DNA replication is a ubiquitous, complex, and conserved cellular process. However, regulation of DNA replication is only understood in a small fraction of organisms that poorly represent the diversity of genetic systems in nature. Here we used a combination of computational and experimental approaches to examine the function and evolution of one such system, the replication band (RB) in spirotrich ciliates, which is a localized, motile hub that traverses the macronucleus while replicating DNA. We show that the RB can take unique physical forms in different species, ranging from polar bands to a "replication envelope", where replication initiates at the nuclear periphery and advances centripetally inwards. Furthermore, we identified genes involved in cellular transport, including calcium transporters and cytoskeletal regulators, that are associated with the RB and may be involved in its function and translocation. These findings reveal the complex evolution and diversity of motile DNA replication systems and raise new possibilities regarding the regulation of nuclear organization and processes.

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