Among-Strain Variation in Resistance of Paramecium caudatum to the Endonuclear Parasite Holospora undulata: Geographic and Lineage-Specific Patterns

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.

Predicting evolution in experimental range expansions of an aquatic model system

“…This method characterises the line for the most frequent COI genotype, and it has a resolution threshold of c. 5%, i.e., it can detect 2-3 cells of a minority genotype in the sample (Killeen et al, 2017). The sequences used are deposited in GenBank under the accession numbers listed in Barth et al (2006) and Weiler et al (2020).…”

Natural Shifts in Endosymbionts' Occurrence and Relative Frequency in Their Ciliate Host Population

“…However, an infection of P. biaurelia with M. polyxenophila has not been observed so far. This might be explained by potential strain specificity or possibly even resistance since the latter acts as key determinant in parasitic host-symbiont interactions as demonstrated for P. caudatum and H. undulata (Weiler et al, 2020 ). The dominating prevalence of M. polyxenophila in the macronucleus in P. caudatum is intermitted by the appearance of H. undulata and C. varicaedens .…”

“…Many if not most symbionts are obligate intracellular thus completely dependent on a host cell for reproduction. As they require resources from the host cell, these bacteria inflict costs on Paramecium (Dusi et al, 2014 ; Weiler et al, 2020 ) like reduction in cell division, motility, survival (Restif and Kaltz, 2006 ; Nørgaard et al, 2021 ; Zilio et al, 2020 ) as well as the potential disruption of sexual processes (Görtz and Fujishima, 1983 ). On the other hand, several experimental studies show that paramecia carrying a bacterial endosymbiont have an advantage relative to aposymbiotic or symbiont-free cells (Hori and Fujishima, 2003 ; Bella et al, 2016 ; Grosser et al, 2018 ; Schu and Schrallhammer, 2018 ; Koehler et al, 2019 ; Pasqualetti et al, 2020 ).…”

“…Next to consequences for host and symbiont, symbiotic interactions have the ability to shape patterns of genetic diversity (Weiler et al, 2020 ), hence playing an important role for the dynamics of ecosystems with implications not only for the symbiotic partners themselves but also for other species abundant in this community (Banerji et al, 2015 ; Bjorbækmo et al, 2020 ). Exemplary, parasites infecting hosts across all trophic levels have the ability to drastically alter their host's behavior and morphology (Lafferty et al, 2008 ; Sukhdeo, 2010 ) as in the case of the parasite H. undulata which lead to changes in the phenotype of its host ( Paramecium ) to evade predation (Banerji et al, 2015 ).…”

Parasitism and host dispersal plasticity in an aquatic model system

“…Of course, interpretations of our results should be undertaken with caution. We know little about the intensity of Paramecium–Holospora interactions in natural populations (Weiler et al., 2020) and, in particular, have no information on the (co)evolutionary history of the strains used in our experiments. Nonetheless, our data suggest a possible genetic basis of context‐dependent dispersal in this system and hence genetic variation that might be seen by natural selection.…”