Acceptable Loss: Fitness Consequences of Salinity-Induced Cell Death in a Halotolerant Microalga.

AbstractEnvironmentally induced reductions in fitness components (survival, fecundity) are generally considered as passive, maladaptive responses to stress. However, there is also mounting evidence for active, programmed forms of environmentally induced cell death in unicellular organisms. While conceptual work has questioned how such programmed cell death (PCD) might be maintained by natural selection, few experimental studies have investigated how PCD influences genetic differences in longer-term fitness across environments. Here, we tracked the population dynamics of two closely related strains of the halotolerant microalga Dunaliella salina following transfers across salinities. We showed that after a salinity increase, only one of these strains displayed a massive population decline (-69% in 1 h), largely attenuated by exposure to a PCD inhibitor. However, this decline was followed by a rapid demographic rebound, characterized by faster growth than the nondeclining strain, such that sharper decline was correlated with faster subsequent growth across experiments and conditions. Strikingly, the decline was more pronounced in conditions more favorable to growth (more light, more nutrients, less competition), further suggesting that it was not simply passive. We explored several hypotheses that could explain this decline-rebound pattern, which suggests that successive stresses could select for higher environmentally induced death in this system.

Parasitism and host dispersal plasticity in an aquatic model system.

Dispersal is a central determinant of spatial dynamics in communities and ecosystems, and various ecological factors can shape the evolution of constitutive and plastic dispersal behaviours. One important driver of dispersal plasticity is the biotic environment. Parasites, for example, influence the internal condition of infected hosts and define external patch quality. Thus, state-dependent dispersal may be determined by infection status and context-dependent dispersal by the abundance of infected hosts in the population. A prerequisite for such dispersal plasticity to evolve is a genetic basis on which natural selection can act. Using interconnected microcosms, we investigated dispersal in experimental populations of the freshwater protist Paramecium caudatum in response to the bacterial parasite Holospora undulata. For a collection of 20 natural host strains, we found substantial variation in constitutive dispersal and to a lesser degree in dispersal plasticity. First, infection tended to increase or decrease dispersal relative to uninfected controls, depending on strain identity, indicative of state-dependent dispersal plasticity. Infection additionally decreased host swimming speed compared to the uninfected counterparts. Second, for certain strains, there was a weak negative association between dispersal and infection prevalence, such that uninfected hosts dispersed less when infection was more frequent in the population, indicating context-dependent dispersal plasticity. Future experiments may test whether the observed differences in dispersal plasticity are sufficiently strong to be picked up by natural selection. The evolution of dispersal plasticity as a strategy to mitigate parasite effects spatially may have important implications for epidemiological dynamics.

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

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.