca. 250 years ago (ya) from central Europe (hence its name). However, recent research suggests that the center of diversity of the genus is Asian, where its closest relatives are found. To solve this paradox, we sampled genome-wide markers of 281 cockroaches from 17 countries across six continents. We confirm that B. germanica evolved from the Asian cockroach Blattella asahinai approximately 2,100 ya, probably by adapting to human settlements in India or Myanmar. Our genomic analyses reconstructed two primary global spread routes, one older, westward route to the Middle East coinciding with various Islamic dynasties (~1,200 ya), and another younger eastward route coinciding with the European colonial period (~390 ya). While Europe was not central to the early domestication and spread of the German cockroach, European advances in long-distance transportation and temperature-controlled housing were likely important for the more recent global spread, increasing chances of successful dispersal to and establishment in new regions. The global genetic structure of German cockroaches further supports our model, as it generally aligns with geopolitical boundaries, suggesting regional bridgehead populations established following the advent of international commerce.

Biology Centre of the Czech Academy of Sciences Institute of Entomology České Budějovice 370 05 Czech Republic

Department of Animal Genetics Vavilov Institute of General Genetics Russian Academy of Sciences Moscow 117971 Russia

Department of Biological Sciences National University of Singapore Singapore 117558 Singapore

Department of Entomology and Plant Pathology North Carolina State University Raleigh NC 27695 7613

Department of Entomology Texas Agricultural and Mechanical University College Station 77843 2475 Texas

Department of Entomology Virginia Polytechnic Institute and State University Virginia VA 24061

Department of Human Parasitology TaiKang Medical School Wuhan University Wuhan 430071 China

Department of Zoology Charles University Prague 12800 Czech Republic

Department of Zoology National Museum Prague 11579 Czech Republic

Evolutionary Genomics Unit Okinawa Institute of Science and Technology Graduate University Onna son 904 0495 Japan

Florida Medical Entomology Laboratory University of Florida Vero Beach FL 32962

School of Biological Sciences University of Western Australia Perth 6009 Western Australia

School of Life Sciences and Technology Bandung Institute of Technology Bandung 40132 Indonesia

Trivedi School of Biosciences Ashoka University Sonipat 131029 India

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Solving the 250-year-old mystery of the origin and global spread of the German cockroach, Blattella germanica