An evolutionary trade-off between parasite virulence and dispersal at experimental invasion fronts

Abstract

Changing environments and habitat structure likely affect eco-evolutionary processes involved in the spatial spread of disease. Exploitative parasites are predicted to evolve in highly connected populations or in expanding epidemics. However, many parasites rely on host dispersal to reach new populations, potentially causing conflict between local transmission and global spread. We performed experimental range expansions in interconnected microcosms of the protozoan Paramecium caudatum, allowing natural dispersal of hosts infected with the bacterial parasite Holospora undulata. Parasites from range front treatments were less virulent and interfered less with host dispersal, but also invested less in horizontal transmission than parasites from range cores. An epidemiological model fitted on experimental time-series data confirmed this trade-off between dispersal adaptation and transmission, so far rarely considered in theoretical models. Our study illustrates the importance of the ecology and evolution of dispersal-related traits in spatial non-equilibrium scenarios, including emerging diseases, metapopulations or biological invasions.

Parasitism and host dispersal plasticity in an aquatic model system

“…Using 2-patch dispersal arenas, Fellous et al (2011) demonstrated that, on average over five P. caudatum strains, rates of dispersal for infected cultures were lower than those for uninfected controls. A similar trend was found in a recent study by Nørgaard et al (2021).…”

“…Previous work in this system had shown that, for a small number of host strains tested, infection reduces dispersal (Fellous et al, 2011;Nørgaard et al, 2021). The first objective of the present study was to test whether this negative effect was general, or whether strains varied in infection state-dependent dispersal.…”

“…We assayed the dispersal of infected and uninfected replicates in dispersal arenas (Figure S1), as described in Nørgaard et al (2021).…”

Predicting evolution in experimental range expansions of an aquatic model system

“…Swimming is accomplished through the coordinated movement of ciliary bands on the cell surface (Wichterman, 1986). Previous work on P. caudatum indicated a genetic basis of dispersal propensity, and plastic responses are induced by biotic factors, such as parasitism, chemical predator signals, or population density (Fellous et al, 2012;Fronhofer et al, 2018;Zilio et al, 2021). Here, we used 20 Paramecium strains (i.e., clonal mass cultures derived from a single individual) from various geographic origins (Weiler et al, 2020;Zilio et al, 2021) and representing different groups of mitochondrial haplotypes ("COI genotypes" or "genotypes", hereafter; Table S1).…”

“…Here, moving a step forward from previous ecological models (Melbourne & Hastings, 2009;Giometto et al, 2014), we employed such a combined approach to assess the predictability of evolutionary outcomes of range expansions in an aquatic model organism, the freshwater protozoan Paramecium caudatum. Following previous studies ) Nørgaard et al (2021, we used interconnected 2-patch systems to establish a range front treatment, where recurrent episodes of dispersal alternated with intermittent periods of population growth. In the contrasting range core treatment, only the non-dispersing individuals were maintained.…”