Photoreceptor optics of the honeybee and its eye colour mutants: the effect of screening pigments on the long-wave subsystem of colour vision

Abstract

With the aim of clarifying the role of screening pigments in photoreceptor optics of the compound eye, a comparative study of the optical properties of the honeybee eye in the visible region of the spectrum was carried out using wild-type bees and eye colour mutantssnow, snowlaranja, ivoryumberandchartreuse with total or partial blockage of the tryptophane-ommochrome pathway. 1. The electroretinogram (ERG) of mutant eyes displayed a sharp on-peak, this component being absent from normal heterozygote eyes (Fig. 6). 2. The ERG of newly emerged bees (a) lacked the above on-peak and showed oscillations in mutants, and (b) lacked the off-peak which always occurs in the ERG of adults in all the genotypes studied when stimulated by visible light. 3. The resting potentials of the receptor and cone cells were not found to be affected by mutationsla, and the receptor potential ins/s andsla/slaphotoreceptors appeared to be similar to that in +/+ 4. Analysis of the amplitude characteristics of the whole eye of eight genotypes showed that the relative numbers of photons absorbed from an extended light source (4.5°×16.5°) and needed to elicit a standard ERG amplitude of 1 mV were as follows:s/s∶iu/iu∶sla/sla∶ch1/ch1∶(+/+; s/+ iu/+; sla/+)=1∶4.3∶8.6∶12.2∶(100–250). These ratios are believed to reflect the progress in ommochrome formation in these strains. 5. Spectral sensitivity curves (SSC) were obtained using an automatic spectrosensitometer and a spectral scan method which gave accurate results. The SSC of the whole eye in+/+ peaked at aλmax of 543±7 nm (SD,n=6), whereasλmax ins/s andsla/slashifted to 528±6 nm (n=9) and 548 ±3nm (n=6) respectively. The SSC ins/+ was the same as that in+/+. The bandwidth (width at 50% of peak sensitivity) of the SSC proved to be similar in+/+ ands/+ (126±10 nm and 128±8 nm), although ins/s the SSC appeared to be significantly narrower (106±7 nm;P<0.01; Fig. 8, Table 2). 6. The peak spectral sensitivity of long-wave (LW) receptors lay at 541±5 nm (SD,n=14) in+/+ and at 526±5 nm (n=13) ins/s; the spectral distributions of the peaks in these genotypes were different. The bandwidth of the SSCs of the photoreceptors were 109±11 nm in+/+ and 103±4 nm ins/s, the difference being insignificant (Fig. 8, Table 2). The SSCs ins/s fit the absorption spectrum of pigment 526 (P 526) rather well whereas those in+/+ are noticeably distorted. The same is true for the whole-eye data. 7. A theory is advanced to account for the acceptance functions of the photoreceptors of eyes with imperfect pigmentation. Light scattering in imperfectly screened eyes was estimated using a factor which the termed we parasitic absorption coefficientp (see Theory). 8. The acceptance functions of LW photoreceptors were measured by three methods, and the results were similar to those predicted from the theory. On this basis the coefficientp was estimated; fors/s photoreceptors it lay between 0.65 and 0.76 according to experiments with a point light source (method 1), and was as great as 2.5 according to measurements with an extended light source (method 2). The latter technique, an integral method, made it possible to detect light scattering in normal bee eye, the coefficientp reaching 0.02 (Fig. 1, Table 3). 9. In genotypes+/+ andsla/slathe absorption spectra of screening pigments were recorded by microspectrophotometry (MSP), and greater transmission of red light than blue-green was found (Fig. 11). 10. Taking into account the screening effect of ommochromes, it is suggested that the visual pigment of LW photoreceptors in the honeybee eye is P 526; the absorption spectrum of this is highly similar to the SSC of LW photoreceptors in thes/s eye. 11. On the basis of our theory and experimental results, the contrast transfer function (CTF) for the white honeybee eye was estimated to be only 0.1 (for white and black patterns with the spatial wavelengthλsp≫Δρ, the acceptance angle). Thus, the absence of screening pigments from the compound eye ofsnow mutants causes the great decrease in image contrast, and this serious sensory defect may be responsible for the fact that these mutants fail to find their way home.