When enemies do not become friends: Experimental evolution of heat-stress adaptation in a vertically transmitted parasite

Abstract

Strict vertical (parent-to-offspring) transmission of symbionts may be associated with benevolence and mutualism, because host reproduction and symbiont transmission are linked. Nonetheless, many such symbionts do reduce host fitness costs and the factors driving their evolution are unclear. Using microcosm populations of Caedibacter taeniospiralis, a vertically transmitted bacterial symbiont of the protozoan Paramecium tetraurelia, we investigated evolutionary change under permissive conditions (26{degrees}C) and under heat stress (32{degrees}C), over 150 host generations. We found evidence for symbiont adaptation to heat stress, involving increased infection persistence and, consequently, higher rates of vertical transmission. For certain genetic backgrounds, heat-stress adaptation was associated with higher proliferation of infected lines at 26{degrees}C, suggesting cost-free evolution of super-generalists. Despite a general decrease in symbiont virulence relative to ancestral strains, infected evolved lines still showed substantial reductions (>20%) in population growth. There was no sign of a temperature-specific reduction in virulence or protection of the host against heat stress. Our results show that obligately vertically transmitted symbionts can still qualify as parasites and evolve adaptations that do not help their hosts. Long-term infection persistence might require additional mechanisms, such as the symbiont-mediated killer trait in this system, allowing the selective elimination of uninfected individuals in the population.