A yellow body-colour phenotype in the pea aphid is associated with enhanced heat-stress tolerance

Body-colour polymorphism is closely associated with fitness variation and environmental adaptation in insects, yet the genetic and physiological significance of rare colour morphs remains poorly characterized. During field surveys, we discovered a wild parthenogenetic yellow morph of the pea aphid, Acyrthosiphon pisum, and examined its inheritance pattern, fitness performance, and heat-stress physiology. Controlled crosses among yellow, deep-red, and green morphs showed that yellow coloration could not be fully explained by the classical single-locus red/green dominance model. Segregation patterns in selfed F₁ lineages were consistent with a two-locus recessive epistasis model, in which the inferred Y locus permits red/green pigmentation and homozygosity for the recessive y allele results in the yellow phenotype. Under control conditions, the yellow parental clone showed reduced fecundity, suggesting a potential fitness cost under non-stressful conditions. However, under heat stress, yellow-associated lineages consistently showed relatively low mortality. Notably, yellow F₂ segregants retained low heat-stress-induced mortality while exhibiting higher fecundity than the yellow parental clone, suggesting that the tolerance-fecundity trade-off may be partially decoupled through hybridization and recombination. When parental, selfed, and cross-derived yellow morphs were pooled and compared with additional wild-derived red and green reference lineages, the yellow group still showed the lowest mortality and the highest HSP70 and HSP83 expression under heat stress. These results suggest that the yellow phenotype may be associated with enhanced survival under heat stress and elevated heat-shock protein expression. Our findings reveal a previously underappreciated component of pea aphid colour polymorphism and provide new insights into the ecological significance of rare colour variants under thermal stress.