The somatic adaptability conferred by mutation accumulation in various tissues in Bombyx mori

Background The evolutionary success of organisms depends on resolving a fundamental conflict of maintaining germline genomic integrity for heritable stability while enabling somatic plasticity for environmental and developmental adaptation. Unfortunately, the molecular strategies governing this partitioning of genomic variation across tissues and life stages remain poorly understood. Results Here, we investigate this trade-off with the domesticated silkworm, Bombyx mori , by generating a high-quality parental genome and performing whole-genome resequencing on 121 F1 offspring across seven developmental stages and multiple tissues. In total, we identify 5,016 SNPs and 1,819 InDels, revealing a stark contrast in mutation landscapes, with an overall mutation rate of ~ 1×10⁻⁷ per site. Reproductive tissues maintain the lowest mutation burden, a finding mechanistically linked to the significant upregulation of DNA mismatch repair system components, ensuring germline fidelity. In contrast, somatic tissues such as the midgut exhibit higher mutational loads, facilitating environmental adaptation. Furthermore, we identified 909 genes affected by copy number variation (CNV), revealing a pivotal role for structural variation in developmental programming. CNV loss predominated (707 genes), peaking with 434 genes in L1 larvae associated with downregulating protein synthesis. Conversely, CNV gain was most prominent in L5 silk glands, in which amplification of the phosphatidylinositol-4,5-bisphosphate (PI(4,5)P2) 4-phosphatase gene cluster correlates with its transcriptional upregulation to drive programmed apoptosis during metamorphosis. Conclusions Our findings demonstrate that organisms actively orchestrate a dual genomic strategy: enhancing DNA repair to preserve the germline while co-opting programmed structural variations to dynamically regulate somatic development.