Abstract
Resistance is a key determinant in interactions between hosts and their parasites. Understanding the amount and distribution of variation in this trait between strains can provide insights into (co)evolutionary processes and their potential to shape patterns of diversity in natural populations. Using controlled inoculation in experimental mass cultures, we investigated the quantitative variation in resistance to the bacterial parasite Holospora undulata across a worldwide collection of strains of its ciliate host Paramecium caudatum. We combined the observed variation with available information on the phylogeny and biogeography of the strains. We found substantial variation in resistance among strains, with upper-bound values of broad-sense heritability >0.5 (intraclass correlation coefficients). Strain estimates of resistance were repeatable between laboratories and ranged from total resistance to near-complete susceptibility. Early (1 week post inoculation) measurements provided higher estimates of resistance heritability than did later measurements (2–3 weeks), possibly due to diverging epidemiological dynamics in replicate cultures of the same strains. Genetic distance (based on a neutral marker) was positively correlated with the difference in resistance phenotype between strains (r = 0.45), essentially reflecting differences between highly divergent clades (haplogroups) within the host species. Haplogroup A strains, mostly European, were less resistant to the parasite (49% infection prevalence) than non-European haplogroup B strains (28%). At a smaller geographical scale (within Europe), strains that are geographically closer to the parasite origin (Southern Germany) were more susceptible to infection than those from further away. These patterns are consistent with a picture of local parasite adaptation. Our study demonstrates ample natural variation in resistance on which selection can act and hints at symbiont adaptation producing signatures in geographic and lineage-specific patterns of resistance in this model system.
Highlights
Evolutionary interactions between hosts and their symbionts can shape patterns of genetic diversity and adaptation in natural communities (Kaltz and Shykoff, 1998; Howells et al, 2013; Caldera et al, 2019)
For this diversification to occur there must be heritable variation in the traits determining the “compatibility” between a host and a symbiont, from resistance and infectivity to more complex life-history or developmental traits (Law and Dieckmann, 1998; Dale and Moran, 2006; Chomicki et al, 2020). This variation can be assessed in controlled infection experiments, using different combinations of host and symbiont genotypes (Carius et al, 2001; Kaltz and Shykoff, 2002; Cayetano and Vorburger, 2013). Such experiments inform on the present evolutionary potential of the interacting players, but can reveal patterns shaped by theirevolutionary past, such as local adaptation (Greischar and Koskella, 2007; Hoeksema and Forde, 2008), lineage or species specificity (Summerer et al, 2007; Chappell and Rausher, 2016) and symbiont life styles (Degnan and Moran, 2008; Sachs et al, 2011)
Phylogenetic analysis revealed that most strains fall into two main clades, defined by the A and B haplogroups (Figure 2 and Table 1)
Summary
Evolutionary interactions between hosts and their symbionts can shape patterns of genetic diversity and adaptation in natural communities (Kaltz and Shykoff, 1998; Howells et al, 2013; Caldera et al, 2019). The ciliated protist Paramecium spp. is a useful model organism for experimental investigations into diverse associations with endosymbiotic bacteria that represent the full continuum of endosymbiotic interactions: from facultative to obligate, and from horizontal to mixed to vertical transmission (Preer et al, 1974; Fokin and Görtz, 2009; Fujishima, 2009; Görtz and Fokin, 2009; Goertz, 2010; Fujishima and Kodama, 2012; Plotnikov et al, 2019) The possession of these endosymbiotic partners is likely the result of Paramecium’s bacterivorous nature, whereby some of its prey have evolved means to evade digestion and to take up residence in the cytoplasm of the cell, and in the host nuclei (Goertz, 2010; Boscaro et al, 2013; Schulz and Horn, 2015; Garushyants et al, 2018; Potekhin et al, 2018; Munoz-Gomez et al, 2019). The Paramecium-Holospora system has served as a model to study epidemiology and evolution in experimental microcosms (Lohse et al, 2006; Nidelet et al, 2009; Duncan et al, 2011a, 2015, 2018; Castelli et al, 2015; Dusi et al, 2015; Nørgaard et al, 2020; Zilio et al, 2020a,b)
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