The evolution of algal photosynthetic light harvesting is a complex story of theft and reinvention. Cryptophyte algae adapted their light-harvesting antenna from the cyanobacterial phycobilisome through several endosymbioses via an ancient red alga. The phycobilisome antenna proteins were stripped for spare parts and modified by the cryptophyte host to include host-derived subunits, forming a soluble protein-pigment heterodimer of dimers. The resulting antenna is a dense, protein-filled compartment sandwiched between two photosystem-containing membranes that convert captured solar energy into chemical potential. Cryptophyte antenna proteins are found in two quaternary states: an open form where the seam between the two dimers gives way to a solvent filled hole and a closed form which has no such feature. This opening of the seam is generated by a single amino acid insertion in the host-derived subunits and is associated with slower energy transfer between pigments. Based on spectral information, each cryptophyte was thought to have only one antenna protein, suggesting that any captured photon would diffuse isotropically between chromophore sites until it reaches a photosystem reaction centre. By solving four new crystal structures, we show that in the cryptophyte Hemiselmis andersenii, multiple different antenna proteins with diverse spectral characteristics tuned by the host-derived subunits are concurrently expressed. One of the structures shows a unique ‘super-open’ form, generated by the insertion of a large stabilising hairpin extension, suggesting an evolutionary push toward open form complexes. The diversity of structures and their spectral properties therefore alludes to an organised protein ultrastructure that generates an energetic funnel.