Abstract
Adult stemmata are distinctive insect photoreceptors located on the posterior surfaces of the optic lobes. They originate as larval eyes that migrate inward during metamorphosis. We used a combination of light microscopy and in situ hybridization to examine their anatomical organization in the butterfly Vanessa cardui and to test for the presence of visual pigments, the light sensitive components of the visual transduction pathway. The bilateral cluster of six internal stemmata is located near the ventral edge of the lamina. They retain the dark screening pigment and overlying crystalline cones of the larval stemmata. We found two opsin mRNAs expressed in the stemmata that are also expressed, respectively, in UV-sensitive and green-sensitive photoreceptor cells in the compound eye. A third mRNA that is expressed in blue-sensitive photoreceptor cells of the compound eye was not expressed in the stemmata. Our results reinforce the idea that the adult stemmata are not merely developmental remnants of larval eyes, but remain functional, possibly as components of the circadian input channel.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Briscoe AD, Bernard GD, Szeto AS, Nagy LM, White RH (2003) Not all butterfly eyes are created equal: rhodopsin absorption spectrum, molecular identification, and localization of ultraviolet-, blue- and green-sensitive rhodopsin-encoding mRNAs in the retina of Vanessa cardui. J Comp Neurol 458:334–349
Felisberti F, Ventura DF (1996) Cerebral extraocular photoreceptors in ants. Tissue Cell 28:25–30
Felisberti F, Ventura DF, Hertel H (1997) Cerebral extraocular photoreceptors in beetles. Comp Biochem Physiol 118A:1353–1357
Fleissner G (1982) Isolation of an insect circadian clock. J Comp Physiol 149:311–316
Fleissner G, Fleissner G (2003) Nonvisual photoreceptors in arthropods with emphasis on their putative role as receptors of natural Zeitbeger stimuli. Chronobiol Int 20:593–616
Gilbert C (1994) Form and function of stemmata in larvae of holometabolous insects. Annu Rev Entomol 39:323–349
Hagberg M (1986) Ultrastructure and central projections of extraocular photoreceptors in caddisflies (Insecta Trichoptera). Cell Tissue Res 245:643–648
Harris MO, Foster SP, Bittar T, Ekanayake K, Looij K, Howard A (1995) Visual behaviour of neonate larvae of the light brown apple moth. Entomol Exp Appl 77:323–334
Ichikawa T (1991) Brain photoreceptors in the pupal and adult butterfly: fate of the lateral ocelli. Zoolog Sci (Tokyo) 8:471–476
Ichikawa T, Tateda H (1982) Distribution of color receptors in the larval eyes of four species of Lepidoptera. J Comp Physiol 149:317–324
Kitamoto J, Sakamoto K, Ozaki K, Mishina Y, Arikawa K (1998) Two visual pigments in a single photoreceptor cell: identification and histological localization of three mRNAs encoding visual pigment opsins in the retina of the butterfly Papilio xuthus. J Exp Biol 2001:1255–1261
Kitamoto J, Ozaki K, Arikawa K (2000) Ultraviolet and violet receptors express identical mRNA encoding an ultraviolet-absorbing opsin: identification and histological localization of two mRNAs encoding short wavelength-absorbing opsins in the retina of the butterfly Papilio xuthus. J Exp Biol 203:2887–2894
Malpel S, Klarsfeld A, Rouyer F (2002) Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. Development 129:1443–1453
Melzer Von RR, Paulus HF (1989) Evolutionswege zum Larvalauge der Insekten—Die Stemmata der hoeheren Dipteren und ihre Abwandlung zum Bolwig-Organ. Z Zool Syst Evolut-Forsch 27:200–245
Norlander RH, Edwards JS (1969) Postembryonic brain development in the Monarch butterfly, Danaus plexippus plexippus L, II: the optic lobes. Wilhelm Roux Archiv 163:197–220
Pollock JA, Benzer S (1988) Transcript localization of four opsin genes in the three visual organs of Drosophila: RH2 is ocellus specific. Nature 333:779–782
Regier D, Stanewsky R, Helfrich-Forster C (2003) Cryptochrome, compound eyes, Hofbauer–Buchner eyelets and ocelli play different roles in the entrainment and masking pathway of the locomotor activity rhythm in the fruit fly Drosophila melanogaster. J Biol Rhythms 18:377–391
Salcedo E, Huber A, Henrich S, Chadwell LV, Chou WH, Paulsen R, Britt SG (1999) Blue- and green-absorbing visual pigments of Drosophila: ectopic expression and physiological characterization of the R8 photoreceptor cell-specific Rh5 and Rh6 rhodopsin. J Neurosci 19:10716–10726
Schulz W-G, Schluter U, Seifert G (1984) Extraocular photoreceptors in the brain of Epilachna varivestis (Coleoptera: Coccinellidae). Cell Tissue Res 236:317–320
Seifert P, Smola U, Schinko I (1987) Internal extraocular photoreceptors in a dipteran insect. Tissue Cell 19:111–118
Strange PH (1961) The spectral sensitivity of Calliphora maggots. J Exp Biol 38:237–248
White RH, Xu H, Munch TA, Bennett RR, Grable EA (2003) The retina of Manduca sexta: rhodopsin expression, the mosaic of green-, blue- and UV-sensitive photoreceptors, and regional specialization. J Exp Biol 206:3337–3348
Yasuyama K, Meinertzhagen IA (1999) Extraretinal photoreceptors at the compound eye’s posterior margin in Drosophila melanogaster. J Comp Neurol 412:193–202
Acknowledgements
We thank Ivana Djuretic, Marilou Sison-Mangus, and Julia Stalleicken for technical assistance, and two anonymous reviewers for their comments.
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by grants from the National Science Foundation to A.D.B. (IBN-0346765) and R.H.W (IBN-9874493).
Rights and permissions
About this article
Cite this article
Briscoe, A.D., White, R.H. Adult stemmata of the butterfly Vanessa cardui express UV and green opsin mRNAs. Cell Tissue Res 319, 175–179 (2005). https://doi.org/10.1007/s00441-004-0994-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-004-0994-3