The costs of evolving resistance in heterogeneous parasite environments

Abstract

The evolution of host resistance to parasites, shaped by associated fitness costs, is crucial for epidemiology and maintenance of genetic diversity. Selection imposed by multiple parasites could be a particularly strong constraint, as hosts either accumulate costs of multiple specific resistances or evolve a more costly general resistance mechanism. We used experimental evolution to test how parasite heterogeneity influences the evolution of host resistance. We show that bacterial host populations evolved specific resistance to local bacteriophage parasites, regardless of whether they were in single or multiple-phage environments, and that hosts evolving with multiple phages were no more resistant to novel phages than those evolving with single phages. However, hosts from multiple-phage environments paid a higher cost, in terms of population growth in the absence of phage, for their evolved specific resistances than those from single-phage environments. Given that in nature host populations face selection pressures from multiple parasite strains and species, our results suggest that costs may be even more critical in shaping the evolution of resistance than previously thought. Furthermore, our results highlight that a better understanding of resistance costs under combined control strategies could lead to a more 'evolution-resistant' treatment of disease.

Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

“…S1). This result indicates that resistance to phages comes at a fitness cost (40)(41)(42)(43)(44), because no bottlenecking could have occurred, given that ca. 10 8 bacterial cells were introduced to fresh microcosms at each serial transfer.…”

Adaptation costs to constant and alternating polluted environments

“…(2003) have shown enhanced fitness in a novel polluted environment for Drosophila melanogaster populations adapted to two alternating stressors compared to populations adapted to only one of them. These results could change the classical vision that adaptation to several stressors decreases the adaptive potential of populations (Hoffmann & Parsons, 1991; Koskella et al., 2012; Tilman & Lehman, 2001). Experimental evolution studies should thus mimic more precisely the temporally and spatially heterogeneous environments found in natural conditions to provide a better understanding of the adaptive potential of populations to pollutants.…”

“…Experimental studies on adaptation costs generally focus on costs induced by a constant stress from a single stressor (Jansen, Stoks, et al., 2011; Ward & Robinson, 2005; Xie & Klerks, 2003) or from a simultaneous combination of stressors (Jansen, de Meester, Cielen, Buser, & Stoks, 2011; Jasmin & Kassen, 2007; Koskella, Lin, Buckling, & Thompson, 2012). Comparatively few studies have examined how populations adapt to a temporally heterogeneous environment and its consequence on adaptation costs (Magalhães, Cailleau, Blanchet, & Olivieri, 2014; Reed et al., 2003; Turner & Elena, 2000), despite the fact that wild populations experience temporal environmental heterogeneity (Hedrick, 1986; Levins, 1968).…”

Evolutionary Ecology of Prokaryotic Immune Mechanisms

“…Surface modification can also provide broad-range immunity against multiple phages, but the range of immunity depends on the type of modification and the phage receptors involved; for example, a point mutation in a receptor is likely to be associated with a lower fitness cost than the complete loss of the same receptor but is also more likely to provide relatively narrow-range resistance against a single or few phage species compared to receptor loss. In agreement with this, evolution of broad-range immunity has been shown to be more costly than narrow-range immunity (164), but the mechanistic basis of immunity in these experiments was not assessed. In some cases, surface modification-based resistance against one phage can increase susceptibility to other phages, as is the case for the cyanobacterium Prochlorococcus (165).…”