Emergent symbiont strains provide thermally robust protection against co-evolved and novel parasitoids of introduced pea aphids

Climate change and biological invasions pose synergistic threats; however, organisms may rapidly adapt through microbial symbiosis. We investigated how defensive symbionts in invasive pea aphids, Acyrthosiphon pisum, respond to emerging threats. Previously rare strains of the protective symbiont Hamiltonella defensa increased from <0.5% to 58% in aphid populations over just a few years. Bioassays revealed that these strains confer reciprocal, enemy-specific defences. One strain (C11) protected against Praon pequodorum, a native parasitoid that only began attacking pea aphids post-introduction, but provided no defence against the co-evolved parasitoid Aphidius ervi. Conversely, a closely related strain (C9) protected strongly against A. ervi but not P. pequodorum. When the Acyrthosiphon pisum secondary endosymbiont (APSE) bacteriophage was spontaneously lost from H. defensa C11 during cultivation, protection against P. pequodorum was completely eliminated, experimentally confirming the essential role of phage-encoded defences. Cultivation-assisted genomic analyses implicate divergent phage virulence cassettes in enemy-targeted defence, creating complementary protection portfolios within populations. The modular architecture of APSE phages enables rapid acquisition of novel capabilities through horizontal gene transfer. Critically, both strains maintained robust anti-parasitoid defence under simulated heat-wave conditions, in contrast to previous findings in which modest temperature increases disabled protection in other H. defensa strains. Our findings demonstrate the potential for heritable symbionts to provide rapid adaptive responses to anthropogenic stressors within ecological timescales, representing a widespread mechanism for host persistence under accelerating global change and having important implications for biological control and ecosystem management.