Length of intervals between epidemics: evaluating the influence of maternal transfer of immunity.

Romain Garnier,Sylvain Gandon,Karin C Harding,Thierry Boulinier

doi:10.1002/ece3.955

Abstract

The length of intervals between epidemic outbreaks of infectious diseases is critical in epidemiology. In several species of marine mammals and birds, it is pivotal to also consider the life history of the species of concern, as the contact rate between individuals can have a seasonal flux, for example, due to aggregations during the breeding season. Recently, particular interest has been given to the role of the dynamics of immunity in determining the intervals between epidemics in wild animal populations. One potentially powerful, but often neglected, process in this context is the maternal transfer of immunity. Here, we explore theoretically how the transfer of maternal antibodies can delay the recurrence of epidemics using Phocine Distemper in harbor seals as an example of a system in which epidemic outbreaks are followed by pathogen extinction. We show that the presence of temporarily protected newborns can significantly increase the predicted interval between epidemics, and this effect is strongly dependent on the degree of synchrony in the breeding season. Furthermore, we found that stochasticity in the onset of epidemics in combination with maternally acquired immunity increases the predicted intervals between epidemics even more. These effects arise because newborns with maternal antibodies temporarily boost population level immunity above the threshold of herd immunity, particularly when breeding is synchronous. Overall, our results show that maternal antibodies can have a profound influence on the dynamics of wildlife epidemics, notably in gregarious species such as many marine mammals and seabirds.

Highlights

In vertebrates, the immune response to parasites relies on both a nonspecific innate response and a delayed and more specific acquired response (Frank 2002)
The transfer of maternal antibodies was found to be able to cause a significant increase in the predicted intervals between epidemics for Phocine distemper virus (PDV) in European harbor seals (Fig. 1)
The mean interval between epizootics after 300 years of simulation was longer when the maternal transfer of antibodies was included for all assumed values of R0, the difference was smaller for lower values of the basic reproductive number

Summary

Introduction

The immune response to parasites relies on both a nonspecific innate response and a delayed and more specific acquired response (Frank 2002). Part of this acquired immune response relies on in the induction of immunoglobulins or antibodies, that can be transmitted to the offspring (Brambell 1970) through the colostrum and the milk in mammals or via the egg yolk in oviparous species Because this transfer can result in a direct but temporary protection against the parasite (see for instance Wallach et al 1992; Gustafsson et al 1994), eco-epidemiological implications of this mechanism might be important (Gasparini et al 2001; Grindstaff et al 2003) but remain sparsely studied (Boulinier and Staszewski 2008).

Methods

Results

Conclusion