Environment-dependent evolution drives divergent adaptive strategies balancing parasite costs and competitive benefits

Prophages, phage genomes integrated into bacterial chromosomes, are widespread, yet how their costs to individual bacterial cells are balanced against benefits to the bacterial lineage remains poorly understood. This trade-off is particularly relevant in polymicrobial environments when prophage induction kills the host cell but releases phages that suppress competing bacteria. Here, to investigate how this conflict shapes bacterial and phage evolution, we experimentally evolved one polylysogenic strain in competition with a phage-sensitive strain across environmental conditions that modulate phage activity. By tracking bacterial growth and phage production over time, we uncover divergent, environment-dependent adaptive strategies consistent with a trade-off between direct costs of prophage activity and lineage-level (indirect) benefits of competitor suppression. At physiological levels of phage production, irrespective of the initial benefit, all populations evolved a 1,000-fold increase in phage production. However, under exacerbated phage production where induction imposed severe fitness costs, hosts purged prophages and adapted through accelerated bacterial growth. Phage production was negatively associated with bacterial yield, while competitive fitness showed a nonlinear relationship with phage production, with an optimum at intermediate-high phage activity. Whole-genome sequencing revealed that adaptation was accompanied by recurrent defects in cellular segmentation arising from mutations in the divisome and shifts in lysate composition, alongside the loss of plasmid-encoded antibiotic resistance genes. Together, our results reveal how resident genetic parasites can generate social trade-offs between the direct cost of prophage-induced death and the lineage-level competitive benefits. Our results provide a framework to study mobile genetic element dynamics within a kin selection mechanistic framework.