How much power can be supplied over Beaglebone Black's USB?
The BBB uses a TPS2051 USB Power Switch. It limits the USB Host port power to 500mA on the high end. The power is drawn from the same system bus that powers the rest of the 5v parts, the 5v input port.

The BBB needs 1A for normal function + a low current usb device (keyboard, mouse, things that draw little current). Using a Cape or a high current USB device would require a power supply that can meet or exceed that extra current draw.