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Those old cards aren't supported by Windows 10, and they do not use the same drivers as the R9 290 so they cannot be used together. Also, why can't you use an adapter for the 290 to get VGA output?
Granted, they are not supported, but nonetheless - windows should detect a device anyways and install a default driver for it. (EDIT) That is what AMD help says, and I am fine with it (/EDIT) Besides - behavior persists on both Windows 10 and 7 and on two boards. This leads me to suspect that those cards are at fault.
290 does not provide an analog output. The best I can do is to use a converter, which I actually already ordered. Converters tho seem to have rather bad reputation, so I'd prefer a native VGA.
This issue was bothering me for some time, so I did further experiments. I tried switching those cards with NVidia NVS300 and HD7450 and, for the sake of it, an USB controller.
Both X300 and X550 fail to even boot if they are not a primary adapter and are invisible even if the first slot is taken by an USB controller. On the flip side - both 7450 and NVS can work from any slot available.
Thusly I for the sake of google robots - x300 and x550 cannot be used anywhere except for the primary PCIE slot.