The history of rabies in the Western Hemisphere

Abstract

Before the introduction of control programs in the 20th century, rabies in domestic dogs occurred throughout the Western Hemisphere. However, historical records and phylogenetic analysis of multiple virus isolates indicate that, before the arrival of the first European colonizers, rabies virus was likely present only in bats and skunks. Canine rabies was either rare or absent among domestic dogs of Native Americans, and first arrived when many new dog breeds were imported during the period of European colonization. The introduction of the cosmopolitan dog rabies lyssavirus variant and the marked expansion of the dog population provided ideal conditions for the flourishing of enzootic canine rabies. The shift of dog-maintained viruses into gray foxes, coyotes, skunks and other wild mesocarnivores throughout the Americas and to mongooses in the Caribbean has augmented the risk of human rabies exposures and has complicated control efforts. At the same time, the continued presence of bat rabies poses novel challenges in the absolute elimination of canine and human rabies. This article compiles existing historical and phylogenetic evidence of the origins and subsequent dynamics of rabies in the Western Hemisphere, from the era preceding the arrival of the first European colonizers through the present day. A companion article reviews the current status of canine rabies control throughout the Western Hemisphere and steps that will be required to achieve and maintain its complete elimination (Velasco-Villa et al., 2017).

Fig. 1

Maximum likelihood phylogenetic tree of RABLV adapted from (Velasco-Villa et al., 2008b), in which relationships among major dog-maintained and dog-related variants of the world with indigenous bat-maintained and bat-related RABLV variants of the Western Hemisphere are depicted. The cosmopolitan dog group represents multiple introductions of dog-maintained RABLV from Europe into the Western Hemisphere, Africa and the Middle East and how they potentially gave rise to the establishment of epizootics in terrestrial mesocarnivores in those continents. Conversely, the Old World group demonstrates other dog-maintained RABLV introductions into Africa, Central Asia and the circumpolar region, likely coming from the Far East.

Fig. 2

Timeline of introduction of the cosmopolitan RABLV group into the Americas, Africa and the Middle East as well as introductions of more ancient Asian RABLV lineages into Africa, Central Asia and the circumpolar region. Dates in the nodes denote an estimated time period in which a common ancestor giving rise to the extant viral diversity existed. The evolutionary history of terrestrial-mammal-associated RABLVs may also be appreciated. The time-scaled phylogeny is reconstructed based on the complete nucleoprotein gene alignment, using the BEAST software package with a codon-partitioned (GTR112 + CP112 + Gamma112) substitution model and an uncorrelated log-normal relaxed molecular clock model. Estimated dates to the most recent common ancestor (MRCA), for important clades, are depicted as 95% highest posterior density intervals. For clarity, the label of each major clade is shown to the right of the phylogeny.

Fig. 3

Distribution of accumulated human rabies cases transmitted by bats in countries of Latin America and the Caribbean from 2005-2015. Grayscale reflects the number of laboratory-confirmed cases in which RABLV variants associated with different species of bats were identified (mainly RABLV lineages associated with vampire bats). Source: SIEPI “Especie”, http://siepi.panaftosa.org.br/Export.aspx. Inset blue bars represent the total number of bat species per country (or their respective bat bio-diversity), and red bars represent the actual number of species most frequently found to be rabies-positive in each country (Escobar et al., 2015).