<p>The Western honey bee (<i>Apis mellifera</i>) forms large colonies which represent organisms in their own right, known as superorganisms. Although this species is among the most extensively studied insects, competing explanations persist regarding fundamental characteristics like colonial lifespan. This review refutes the notion of colonial immortality due to an inverted identification of parent and offspring, advocating instead for viewing a traditional honey bee colony as a matrilineage of mortal superorganisms. By refining the colonial life cycle to trace zygotic, embryonic, fetal, juvenile, and adult stages during superorganismal ontogeny, we extend the animal-superorganism analogy to reveal a viviparous organism engaged in strictly sexual reproduction and complex maternal care. Furthermore, analyzing the multiple pathways to female reproduction indicates that swarming in itself does not represent reproduction, as it precedes fertilization. Under this framework, the prime swarm allows the maternal superorganism to survive reproduction, whereas afterswarms serve to multiply offspring within a single reproductive cycle. These insights have implications for honey bee parasitology, demographic monitoring, and beekeeping management and provide a more rigorous foundation for the superorganism concept applicable to sexually reproducing social insects with queen supersedure or turnover.</p>