We report supramolecular quantum mechanics/molecular mechanics simulations on the peridinin-chlorophyll a protein (PCP) complex from the causative algal species of red tides. These calculations reproduce for the first time quantitatively the distinct peridinin absorptions, identify multichromophoric molecular excitations, and elucidate the mechanisms regulating the strongly allowed S0 (11Ag-) → S2 (11Bu+) absorptions of the bound peridinins that span a 58 nm spectral range in the region of maximal solar irradiance. We discovered that protein binding site-imposed conformations, local electrostatics, and electronic coupling contribute equally to the spectral inhomogeneity. Electronic coupling causes coherent excitations among the densely packed pigments. Complementary pairing of tuning mechanisms is the result of a competition between pigment-pigment and pigment-environment interactions. We found that the aqueous solvent works in concert with the charge distribution of PCP to produce a strong correlation between peridinin spectral bathochromism and the local dielectric environment.