So-called telephone/telegraph lines carried multiple items. Of course, electric power was mounted at a higher level than communications lines.
As for the communications lines, in addition to company telegraph lines, additional lines were available for Western Union. As for company lines, there were separate circuits: tower-to-tower (Tower A could talk to Tower B without anyone else listening in), block station to block station (same privacy), a whole separate line running from the dispatcher to all locations under his control (enabling the dispatcher to talk to more than one tower if necessary), another line enabling call boxes to communicate with either the nearest tower, or the dispatcher, plus whatever other circuits the railroad might feel were appropriate to the territory.
On the New Haven Railroad (my employer in the mid-60s), telegraph had been replaced by telephone circa 1927 or so, but we still had the old crank-and-cuss phones. Call boxes out on the line had a switch enabling the user to either connect with the tower or connect with the dispatcher. The dispatcher contacted the towers via numbered rings (one short one long, two longs, etc.). Then Centrex came in and it was just like using a telephone, as long as you knew what number to dial.