Genetic variation in resistance, but not tolerance, to a protozoan parasite in the monarch butterfly

Abstract

Natural selection should strongly favour hosts that can protect themselves against parasites. Most studies on animals so far have focused on resistance, a series of mechanisms through which hosts prevent infection, reduce parasite growth or clear infection. However, animals may instead evolve tolerance, a defence mechanism by which hosts do not reduce parasite infection or growth, but instead alleviate the negative fitness consequences of such infection and growth. Here, we studied genetic variation in resistance and tolerance in the monarch butterfly (Danaus plexippus) to its naturally occurring protozoan parasite, Ophryocystis elektroscirrha. We exposed 560 monarch larvae of 19 different family lines to one of five different parasite inoculation doses (0, 1, 5, 10 and 100 infective spores) to create a range of parasite loads in infected butterflies. We then used two proxies of host fitness (adult lifespan and body mass) to quantify: (i) qualitative resistance (the ability to prevent infection; also known as avoidance or anti-infection resistance); (ii) quantitative resistance (the ability to limit parasite growth upon infection; also known as control or anti-growth resistance); and (iii) tolerance (the ability to maintain fitness with increasing parasite infection intensity). We found significant differences among host families in qualitative and quantitative resistance, indicating genetic variation in resistance. However, we found no genetic variation in tolerance. This may indicate that all butterflies in our studied population have evolved maximum tolerance, as predicted by some theoretical models.

Age-Specific Variation in Immune Response inDrosophila melanogasterHas a Genetic Basis

“…Tolerance has long been recognized as a trait that could evolve in response to selection although conditions favoring the maintenance of variation in tolerance are often argued to be more stringent that those maintaining variation in resistance traits in natural populations (Roy and Kirchner 2000;Miller et al 2005Miller et al , 2006. Indeed variation in tolerance is not always found (Lefevre et al 2011) but there is ample evidence of its existence in natural populations (Fineblum and Rausher 1995;Mauricio et al 1997;Blanchet et al 2010) and more empirical work is necessary to explain the maintenance of this variation (Read et al 2008;Svensson and Raberg 2010). Mutant studies have identified a few genes/pathways that play a role in tolerance to infection Shinzawa et al 2009) but as far as we aware no genes have been identified that contribute to natural variation in tolerance.…”

Experimental infection dynamics: using immunosuppression andin vivoparasite tracking to understand host resistance in an amphibian-trematode system

“…For instance, Altizer et al (Altizer et al, 2001) found variations in the susceptibility of different populations of monarch butterflies to the protozoan parasite Ophryocystis elektroscirrha using field surveys. Then, a subsequent study by Lefèvre et al (Lefèvre et al, 2011) employed an experimental approach to show how host populations varied in their resistance but not tolerance to this pathogen.…”

Disease ecology across soil boundaries: effects of below-ground fungi on above-ground host–parasite interactions

“…Moreover, using lifespan as an estimate of virulence has proven repeatedly to correlate well with estimates of parasite reproduction, monarch resistance and monarch tolerance to infection (e.g. [17,18,21]). …”

“…This measurement, used routinely in this host -parasite system [17,18,21,38] combines longevity and starvation resistance, both of which are highly correlated with the lifespan and life-time fitness of monarchs under more natural conditions [17]. After death, the spore load of each butterfly was measured following described methods [17].…”