Parasite interactions in natural populations: insights from longitudinal data

Abstract

The physiological and immunological state of an animal can be influenced by current infections and infection history. Consequently, both ongoing and previous infections can affect host susceptibility to another parasite, the biology of the subsequent infection (e.g. infection length) and the impact of infection on host morbidity (pathology). In natural populations, most animals will be infected by a succession of different parasites throughout the course of their lives, with probably frequent concomitant infections. The relative timing of different infections experienced by a host (i.e. the sequence of infection events), and the effects on factors such as host susceptibility and host survival, can only be derived from longitudinal data on individual hosts. Here we review some of the evidence for the impact of co-infection on host susceptibility, infection biology and pathology focusing on insights obtained from both longitudinal studies in humans and experiments that explicitly consider the sequence of infection. We then consider the challenges posed by longitudinal infection data collected from natural populations of animals. We illustrate their usefulness using our data of microparasite infections associated with field vole (Microtus agrestis) populations to examine impacts on susceptibility and infection length. Our primary aim is to describe an analytical approach that can be used on such data to identify interactions among the parasites. The preliminary analyses presented here indicate both synergistic and antagonistic interactions between microparasites within this community and emphasise that such interactions could have significant impacts on host-parasite fitness and dynamics.

Parasite competition hidden by correlated coinfection: using surveys and experiments to understand parasite interactions

“…These findings are consistent with the predictions of Graham (2008), who suggested that when resources are not limiting, topdown forces (i.e., immune function) will control interactions between co-occurring parasites, especially for ecologically similar parasites that are subjected to the same elements of the immune systems (Pedersen and Fenton 2007). Observed competitive effects likely owe to decreases in parasite persistence (i.e., increases in host clearance rate) after infection rather than changes in host susceptibility, given that we saw an increase in Ribeiroia recovery with coinfection when hosts were necropsied within 10 days (Telfer et al 2008). …”

“…In many systems, hosts vary in susceptibility, creating heterogeneity in infections even following comparable exposures (Karvonen et al 2007, Cattadori et al 2008. Naturally occurring hosts also differ in parasite exposure as a function of microhabitat use, behavior, or development time (Poulin 2007, Telfer et al 2008, all of which could enhance infection heterogeneity and exposure to both parasites. Although not tested here, heterogeneities in parasite exposure could be influenced by prior or concurrent exposure to another parasite (e.g., Cattadori et al 2008).…”

“…But within each of these easily-observed groups exists another community of interacting parasite species. Although most studies focus on single-host-single-pathogen interactions, growing evidence suggests that interactions among co-occurring parasites can influence host pathology, parasite transmission, and the evolution of virulence (Cox 2001, Pedersen and Fenton 2007, Lello et al 2008, Telfer et al 2008, Lively 2009. A promising frontier in understanding parasite interactions within hosts involves applying the principles of community ecology to within-host communities (Pedersen and Fenton 2007, Poulin 2007, Graham 2008.…”

Heligmosomoides polygyrusreduces infestation ofIxodes ricinusin free-living yellow-necked mice,Apodemus flavicollis

“…There is increasing evidence that interactions between parasites may also play a significant role in affecting susceptibility of hosts to infection (Hochberg and Holt, 1990 ;Sousa, 1994 ;Petney and Andrew, 1998 ;Cox, 2001 ;Lello et al 2004 ;Maizels et al 2004 ;Faulkner et al 2005 ;Hartgers and Yazdanbakhsh, 2006 ;Cattadori et al 2007Cattadori et al , 2008 ; Lello and Hussell, 2008). However, while these findings indicate that we should consider the whole community of parasites to understand the dynamics of each component species, results from previous studies are not always consistent (Behnke et al 2001 ;Poulin, 2001 ;Behnke, 2008 ;Graham, 2008 ;Telfer et al 2008). Studies in controlled laboratory conditions have not only identified strong parasite interactions but also teased apart some of the molecular mechanisms involved (Curry et al 1995 ;Maizels et al 2004 ;Edwards et al 2005 ;Kamal and El Sayed Khalifa, 2006 ;Graham et al 2007 ;Bradley and Jackson, 2008 ;Fenton et al 2008).…”

Progress on research on rodents and rodent-borne zoonoses in South-east Asia

“…Moreover, identifying a reservoir for a single parasite may be rather restrictive due to the circulation of multiple pathogens in natural systems. Multiple infection is the rule, but has only recently been considered as a key factor in wild ecosystems (Telfer et al 2008;Bordes and Morand 2009).…”