Abstract:  Aphids, a group of widely distributed piercing-sucking insects, rely on the symbiotic relationship with the primary endosymbiont Buchnera to acquire essential nutrients for survival and reproduction. During the long-term coevolution, aphids have developed specialized bacteriocytes to mediate nutrient exchange with Buchnera while avoiding immune activation. This intracellular symbiosis is maintained through vertical transmission dependent on endocytosis and exocytosis mechanisms, ensuring persistent infection of Buchnera within aphid populations. However, the stable nutrient supply in endosymbiotic environment leads to extensive genome degeneration in Buchnera. On the one hand, the systematic loss of genes related to redundant nutrient metabolism and environmental stress response has resulted in the loss of over 90% of the genes of Buchnera genomes, leading to drastic genome reduction. On the other hand, the physical barrier formed by bacteriocytes prevents Buchnera from acquiring new genes from external bacteria, at the same time, the absence of key genes involved in DNA repair leads to the loss of mutation repair ability. These factors collectively result in extreme AT content and continuous functional gene loss in the genome of Buchnera. The genomic degeneration of Buchnera compromises its metabolic functions, manifesting as reduced essential amino acid synthesis, loss of key genes involved in inorganic salt metabolism, and dysregulation of heat shock protein expression. These deficiencies accelerate aphid speciation and reduce their adaptability under heat stress. To compensate for these obligate symbiotic constraints, aphids employ strategies such as acquiring secondary symbionts or replacing primary symbionts. Some lineages have even evolved dual primary symbionts, alleviating adverse effect of genomic degradation through functional complementation. In this review, we summarized the evolutionary paradox in aphid-Buchnera symbiosis. Although the degeneration of Buchnera genome improved the efficiency of nutrient supply, it restricted the adaptation of aphid hosts to the environmental changes. We further proposed novel compensatory strategies developed by aphids to overcome obligate symbiotic constraints, offering new perspectives for understanding relationship between insects and endosymbionts, and laying theoretical foundations for aphid control strategies targeting symbionts.

Key words: Aphid, endosymbiont; Buchnera, genome degeneration, symbiosis, environmental adaptation