AirDrop was originally implemented using Bonjour/Bluetooth PAN (personal area network). Newer versions (starting with OS X Yosemite and iOS 7) support an improved version that's built on Bluetooth LE (iOS) and Wi-Fi (iOS, OS X), but also support the older implementation – you just have to tell it to look for those.
So, when you click "Search for an Older Mac", AirDrop actually switches from the newer Bluetooth LE/Wi-Fi implementation to the older Bonjour/Bluetooth PAN combo. Since they are two different protocols, they don't (can't?) show at the same time.
This iMore article, as well as WikiPedia, have additional info.
Edit: It may be possible to show old Macs alongside newer ones if you set the
BrowseAllInterfaces system default to true. I haven't done this yet to confirm, but it may be the ticket.
Run this in Terminal:
# Enable AirDrop over Ethernet and on unsupported Macs running Lion
defaults write com.apple.NetworkBrowser BrowseAllInterfaces -bool true
My understanding is that this will allow AirDrop to run over Ethernet, but, more importantly, over Wi-Fi on technically unsupported (i.e. older) devices.