Turning up the heat: Symbiont-dependent insects and rising global temperatures

Bacterial symbionts protect insects against environmental stressors, including high temperatures. Paradoxically, high temperatures can also impair some symbionts, raising questions on the fates of symbiont-dependent insects under global climate change. To address this, we utilize the pea aphid, a cosmopolitan crop pest harboring a heat-sensitive, obligate Buchnera symbiont. This insect also harbors combinations of seven non-essential, protective bacterial symbionts. One such symbiont, Hamiltonella defensa, is proposed to defend against high temperatures that curtail Buchnera survival. To assess the robustness of this phenotype, we studied clonal pea aphid lines varying only in the presence/absence of variable Hamiltonella strains. We compared aphid fitness following three generations under stressful 30℃/19℃ and 33℃/16℃ day/night temperature regimes. Short 38℃ heat shock exposure was used as a second type of heat stress. While aphid genotype shaped symbiont-conferred fitness benefits, there was a strong effect of Hamiltonella strain, with two particular variants increasing population growth. These strains improved survival and fecundity under the same conditions, and were similarly protective under heat shock. Other Hamiltonella strains, including a close relative of a thermally protective variant, failed to boost fitness under hot conditions, suggesting thermal tolerance is not a ubiquitous benefit of harboring Hamiltonella. Intriguingly, one lab-protective Hamiltonella strain spread rapidly in the field during a 2012 warming event in southeastern Pennsylvania, revealing the real-world importance of our lab-studied protective phenotype. Heat-protective symbionts thus emerge as adaptive agents in a warming world, raising questions on their mechanisms of benefit and the drivers of this phenotype’s lability.