Abstract
Flying insects occupy both diurnal and nocturnal niches, and their visual systems encounter distinct challenges in both conditions. Visual adaptations, such as superposition eyes of moths, enhance sensitivity to low light levels but trade off with spatial and temporal resolution. Conversely, apposition eyes of butterflies enable high spatial resolution but are poorly sensitive in dim light. Although diel activity patterns of insects influence visual processing, their role in evolution of visual systems is relatively unexplored. Lepidopteran insects present an excellent system to study how diel activity patterns and phylogenetic position influence the visual transduction system. We addressed this question by comparing electroretinography measurements of temporal response profiles of diverse Lepidoptera to light stimuli that were flickering at different frequencies. Our data show that the eyes of diurnal butterflies are sensitive to visual stimuli of higher temporal frequencies than nocturnal moths. Hesperiid skippers, which are typically diurnal or crepuscular, exhibit intermediate phenotypes with peak sensitivity across broader frequency range. Across all groups, species within families exhibited similar phenotypes irrespective of diel activity. Thus, Lepidopteran photoreceptors may have diversified under phylogenetic constraints, and shifts in their sensitivity to higher temporal frequencies occurred concomitantly with the evolution of diurnal lifestyles.
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Abbreviations
- ERG:
-
Electroretinogram
- FFF:
-
Flicker fusion frequency
- CI:
-
Confidence interval
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Acknowledgements
We thank M. Kemparaju for help with lab-bred Daphnis specimens, Allan Francis Joy for help in sample collection and rearing of Macroglossum sp., G.S. Girish Kumar for help in sample collection, Tanvi Deora for comments on manuscript, members of the flight lab for general discussions, Krushnamegh Kunte for providing us with lab-bred butterflies, and Jahnavi Joshi and Krishnapriya Tamma for valuable input during manuscript preparation. We thank the two anonymous reviewers for their constructive comments.
Funding
Funding for this study was provided by grants from the Air Force Office of Scientific Research (AFOSR) # FA2386-11-1-4057 and # FA9550-16-1-0155, and National Centre for Biological Sciences (Tata Institute of Fundamental Research) to SPS. AK is funded by a Department of Science and Technology (DST) INSPIRE Faculty award and a Science and Engineering Board (SERB) Early Career Research Award from the Government of India.
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Conceived and designed the study: PC AK UM SPS. Standardized ERG recording protocol: AK. Designed data acquisition and analysis hardware and software: UM. Sampled Lepidoptera and performed experiments: PC AK. Analyzed data: PC UM. Interpreted data and wrote the manuscript: PC UM AK SPS.
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All experiments in this study were conducted in accordance with the guidelines and standards of an Institutional Animal Ethics Committee. None of the species sampled in this study are endangered or listed on national and international red lists or on the Wildlife Protection Act (1972), and were not sampled within a protected area.
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359_2020_1429_MOESM1_ESM.pdf
Supplementary Fig. 1 a Sample electroretinogram of Ariadne ariadne (Nymphalidae), showing on-transient and a negative ERG. b Sample electroretinogram of Gangara thyrsis (Hesperiidae), showing on and off transients and a weakly positive ERG. c A normalized temporal response profile of Ariadne ariadne (Nymphalidae). The response amplitude declined till 50 Hz and exhibited a peak at around 100 Hz. d, e Sample electroretinograms at 10 Hz and 50 Hz of Ariadne ariadne (Nymphalidae). The bottom panel shows zoomed in flicker responses at the two frequencies (PDF 984 kb)
359_2020_1429_MOESM2_ESM.pdf
Supplementary Fig. 2 a-d Raw temporal response profiles of four individuals of Daphnis nerii, without normalization, measured at various time-points of the day. These moths exhibited weak or undetectable secondary peaks, and were therefore not normalized for comparison as we did for the rest of the dataset. Note, however, that the broad shape of the temporal response profile did not change across times of the day, consistent with our findings from other moths. e Raw response profile of Udaspes folus (Hesperiidae), without normalization. This specimen also did not exhibit secondary peaks. We have not analyzed this response profile further (see text for further note) (PDF 379 kb)
359_2020_1429_MOESM3_ESM.pdf
Supplementary Fig. 3 Boxplots comparing FFF across families for two different thresholds. a FFF is computed with 1% threshold—same as in Fig. 3b. See legend of Fig. 3b for details. b FFF is computed with 5% threshold. FFFs of individuals sampled from the butterfly family Nymphalidae significantly differed from those sampled from the moth families, Sphingidae and Erebidae. FFF of Papilionidae significantly differed from Nymphalidae. (p<0.05, Kruskal–Wallis test followed by Nemenyi post-hoc comparison test. Chi-square statistic = 31.35, Sphingidae and Erebidae: n = 17 individuals, Hesperiidae: n = 6 individuals, Pieridae: n = 8 individuals, Nymphalidae: n = 17 individuals, Papilionidae: n = 12 individuals). c Boxplots comparing FFF of diurnal Sphingidae and nocturnal Sphingidae (First two columns) and crepuscular Nymphalidae and diurnal Nymphalidae (Last two columns). The FFF of diurnal Sphingids did not significantly differ from the nocturnal Sphingids (p>0.05, Wilcoxon rank-sum test, Diurnal Sphingids: n = 6 individuals, Nocturnal Sphingids: n = 9 individuals). The FFF of crepuscular Nymaphalids did not significantly differ from diurnal Nymphalids (p>0.05, Wilcoxon rank-sum test, Crepuscular Nymphalids: n = 7 individuals, Diurnal Nymphalids: n = 10 individuals). (PDF 148 kb)
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Chatterjee, P., Mohan, U., Krishnan, A. et al. Evolutionary constraints on flicker fusion frequency in Lepidoptera. J Comp Physiol A 206, 671–681 (2020). https://doi.org/10.1007/s00359-020-01429-3
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DOI: https://doi.org/10.1007/s00359-020-01429-3