Visual adaptation of a biting fly that permanently foregoes flight

ABSTRACT Sensory systems are essential for behaviour, but energetically expensive. Selection favours accurate coding of pertinent stimuli and penalises excess functionality, but selective pressures can change over an organism's life. The dipteran superfamily Hippoboscoidea includes obligate blood-feeding flies with greatly varying ecologies, from fast-flying, free-living, visually oriented tsetse, to flightless, ectoparasitic, non-visual bat flies. Deer keds (Lipoptena andaluciensis, Diptera: Hippoboscidae) combine these lifestyles by flying to seek hosts based at least partly on vision, and then breaking off their wings to live as permanent ectoparasites. We use transcriptomics to understand evolutionary and developmental adaptations of the deer ked visual system to these dramatically varying selective pressures. We identified transcripts for five opsins, corresponding to the visual opsins of free-living tsetse. These included Rh1, Rh3, Rh5 and Rh6 of the compound eyes, comprising UV-, blue- and green-absorbing types serving colour and motion vision, and Rh2 of the ocelli, serving flight control. These opsins were still expressed in wingless, ectoparasitic adults but at significantly reduced levels, consistent with reduced investment in vision but not loss of any aspect of visual function. We speculate that limited plasticity in opsin expression may constrain visual adaptation to ectoparasitism, potentially imposing a long-term cost to foregoing flight.