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James II was only 6 when he was crowned in 1437. Archibald, 5th Earl of Douglas, head of the grand and powerful Black Douglases was appointed Regent. When he died two years later, two men, Sir Alexander Livingstone and Sir William Crichton fought to take the place of the Douglases. They invited the new Earl of Douglas, then only 16 years old, to dine with his brother and a friend at Edinburgh Castle. At the end of the meal the head of a black bull was brought to the table, and at this sign all three were murdered.

This same William Crichton consolidated and extended the late 14th century tower into a Tower, Keep and Gatehouse. He also built the Collegiate Church about 500 yards East of the castle, as a place where daily orisons could be sung for the welfare of his soul. Towards the end the century further additions were made.Towards the end the century further additions were made; the area coloured black in the plan.

William, the Third Laird of Crichton, having conspired against James III in 1483, was besieged at Crichton Castle and forced to flee. King James gave the castle and its lands to his favourite, Sir John Ramsey, who he created Lord Bothwell. But he too became involved in treachery and so Crichton was given to Patrick Hepburn, Lord Hailes who became Earl Bothwell.

Later, on the 10th - 12th January 1562, Mary Queen of Scots was guest here at the marriage of her half-brother, Lord James Stewart to Lady Janet Hepburn. The celebration had been arranged at Crichton by the hot-headed James Hepburn, 4th Earl of Bothwell... and future husband of Queen Mary.

On Queen Mary and Bothwell's downfall in 1567, James VI gave Crichton to Francis, the child of James Stuart and Janet Hepburn, and in honour of her family name conferred on him the title of Bothwell. The new Earl of Bothwell, wild and dangerous, was described thus: "a terror to the most desperate duellists of Europe, and a subduer of the proudest champions, both Turks and Christians... the gasconades of France, the rhodomontades of Spain, the fanfaronades of Italy and braggadocio brags of all other countries"

Francis's frequent travels abroad brought him into contact with the flourishing of the European Renaissance, and in about 1585 he renovated Crichton in a stylish and up-to-date manner.

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