Pathogen and host genotype differently affect pathogen fitness through their effects on different life-history stages

Abstract

BackgroundAdaptation of pathogens to their hosts depends critically on factors affecting pathogen reproductive rate. While pathogen reproduction is the end result of an intricate interaction between host and pathogen, the relative contributions of host and pathogen genotype to variation in pathogen life history within the host are not well understood. Untangling these contributions allows us to identify traits with sufficient genetic variation for selection to act and to identify mechanisms of coevolution between pathogens and their hosts. We investigated the effects of pathogen and host genotype on three life-history components of pathogen fitness; infection efficiency, latent period, and sporulation capacity, in the oat crown rust fungus, Puccinia coronata f.sp. avenae, as it infects oats (Avena sativa).ResultsWe show that both pathogen and host genotype significantly affect total spore production but do so through their effects on different life-history stages. Pathogen genotype has the strongest effect on the early stage of infection efficiency, while host genotype most strongly affects the later life-history stages of latent period and sporulation capacity. In addition, host genotype affected the relationship between pathogen density and the later life-history traits of latent period and sporulation capacity. We did not find evidence of pathogen-by-host genotypic (GxG) interactions.ConclusionOur results illustrate mechanisms by which variation in host populations will affect the evolution of pathogen life history. Results show that different pathogen life-history stages have the potential to respond differently to selection by host or pathogen genotype and suggest mechanisms of antagonistic coevolution. Pathogen populations may adapt to host genotypes through increased infection efficiency while their plant hosts may adapt by limiting the later stages of pathogen growth and spore production within the host.

The Jack of All Trades Is Master of None: A Pathogen's Ability to Infect a Greater Number of Host Genotypes Comes at a Cost of Delayed Reproduction

“…We did not detect a significant strain effect on infection efficiency although we did so in a previous experiment conducted in growth chambers (Bruns et al. ), perhaps due to greater environmental variation in the current greenhouse study. Variation in infection efficiency affected differences in pustule density, which in turn, strongly affected the expression of later life‐history traits.…”

“…A quantitative spray inoculator (Scientific apparatus shop, University of Minnesota) was used to inoculate a 15 cm section of the penultimate leaf of each plant, as previously described (Bruns et al. ). To estimate the inoculation dose for each plant receiving the high spore dose, a glass slide mounted with double‐sided tape was fixed next to the leaf.…”

“…Spores were transferred to gel capsules, desiccated, and weighed to obtain estimates of total dry spore mass as previously described (Bruns et al. ). There are approximately 5 × 10 8 spores per gram of dried P. coronata urediniospores (data not shown).…”

The impact of parasitism on resource allocation in a fungal host: the case of Cryphonectria parasitica and its mycovirus, Cryphonectria Hypovirus 1

“…Adamo (1999) observed an increase in egg laying following the activation of the host immune system by injection of inert components of the cell wall of the bacteria Serratia marcescens , again suggesting an acceleration of reproduction in the face of probable parasitism. Similar changes in life history in response to parasitism also exist in plants, as do many cases of variation in life‐history traits involved in resistance or tolerance have been reported in Arabidopsis thaliana (Kover & Schaal, 2002; Pagán, Alonso‐Blanco, & Garcia‐arenal, 2008; Salvaudon & Shykoff, 2013) as well as in other plant species (Bruns, Carson & May, 2012). Surprisingly, in fungi, no clear evidence of parasite‐driven modifications on fungal life‐history traits has yet been reported, although conversely host genetic identity was found to alter resource allocation balance in two fungal pathogens, the oomycete Hyaloperonospora parasitica (Heraudet, Salvaudon, & Shykoff, 2008) and the basidiomycete Puccinia triticina (Pariaud et al., 2013).…”

“…Such trade‐offs have been reported in animals (Creighton, Heflin, & Belk, 2009; Kubička & Kratochvíl, 2009; Ohbayashi‐Hodoki & Shimada, 2005; Reznick, 1983; Yund, Marcum, & Stewart‐Savage, 1997) and in plants (Houle, 1999; Obeso, 2002; Silvertown & Dodd, 1999; Sletvold & Ågren, 2015). However, investigations of resource allocation in fungi appear to be scarce (Bruns et al., 2012) and are often oriented toward the study of trade‐off between a fungal pathogen and its host (Heraudet et al., 2008; Kover, 2000; Pariaud et al., 2013). Our data demonstrating a negative correlation in virus‐free C. parasitica isolates between asexual sporulation and mycelial growth extends support for the hypothesis of trade‐offs between current reproduction and somatic growth to a new kingdom of multicellular organisms.…”