The phylogeography of Myotis bat-associated rabies viruses across Canada

Abstract

As rabies in carnivores is increasingly controlled throughout much of the Americas, bats are emerging as a significant source of rabies virus infection of humans and domestic animals. Knowledge of the bat species that maintain rabies is a crucial first step in reducing this public health problem. In North America, several bat species are known to be rabies virus reservoirs but the role of bats of the Myotis genus has been unclear due to the scarcity of laboratory confirmed cases and the challenges encountered in species identification of poorly preserved diagnostic submissions by morphological traits alone. This study has employed a collection of rabid bat specimens collected across Canada over a 25 year period to clearly define the role of particular Myotis species as rabies virus reservoirs. The virus was characterised by partial genome sequencing and host genetic barcoding, used to confirm species assignment of specimens, proved crucial to the identification of certain bat species as disease reservoirs. Several variants were associated with Myotis species limited in their Canadian range to the westernmost province of British Columbia while others were harboured by Myotis species that circulate across much of eastern and central Canada. All of these Myotis-associated viral variants, except for one, clustered as a monophyletic MYCAN clade, which has emerged from a lineage more broadly distributed across North America; in contrast one distinct variant, associated with the long-legged bat in Canada, represents a relatively recent host jump from a big brown bat reservoir. Together with evidence from South America, these findings demonstrate that rabies virus has emerged in the Myotis genus independently on multiple occasions and highlights the potential for emergence of new viral-host associations within this genus.

Bat rabies in Washington State: Temporal-spatial trends and risk factors for zoonotic transmission (2000–2017)

“…Big brown bats can form large maternity colonies up to several hundred individuals [ 41 , 48 ], which might facilitate intraspecific RABV transmission. However, this alone is an insufficient explanation, as little brown bats are also highly colonial [ 41 ], but RABV positivity is thought to be low in this species, consistent with our findings [ 13 ]. Alternatively, big brown bats might be more likely to be submitted for testing by virtue of their synanthropic disposition.…”

“…While RABV is typically maintained as species-specific variants within a given reservoir, cross-species transmission occurs occasionally, and has been implicated in host shift events leading to the establishment of RABV into new reservoir species [ 9 – 13 ]. Therefore, rabies surveillance in wild mesocarnivores and bats is essential to guide risk assessments, and detect epizootics or changes in RABV reservoir epidemiology that can alter the dynamics of zoonotic transmission.…”

“…Of 205,439 bats submitted for RABV testing in the continental United States, 6.7% were positive during 2001–2009 [ 3 ], including at least 33 of 41 indigenous bat species [ 14 ]. However, the accuracy of species-specific bat rabies surveillance data in the United States can be compromised by inadequate species identification [ 3 , 9 , 13 ]. In particular, Myotis species can be difficult to differentiate, due to their similar morphology [ 13 , 15 , 16 ].…”

“…Although mesocarnivores such as coyotes ( Canis latrans ), foxes ( Urocyon cineroargenteus , Vulpes spp. ), raccoons ( Procyon lotor ), and skunks ( Mephitits mephitis , Spilogale putorius ) constitute other RABV reservoirs in North America [ 1 ], none are currently known reservoirs in Washington State or bordering jurisdictions (British Columbia, Idaho, and Oregon) [ 4 , 13 , 17 ]. Trends in bat rabies surveillance in North America have been described previously [ 18 – 24 ], but the most recent description of bat rabies epidemiology in the Pacific Northwest dates back to 1985 [ 25 , 26 ].…”

Rabies in Alaska, from the past to an uncertain future

“…The silver-haired bat rabies strain has been isolated from two myotis species in Alaska (Keen's myotis and the little brown bat); this may represent a crossspecies transmission between an infected silver-haired bat and these two Myotis species. Alternatively, it is possible that species misidentification of the myotis bats has occurred; the rabid bats in Alaska have been identified based on morphological criteria, a method which has been reported to misidentify bats approximately 38% of the time, when compared to genetic barcoding [35]. Genetic barcoding (identification of a species by its unique cytochrome c oxidase subunit 1 DNA sequence) of the five rabid bats recovered in Alaska will be invaluable to help delineate the pattern of rabies transmission among bats in this state.…”