In the airline where I work (CX) we rarely have two captains on one flight, if there are it is either due to a training flight or there was a roster disruption and all that was available was another captain. On long flights, we have four pilots, usually one captain, one relief command qualified first officer, another first officer (may or may not be relief qualified) and a second officer. The captain and one of the first officers (the non relief qualified one if there is one) will be rostered to operate. The second officer is a cruise pilot and only allowed in the seat above 20,000ft. If its a night flight we split the rest in half, so Captain and rostered to operate FO (if relief FO is landing critical he will do take off and ldg) will normally do take off and then choose the most suitable rest, ie first half or second half. Then SO and relief FO will jump in the seats, switching back again for the landing. Sometimes the rest is broken up differently. If both FOs are relief qualified any combination will work, FO sitting with FO, either FO sitting with SO or CN sitting with anyone. If only one FO is relief qualified he must be one of the people in the front when the CN is resting and the non relief qualified FO can not sit with the SO. CN always sits in the left, the guy acting as the relief FO always sits in the right.
The norm is CN flies one way and rostered to operate FO flies the other, if the other FO is landing critical he will take one of the sectors, sometimes one FO flies one way and the other FO gets the other sector. The SO never gets to fly
. There are no set rules as to who does the sector.
Every airline will have slight variances, I think SQ always has another CN to be relief for eg.