Research Article: Maternal antibody and the maintenance of a lyssavirus in populations of seasonally breeding African bats

Date Published: June 12, 2018

Publisher: Public Library of Science

Author(s): David T. S. Hayman, Angela D. Luis, Olivier Restif, Kate S. Baker, Anthony R. Fooks, Clint Leach, Daniel L. Horton, Richard Suu-Ire, Andrew A. Cunningham, James L. N. Wood, Colleen T. Webb, Charles E Rupprecht.


Pathogens causing acute disease and death or lasting immunity require specific spatial or temporal processes to persist in populations. Host traits, such as maternally-derived antibody (MDA) and seasonal birthing affect infection maintenance within populations. Our study objective is to understand how viral and host traits lead to population level infection persistence when the infection can be fatal. We collected data on African fruit bats and a rabies-related virus, Lagos bat virus (LBV), including through captive studies. We incorporate these data into a mechanistic model of LBV transmission to determine how host traits, including MDA and seasonal birthing, and viral traits, such as incubation periods, interact to allow fatal viruses to persist within bat populations. Captive bat studies supported MDA presence estimated from field data. Captive bat infection-derived antibody decayed more slowly than MDA, and while faster than estimates from the field, supports field data that suggest antibody persistence may be lifelong. Unobserved parameters were estimated by particle filtering and suggest only a small proportion of bats die of disease. Pathogen persistence in the population is sensitive to this proportion, along with MDA duration and incubation period. Our analyses suggest MDA produced bats and prolonged virus incubation periods allow viral maintenance in adverse conditions, such as a lethal pathogen or strongly seasonal resource availability for the pathogen in the form of seasonally pulsed birthing.

Partial Text

Understanding what mechanisms allow maintenance of infections within populations is fundamental to disease ecology [1, 2]. Pathogens that cause acute disease and death or lasting immunity may require specific spatial (e.g. metapopulation [3]), or temporal (e.g. hibernation [4]) processes or multiple host species to persist in populations [5]. Lyssaviruses, such as rabies virus (RABV), cause acute disease that is invariably fatal in most mammalian species once clinical signs develop. Models of lyssavirus dynamics have concentrated on RABV in terrestrial mammals (e.g., domestic dogs, raccoons and foxes [6–11]). However, the vast majority of lyssaviruses, of which RABV is only one, have bats as their natural (co-evolved) reservoir hosts [12–14]. Phylogenetic analyses suggest that all lyssaviruses, including RABV, originated from bats [15]. The genetic distance among some African and Eurasian bat lyssaviruses means that RABV-derived vaccines are ineffective in providing protection due to a lack of cross-reactivity [16–18]. Understanding the dynamics of bat lyssaviruses is therefore necessary to understand infection emergence and to manage zoonotic disease risk [19–22].

Our study enabled us to confirm that MDA to LBV in E. helvum exists and to estimate antibody rates of decay in captive bat (Fig 2). Our results support field data that suggest adult infection-derived antibody duration is prolonged and perhaps lifelong [44]. Combining species-specific field serological and demographic data into a mechanistic model of LBV dynamics, we predict that MDA may reduce the probability of virus maintenance in populations of these tropical bats (Fig 4).




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