Sociospatial structure explains marked variation in brucellosis seroprevalence in an Alpine ibex population

Abstract

In a context of (re)emerging infectious diseases with wildlife reservoirs, understanding how animal ecology shapes epidemiology is a key issue, particularly in wild ungulates that share pathogens with domestic herbivores and have similar food requirements. For the first time in Europe, brucellosis (Brucella melitensis), a virulent zoonosis, persisted in an Alpine ibex (Capra ibex) population and was transmitted to cattle and humans. To better understand disease dynamics, we investigated the relationships between the spatial ecology of ibex and the epidemiology of brucellosis. Combining home range overlap between 37 GPS-collared individuals and visual observations of 148 visually-marked individuals monitored during the 2013–2016 period, we showed that females were spatially segregated in at least 4 units all year round, whereas males were more prone to move between female units, in particular during the rutting period. In addition to ibex age, the spatial structure in females largely contributed to variation in seroprevalence in the whole population. These results suggest that non-sexual routes are the most likely pathways of intraspecific transmission, crucial information for management. Accounting for wildlife spatial ecology was hence decisive in improving our ability to better understand this health challenge involving a wildlife reservoir.

Genetic epidemiology of the Alpine ibex reservoir of persistent and virulent brucellosis outbreak

“…6 males and 8 females) translocated from the Mont Pleureur population in Switzerland 66 . Since the discovery of the outbreak in 2012, the population has been continuously monitored by Capture-Mark-Recapture (CMR) 29 . Using GPS data on marked individuals, Marchand et al 29 demonstrated that females are structured in five distinct socio-spatial units (SSU1-SSU5, Fig.…”

“…In this context, it was critical to identify the drivers of pathogen persistence in this population and individual characteristics favoring its spread. Previous works showed that host-infectiousness vary significantly across age and sex and among socio-spatial units within the Bargy massif 29 . However, genetic factors of susceptibility to brucellosis in Alpine ibex have never been investigated while several associations with innate gene polymorphism have been discovered in domestic ungulates 31,32 .…”

“…However, the situation in Bargy is alarming since the disease has affected an unprecedented high proportion of the population (38% in 2013, 95% CI [28.2; 47.8]; n = 77). Brucellosis persisted at high levels in the following years despite intense culling of animals which led to the removal of 40% of the population (see Marchand et al 29 for details). Beyond the conservation and ethical issues, this outbreak has raised public health and economic concerns since, for the first time, cattle and humans were infected by the wildlife reservoir 30 .…”

Circadian periodicity in space use by ungulates of temperate regions: How much, when and why?

“…Further details about the field methods for the Alpine ibex study can be found in Marchand et al. ().…”

Does host socio-spatial behavior lead to a fine-scale spatial genetic structure in its associated parasites?

“…While most studies on the genetic structures of H. contortus populations were performed on livestock (see [9,72]), revealing low levels of genetic differentiation even at large (e.g., state or country) spatial scales (reviewed by [33]), scarce knowledge is available in wild populations [15]. In such populations, the behavioral ecology of the host species (e.g., philopatry, sexual segregation, dispersal or migration) and landscape structure and connectivity influence host movements (e.g., [42,83]) and may generate marked socio-spatial structures at small intra population scales (e.g., [53,64]). However, how these host populations' structures influence the gene flow of their parasites is still an open question for numerous populations of wild ruminants [15].…”