Species diversity concurrently dilutes and amplifies transmission in a zoonotic host–pathogen system through competing mechanisms

Abstract

In this era of unprecedented biodiversity loss and increased zoonotic disease emergence, it is imperative to understand the effects of biodiversity on zoonotic pathogen dynamics in wildlife. Whether increasing biodiversity should lead to a decrease or increase in infection prevalence, termed the dilution and amplification effects, respectively, has been hotly debated in disease ecology. Sin Nombre hantavirus, which has an ∼35% mortality rate when it spills over into humans, occurs at a lower prevalence in the reservoir host, the North American deermouse, in areas with higher small mammal diversity-a dilution effect. However, the mechanism driving this relationship is not understood. Using a mechanistic mathematical model of infection dynamics and a unique long-term, high-resolution, multisite dataset, it appears that the observed dilution effect is a result of increasing small-mammal diversity leading to decreased deermouse population density and, subsequently, prevalence (a result of density-dependent transmission). However, once density is taken into account, there is an increase in the transmission rate at sites with higher diversity-a component amplification effect. Therefore, dilution and amplification are occurring at the same time in the same host-pathogen system; there is a component amplification effect (increase in transmission rate), but overall a net dilution because the effect of diversity on reservoir host population density is stronger. These results suggest we should focus on how biodiversity affects individual mechanisms that drive prevalence and their relative strengths if we want to make generalizable predictions across host-pathogen systems.

Maintenance of Borrelia burgdorferi among vertebrate hosts: a test of dilution effect mechanisms

“…Our results support previous work, indicating that multiple mechanisms contribute to the dilution effect in disease systems (Luis et al. ). Likewise, for the Lyme disease system, the strength of these mechanisms varied.…”

“…Traditionally, science involves making inferences about mechanisms based on the experimental manipulation of study systems. To date, few studies have experimentally tested the dilution effect to establish causal mechanisms (but see Venesky et al 2013, Halliday et al 2017, Linske et al 2018, Luis et al 2018, Strauss et al 2018. Individual-based models (IBMs) can allow us to simulate communities with various host compositions to assess the relative importance of proposed mechanisms of the dilution effect hypothesis.…”

Cross-species pathogen spillover across ecosystem boundaries: mechanisms and theory

“…Higher species richness may result in more direct or indirect contacts between different species, thereby increasing spillover opportunities and spillover diversity [49]. Although the complex interplay between species diversity and parasite transmission within a given host species has been studied in some depth, and can be negative or positive depending on the context [50,51], less is known about how species diversity affects transmission between species [14]. All else being equal, a positive relationship between biodiversity and spillover diversity has been proposed [3,14,[52][53][54], as parasite diversity is expected to increase with host diversity [55].…”

Tree diversity regulates forest pest invasion

“…To date, numerous studies have separately examined how host species diversity may promote or diminish parasite/ disease diversity (6,7). While small-scale and experimental research (especially on a single parasite) has provided empirical and theoretical evidence of facilitation, dilution, or both (8), corresponding patterns in natural ecosystems are largely unknown, especially over regional or continental scales. More importantly, the role of overall community diversity (i.e., hosts plus nonhosts in the entire assemblages) in multipest invasion remains elusive (9)(10)(11)(12).…”