[en] The Australian lycaenid butterfly Jalmenus evagoras has iridescent wings that are sexually dimorphic, spectrally and in their degree of polarization, suggesting that these properties are likely to be important in mate recognition. We first describe the results of a field experiment showing that free-flying individuals of J. evagoras discriminate between visual stimuli that vary in polarization content in blue wavelengths but not in others. We then present detailed reflectance spectrophotometry measurements of the polarization content of male and female wings, showing that female wings exhibit blue-shifted reflectance, with a lower degree of polarization relative to male wings. Finally, we describe a novel method for measuring alignment of ommatidial arrays: by measuring variation of depolarized eyeshine intensity from patches of ommatidia as a function of eye rotation, we show that (a) individual rhabdoms contain mutually perpendicular microvilli; (b) many rhabdoms in the array have their microvilli misaligned with respect to neighboring rhabdoms by as much as 45 deg; and (c) the misaligned ommatidia are useful for robust polarization detection. By mapping the distribution of the ommatidial misalignments in eye patches of J. evagoras, we show that males and females exhibit differences in the extent to which ommatidia are aligned. Both the number of misaligned ommatidia suitable for robust polarization detection and the number of aligned ommatidia suitable for edge detection vary with respect to both sex and eye patch elevation. Thus, J. evagoras exhibits finely tuned ommatidial arrays suitable for perception of polarized signals, likely to match sex-specific life history differences in the utility of polarized signals.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Childers, Richard A Rabideau ; Department of Organismic & Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA ; Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA
Bernard, Gary D ; Department of Electrical & Computer Engineering, University of Washington, Seattle, WA 98195, USA
Huang, Heqing ; Department of Applied Physics & Applied Mathematics, Columbia University, New York, NY 10027, USA
Tsai, Cheng-Chia ; Department of Applied Physics & Applied Mathematics, Columbia University, New York, NY 10027, USA
Stoddard, Mary Caswell ; Department of Ecology & Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA
Hogan, Benedict G ; Department of Ecology & Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA
Greenwood, Joel S F ; Center for Brain Science, Harvard University, 52 Oxford St - room 331, Cambridge, MA 02138, USA ; Neurotechnology Core, Kavli Institute for Neuroscience, Yale University School of Medicine, New Haven, CT 06510, USA
Soucy, Edward R ; Center for Brain Science, Harvard University, 52 Oxford St - room 331, Cambridge, MA 02138, USA
Cornwall, Mark ; Department of Organismic & Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA ; Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA
Lim, Matthew Lek Min ; Department of Organismic & Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA ; Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA ; Department of Biological Sciences, National University of Singapore, 16 Science Drive 4, Singapore117558
Lienard, Marjorie ; Université de Liège - ULiège > GIGA > GIGA Molecular Biology of Diseases ; Department of Organismic & Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA ; The Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA ; Department of Biology, Lund University, 22362 Lund, Sweden
Yu, Nanfang ; Department of Applied Physics & Applied Mathematics, Columbia University, New York, NY 10027, USA
Pierce, Naomi E ; Department of Organismic & Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA ; Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA
NSF - National Science Foundation AFOSR - Air Force Office of Scientific Research Sverige Vetenskapsrådet
Funding text :
R.A.R.C. was supported by the Graduate Research Fellowship Program (GRFP) of the National Science Foundation (NSF). Research was supported by the National Science Foundation (PHY-1411445 awarded to N.Y. and N.E.P., CMMI-2005747 awarded to N.Y., DEB-1541560 awarded to N.E.P.), the Air Force Office of Scientific Research (FA9550-16-1-0322 through the Defense University Research Instrumentation Program awarded to N.Y.), and the Swedish Research Council (Vetenskapsrådet, VR 2020-0517) to M.A.L. Deposited in PMC for immediate release.We thank James Crall, Mark A. Elgar, Gabriel Miller, Gerard Talavera and Roger Kitching for their advice on different parts of the manuscript. Roger and Beverly Kitching hosted us at their home in Brisbane while we were preparing to conduct behavioral assays (not once, but twice after we were rained out the first time). Various computations in this paper were run on the FASRC Cannon cluster supported by the FAS Division of Science Research Computing Group at Harvard University. We thank the Wetmore-Colles Fund of the MCZ for supporting Open Access. R.A.R.C. was supported by the Graduate Research Fellowship Program (GRFP) of the National Science Foundation (NSF). Research was supported by the National Science Foundation (PHY-1411445 awarded to N.Y. and N.E.P., CMMI-2005747 awarded to N.Y., DEB-1541560 awarded to N.E.P.), the Air Force Office of Scientific Research (FA9550-16-1-0322 through the Defense University Research Instrumentation Program awarded to N.Y.), and the Swedish Research Council (Vetenskapsrådet, VR 2020-0517) to M.A.L. Deposited in PMC for immediate release.
Bates, D., Mächler, M., Bolker, B. and Walker, S. (2015). Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1-48. doi:10.18637/jss.v067.i01
Benjamini, Y. and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B (Methodological) 57, 289-300. doi:10.1111/j.2517-6161.1995.tb02031.x
Bernard, G. D. and Wehner, R. (1977). Functional similarities between polarization vision and color vision. Vision Res. 17, 1019-1028. doi:10.1016/0042-6989(77)90005-0
Boyd, G. (2012). Optical enhancement films. In Handbook of Visual Display Technology (ed. Chen Janglin, Cranton Wayne and Fihn Mark), pp. 1625-1646. Springer. Available at: https://doi.org/10.1007/978-3-540-79567-4_97.
Collyer, M. L. and Adams, D. C. (2018). RRPP: An r package for fitting linear models to high-dimensional data using residual randomization. Method. Ecol. Evol. 9, 1772-1779. doi:10.1111/2041-210X.13029
Daly, I. M., How, M. J., Partridge, J. C., Temple, S. E., Marshall, N. J., Cronin, T. W. and Roberts, N. W. (2016). Dynamic polarization vision in mantis shrimps. Nat. Commun. 7, 1-9. doi:10.1038/ncomms12140
Douglas, J. M., Cronin, T. W., Chiou, T.-H. and Dominy, N. J. (2007). Light habitats and the role of polarized iridescence in the sensory ecology of neotropical nymphalid butterflies (Lepidoptera: Nymphalidae). J. Exp. Biol. 210, 788-799. doi:10.1242/jeb.02713
Eastwood, R., Pierce, N. E., Kitching, R. L. and Hughes, J. M. (2006). Do ants enhance diversification in lycaenid butterflies? Phylogeographic evidence from a model myrmecophile, Jalmenus evagoras. Evolution Int. J. Org Evolution 60, 315-327. doi:10.1111/j.0014-3820.2006.tb01109.x
Elgar, M. A. and Pierce, N. E. (1988). Mating success and fecundity in an ant-tended lycaenid butterfly. In Reproductive Success: Studies of Selection and Adaptation in Contrasting Breeding Systems, 59-75. Chicago: Chicago University Press.
Fordyce, J., Nice, C. C., Forister, M. L. and Shapiro, A. M. (2002). The significance of wing pattern diversity in the Lycaenidae: mate discrimination by two recently diverged species. J. Evol. Biol. 15, 871-879. doi:10.1046/j.1420-9101.2002.00432.x
Fox, J. (2003). Effect displays in R for generalised linear models. J. Stat. Softw. 8, 1-27. doi:10.18637/jss.v008.i15
Halekoh, U. and Højsgaard, S. (2014). A Kenward-Roger approximation and parametric bootstrap methods for tests in linear mixed models-the R package pbkrtest. J. Stat. Softw. 59, 1-32. doi:10.18637/jss.v059.i09
Heinze, S. and Reppert, S. M. (2011). Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69, 345-358. doi:10.1016/j.neuron.2010. 12.025
How, M. J. and Marshall, N. J. (2014). Polarization distance: a framework for modelling object detection by polarization vision systems. Proc. R. Soc. B 281, 20131632. doi:10.1098/rspb.2013.1632
Hughes, L., Siew-Woon Chang, B., Wagner, D. and Pierce, N. E. (2000). Effects of mating history on ejaculate size, fecundity, longevity, and copulation duration in the ant-tended lycaenid butterfly, Jalmenus evagoras. Behav. Ecol. Sociobiol. 47, 119-128. doi:10.1007/s002650050002
Kelber, A. (1999). Ovipositing butterflies use a red receptor to see green. J. Exp. Biol. 202, 2619-2630. doi:10.1242/jeb.202.19.2619
Kelber, A., Thunell, C. and Arikawa, K. (2001). Polarisation-dependent colour vision in Papilio butterflies. J. Exp. Biol. 204, 2469-2480. doi:10.1242/jeb.204.14. 2469
Labhart, T. and Meyer, E. P. (1999). Detectors for polarized skylight in insects: A survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc. Res. Tech. 47, 368-379. doi:10.1002/(SICI)1097-0029(19991215)47:6<368::AID-JEMT2>3.0.CO;2-Q
Labhart, T., Baumann, F. and Bernard, G. D. (2009). Specialized ommatidia of the polarization-sensitive dorsal rim area in the eye of monarch butterflies have nonfunctional reflecting tapeta. Cell Tissue Res. 338, 391-400. doi:10.1007/s00441-009-0886-7
Maia, R., Gruson, H., Endler, J. A. and White, T. E. (2019). pavo 2: new tools for the spectral and spatial analysis of colour in R. Method. Ecol. Evol. 10, 1097-1107. doi:10.1111/2041-210X.13174
Maia, R., Eliason, C. M., Bitton, P.-P., Doucet, S. M. and Shawkey, M. D. (2013). pavo: an R package for the analysis, visualization and organization of spectral data. Method. Ecol. Evol. 4, 906-913. doi:10.1111/2041-210X.12069
Marshall, N. J., Powell, S. B., Cronin, T. W., Caldwell, R. L., Johnsen, S., Gruev, V., Chiou, T.-H. S., Roberts, N. W. and How, M. J. (2019). Polarisation signals: a new currency for communication. J. Exp. Biol. 222, 3. doi:10.1242/jeb. 134213
Matsushita, A., Stewart, F., Ilić, M., Chen, P.-J., Wakita, D., Miyazaki, N., Murata, K., Kinoshita, M., Belušič, G., Arikawa, K. et al. (2022). Connectome of the lamina reveals the circuit for early color processing in the visual pathway of a butterfly. Curr. Biol. 32, 2291-2299.e3. doi:10.1016/j.cub.2022.03.066
Nilsson, D.-E. and Howard, J. (1989). Intensity and polarization of the eyeshine in butterflies. J. Comp. Physiol. A 166, 51-56. doi:10.1007/BF00190209
Pellmyr, O. (1983). Plebeian courtship revisited: studies on the female-produced male behavior-eliciting signals in Lycaeides idas courtship (Lycaenidae). J. Res. Lepid. 21, 147-157. doi:10.5962/p.333793
Pierce, N., Kitching, R. L., Buckley, R. C., Taylor, M. F. J. and Benbow, K. F. (1987). The costs and benefits of cooperation between the Australian lycaenid butterfly, Jalmenus evagoras, and its attendant ants. Behav. Ecol. Sociobiol. 21, 237-248. doi:10.1007/BF00292505
Pierce, N. E. and Nash, D. R. (1999). The imperial blue, Jalmenus evagoras (Lycaenidae). Monogr. Aust. Lepid. 6, 279-315.
Rabideau Childers, R. (2023). Data for: A hypothesis for robust polarization vision: An example from the Australian Imperial Blue butterfly, Jalmenus evagoras. Dryad, Dataset. doi:10.5061/dryad.kprr4xh6t
Schneider, C. A., Rasband, W. S. and Eliceiri, K. W. (2012). NIH Image to ImageJ:
years of image analysis. Nat. Methods 9, 671-675. doi:10.1038/nmeth.2089
Srinivasan, M. (1994). Pattern recognition in the honeybee: recent progress.
J. Insect Physiol. 40, 183-194. doi:10.1016/0022-1910(94)90041-8
Stewart, F. J., Kinoshita, M. and Arikawa, K. (2019). Monopolatic motion vision in
the butterfly Papilio xuthus. J. Exp. Biol. 222, 1. doi:10.1242/jeb.191957
Stoddard, M. C. and Prum, R. O. (2008). Evolution of avian plumage color in a
tetrahedral color space: a phylogenetic analysis of new world buntings. Am. Nat.
171, 755-776. doi:10.1086/587526
Sweeney, A., Jiggins, C. and Johnsen, S. (2003). Polarized light as a butterfly mating signal. Nature 17, 2002-2003. doi:10.1038/423031a
Thévenaz, P., Ruttimann, U. E. and Unser, M. (1998). A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Proc. 7, 27-41. doi:10. 1109/83.650848
Vorobyev, M. and Osorio, D. (1998). Receptor noise as a determinant of colour thresholds. Proc. R. Soc. Lond. B Biol. Sci. 265, 351-358. doi:10.1098/rspb.1998. 0302
Waterman, T. H. (1981). Polarization sensitivity. In Handbook of Sensory Physiology, VII/6B (ed. H. Autrum), pp. 281-469. Springer-Verlag.
