Genotype, Maternal Effects, and Host Plant Collectively Influence Life‐History Strategies and Immune Competence in Pea Aphids

ABSTRACT Acyrthosiphon pisum exhibits pronounced host‐associated differentiation; however, the mechanistic basis by which “parental lineage × host plant” interactions shape offspring physiology and immune function remains poorly understood. Heat shock proteins (HSPs) maintain protein homeostasis under stress by facilitating protein folding and repair, whereas c‐Jun N‐terminal kinase ( JNK ) functions as a central signaling component in innate immunity. This study integrated the molecular responses of these pathways with key life‐history traits—including survival, development, reproduction, and hatching—to elucidate their respective roles and mechanisms under different parental and host contexts. Two green‐morph clones of A. pisum —the V clone (from Vicia sativa ) and the T clone (from Trifolium pratense )—were selected as the parental lines for this study. Four colonies were generated through reciprocal crosses (Voff: V♀ × V♂; TV: T♂ × V♀; VT: V♂ × T♀; Toff: T♀ × T♂), and we assessed the fitness‐related traits of the fertilized eggs, including HSP gene expression, hatching rate, and hatching time. Corresponding parthenogenetic lineages were also established. These clonal lineages were subsequently evaluated on three host plants ( V. sativa , V. faba , and T. pratense ). Fertilized egg assays revealed significant differences in HSP70 expression among colonies, and HSP70 expression had a significant positive effect on hatching rate but was not associated with hatching time. The Voff colony exhibited the highest HSP70 expression and hatching success, highlighting the pivotal role of maternal genotype in offspring developmental success. Results indicated that both colony and maternal origin significantly affected adult performance. Reciprocal cross offspring (TV) displayed the greatest 7‐day fecundity and hind‐leg length on V. sativa and V. faba , emphasizing genotype‐by‐host interactions. Immune challenges with Micrococcus luteus revealed lineage‐ and host‐dependent JNK transcription and post‐infection mortality. The TV line exhibited the strongest immune response on V. sativa and V. faba , while VT performed best on T. pratense . JNK expression had a significant positive effect on fecundity and a significant negative effect on mortality, linking immune activity with life‐history traits. These findings highlight (1) the critical role of maternal genotype in regulating offspring HSP expression and development, (2) the influence of genotype–host interactions on fitness, and (3) the association between JNK ‐mediated immunity and life‐history traits. This work advanced understanding of how parental lineage and host context jointly shape A. pisum fitness and provided a foundation for lineage‐specific biological control strategies.