Dispersal in a patchy landscape reveals contrasting determinants of infection in a wild avian malaria system

Abstract

Summary 1.Understanding exactly when, where and how hosts become infected with parasites is critical to understanding host-parasite co-evolution in natural populations. However, for host-parasite systems in which hosts or parasites are mobile, for example in vector-borne diseases, the spatial location of infection and the relative importance of parasite exposure at successive host lifehistory stages are often uncertain. 2. Here, using a 6-year longitudinal data set from a spatially referenced population of blue tits, we test the extent to which infection by avian malaria parasites is determined by conditions experienced at natal or breeding sites, as well as by postnatal dispersal between the two. 3. We show that the location and timing of infection differs markedly between two sympatric malaria parasite species. For one species (Plasmodium circumflexum), our analyses indicate that infection occurs after birds have settled on breeding territories, and because the distribution of this parasite is temporally stable across years, hosts born in malarious areas could in principle alter their exposure and potentially avoid infection through postnatal dispersal. Conversely, the spatial distribution of another parasite species (Plasmodium relictum) is unpredictable and infection probability is positively associated with postnatal dispersal distance, potentially indicating that infection occurs during this major dispersal event. 4. These findings suggest that hosts in this population may be subject to divergent selection pressures from these two parasites, potentially acting at different life-history stages. Because this implies parasite species-specific predictions for many coevolutionary processes, they also illustrate the complexity of predicting such processes in multi-parasite systems.

Avian haemosporidian parasites in an urban forest and their relationship to bird size and abundance

“…Heterogeneities of the environment also play an important role in infection risk; such as closeness to water bodies where vectors are more abundant (e.g. Wood et al 2007;Knowles et al 2014), and different forestry practices that can create puddles for vector breeding, which increases infection probabilities (Lüdtke et al 2013). Although we found a significant interaction between body size and abundance, it seems that there is not a strong trade-off between these two variables in regard to infection probability.…”

How parasite-mediated costs drive the evolution of disease state-dependent dispersal

“…Hence, it is expected that both factors enhance I-biased dispersal, but this depends on the autocorrelation (as discussed in Section 4.1). Indeed, infection during (and after) dispersal is observed in a bird species (Knowles et al, 2013), and recovery during dispersal is also observed in salmon that are infected with the larvae of freshwater pearl-mussels (e.g. Morales et al, 2006;Akiyama and Iwakuma, 2009;Terui et al, 2014).…”

“…For example, Knowles et al (2013) reported that infection occurred after dispersal, and potentially during dispersal, in the blue tit (C. caeruleus). In the study, they examined the location and timing of infections from two malaria parasites (Plasmodium circumflexum and P. relictum), and determined that the infection with P. circumflexum occurred after birds settled into breeding territories.…”

“…In a host-parasite system, parasite life history can greatly modify the dispersal costs of their hosts. For example, in the case of the blue tit (Cyanistes caeruleus Knowles et al, 2013), if the infection (or indirect transmission) of parasites occurs during dispersal, then susceptible individuals experience a higher cost than do infected individuals. Similarly, if infected hosts have a chance of recovery during dispersal (e.g.…”

The impact of lungworm parasites on rates of dispersal of their anuran host, the invasive cane toad

“…Parasite infection is known to affect locomotor performance in laboratory ''racetrack'' studies, in toads as well as in other anurans (Goodman and Johnson 2011;Kelehear et al 2009;Marr et al 2010;Moretti et al 2014;Pizzatto and Shine 2011). However, in the wild, sustained rates of movement and dispersal likely are influenced by many factors (e.g., resource availability, habitat openness) that are not incorporated in laboratory studies (Knowles et al 2014;Stevens and Coulon 2012). Modelling and empirical studies have shown that parasites may increase or decrease host dispersal, depending on the circumstances (Iritani 2015;Iritani and Iwasa 2014;Lion et al 2006;Scott 1988).…”