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Chaos Knuckles is a natural evolution of Knuckles the Echidna. It was caused due to Knuckles' father Locke infusing Knuckles' egg with mass energy from a Chaos Emerald, which ultimately allowed Knuckles to evolve beyond the scale of any other Echidna.
Knuckles' eventual transformation into Chaos Knuckles was set in motion even before he was born. It began when the Ancient Walkers sent a dream to his father Locke, warning him of a future threat that Knuckles would have to face and would only survive if he was made into a superior Guardian to those who had come before. Resolving to do this, Locke performed experiments on himself to alter his DNA, hoping initially that he would be able to make himself into a stronger guardian and thus spare Knuckles the coming battle. Failing, he was forced to expose Knuckles' egg to the radiation of Angel Island's singular—at the time—Chaos Emerald. As a result, Knuckles became a mutant Echidna with abilities far beyond normal, even for a guardian. However, it would not be until Knuckles' teenage years that Chaos Knuckles was manifested.
Following the Quantum Beam's teleportation of all of Angel Island's inhabitants except for Knuckles to the Twilight Zone, Knuckles wound up on the surface in the company of Rob O' the Hedge, Amy Rose, Antoine D'Coolette, and Bunnie Rabbot in search of Antoine's roboticized father, the High Sheriff of Mercia. Finding him in Albion about to be disassembled, Knuckles intervened, inadvertently tapping into his direct connection to the Chaos Force to protect himself from harm. As a result, he began undergoing a transformation eerily similar to that made by his great-uncle Dimitri into the original Enerjak. This prompted Gala-Na, the head of Albion's executive council, to order his capture, but Chaos Knuckles teleported himself and his friends out of harm's way. Seeking help, he turned to Charmy Bee, the only member of the Chaotix not to be on Angel Island when the Quantum Beam hit. Knuckles' reunion with the Bee Prince lasted only a short time, though, when Nack the Weasel and his sister Nic the Weasel, in the employ of Gala-Na, arrived and had the Bees at gunshot to force Knuckles to accompany them to where Gala-Na and a team of Albion technicians and scientists waited.
Restrained and connected to the Chaos Siphon Suit developed by Dr. Finitevus, Chaos Knuckles began to have his powers painfully drained out of his body and released. Before the process got far, though, Charmy and his girlfriend Saffron intervened, disrupting the process. The resulting feedback reaction destroyed the Syphon Suit, increasing Chaos Knuckles' powers and turned Finitevus into a "photo-negative" of the Guardian. Maddened by the pain of his accelerated evolution, Chaos Knuckles fled to Angel Island. He was met there by none other than Miles "Tails" Prower, his friend and ally from Knothole who attempted to calm Knuckles down. Failing miserably, the Fox was beaten into unconsciousness and taken to his uncle, Merlin Prower, by Knuckles' great-grandfather Athair. The two soon had Tails back on his feet, and sent him to battle Knuckles after infusing him with the power needed to become Turbo Tails. However, their teleportation was interrupted by Mammoth Mogul, who replaced Tails with a duplicate and took the original to his new lair to drain energy from him to sustain himself. Knuckles did battle with the clone and soon achieved victory. Before he could finish the fight, however, Chaos Knuckles heard Julie-Su's voice, and flew of to investigate. He had an encounter with his deceased ancestor, Hawking, and a brief glimpse into the recent past of Angel Island.
Alliance with the Dark Legion
Finding Julie-Su in the clutches of the Dark Legion, Chaos Knuckles confronted Dimitri over the disappearance of Angel Island's inhabitants. Reassuring his volatile relative, Dimitri explained that a plan was already in place to bring the people back. The suicide attack on the Legion Battle Cruiser by Guardian Tobor, which Knuckles sensed, halted his attempt, and Dimitri turned to Knuckles for help. Knuckles learned that his evolution granted him the power to travel through time, and that there were three events in Echidna history that, if altered, could undo the Quantum Beam's effects and indeed reunify the Echidna people as if they never had been separated. Despite Julie-Su's protests, Knuckles agreed, travelling back in time first to prevent Angel Island's creation, only for the island to be destroyed as a result. Trying again by lowering Angel Island back to the surface, Knuckles succeeded only in destroying it by bringing it crashing to the surface. His worst mistake was in preventing the death of Edmund, the first Guardian, which would have led to all the Echidnas being roboticized and enslaved by Dr. Ivo Robotnik. Fortunately, Knuckles' instincts returned him to his own time before the changes made to the timeline could become permanent.
Despite their alliance, Dimitri and his great-great-granddaughter, Lien-Da, feared that Knuckles would turn against them and disrupt their plans. This fear was proven correct when Knuckles used his immense new powers to undo the Quantum Beam's effects by himself, restoring Angel Island's inhabitants. Knuckles, however, supported Dimitri's idea of reunifying the Echidna people, and thus vouched for him despite the opposition of such parties as Echidna Security Team Constable Remington and his own mother Lara-Le. Refuting such concerns, he attended a meeting between Dimitri and the Mitre of Echidnaopolis, and stepped in the way when a Dark Legion assassin hired by Lien-Da opened fire. Faking his own death, he tricked Dimitri into revealing his true dedication to the reunification. With this agreement seemingly cemented despite Dimitri's failing health, Knuckles felt comfortable in relaxing along with the returned Chaotix.
An old foe soon rose to bring and end to Chaos Knuckles' happiness; Mammoth Mogul, fresh from a battle with Sonic the Hedgehog and determined to obtain a new source of Chaos energy. Capturing Dimitri, Mogul threatened to kill him unless Knuckles surrendered himself to him. For unknown reasons, during a transmission of Mogul's demands Knuckles found himself revisiting a forgotten part of his past, in which he and his father had confronted Robians sent by Robotnik to attack Angel Island. Travelling in to meet Mogul alone, Chaos Knuckles confronted him briefly before Mogul sprung his trap, revealing that the room in which he was holding Dimitri, the very room he and Knuckles stood in, was a Chaos Syphon. Weakening rapidly, Knuckles called on his last resort, pushing his power past the ability of his body to endure. Remington, Lien-Da, the Chaotix, and the Dark Legion arrived shortly afterwards, finding the building Mogul had been hiding in reduced to rubble. They found Mogul himself gone, Dimitri alive, and Knuckles dead.
In truth, Knuckles had ascended to yet another higher state of being, and was present in spirit at his own funeral together with several other deceased members of the Brotherhood of Guardians. After speaking briefly with them, he was led to the Virtual Zone by Chao messengers of Aurora. She showed Knuckles details of his past, both remembered and forgotten, and told him of his duty to become one with the Chaos Force. Knuckles agreed, with the request that he be allowed to return to his normal red form. Achieving this, he joined the force, but separated himself from it and demanded to return to Mobius after seeing his friends battling the Xorda. Reluctantly, Aurora agreed, and Knuckles departed, only to arrive back home with his powers gone. Later, it would be revealed that they had been rendered dormant, and the power of the Master Emerald was enough to restore them.
EnerjakWhen coming into contact with Dr. Finitevus' hex, Knuckles briefly took on the form of Chaos Knuckles before fully transforming into Enerjak.
With a direct connection to the Chaos Force stronger than that of any other known living being, Chaos Knuckles possesses abilities beyond those of any previous Guardian and virtually any other wielder of such power.
Chaos Knuckles is functionally omnipotent, and has proved he had virtually unlimited reserves by overloading and destroying a device called a Chaos Syphon on two different occasions. In addition to the enhanced physical abilities, energy blasts, and teleportation abilities exhibited by his fellow Guardians and other wielders of Chaos energy, Chaos Knuckles could also travel in time, communicate with other Guardians living or dead across distances, warp reality to shape matter, as shown when he conjured a bouquet for Julie-Su seemingly out of thin air, heal, control minds, and manipulate Chaos energy to a much greater level and degree than had ever seen before.
- In the Light Mobius future, it is revealed that Knuckles has the potential to become Chaos Knuckles once again, as he did so in order to bring about Dr. Robotnik's final defeat along that timeline and tried to change Mobius into the utopia he had long envisioned. However, Sonic was able to stop him by using a device called the Nullifier, stopping Knuckles and costing him his right eye.
- Chaos Knuckles might reference the fact that when Sega was developing Sonic the Hedgehog 3, they were originally going to make Knuckles green instead of red.