- Email: [email protected]
Origin and evolution of arthropod visual systems
Arthropod Structure & Development 35 (2006) 209e210 www.elsevier.com/locate/asd
Introduction
Origin and evolution of arthropod visual systems Since the much cited contribution by Paulus (1979) more than 25 years ago, the architecture of Euarthropod median and lateral eyes has been discussed in the context of their diagnostic potential for reconstructing plausible evolutionary scenarios (Paulus, 2000; Dohle, 2001; Bitsch and Bitsch, 2005). Together, these works demonstrate the importance of compound eye characters for gaining insights into arthropod phylogeny. Likewise, molecular and neuroanatomical research allows a deeper appreciation of how different groups might relate to each other. A case in point is that the Myriapoda have traditionally been accepted as the closest relatives of the Hexapoda. However, this view has undergone major revision due to recent molecular phylogenetics, based on RNA data or protein coding nuclear genes (Friedrich and Tautz, 1995; Regier et al., 2005; Mallat and Giribet, 2006), as well as on comparative neuroanatomical studies of arthropod nervous systems (Harzsch, 2006; Strausfeld, 2005). There is now agreement from molecular phylogenetics and ‘‘neurophylogeny’’ for inferring a close relationship of the Hexapoda and Crustacea or even a position of the Hexapoda within the Crustacea. The name ‘‘Tetraconata’’ has been suggested for such a taxon that embraces the hexapods and crustaceans (Dohle, 2001), referring to the tetrapartite crystalline cone of the ommatidia as a feature uniting both taxa. A surge of recent papers on the eye structure of chilopods (Mu¨ller et al., 2003; Mu¨ller and Meyer-Rochow, 2006a,b) further attest that research on the morphology and physiology of arthropod visual systems is an active and prosperous field of research (see, Warrant and Nilsson, 2006). At the same time, progress in dissecting genetic networks that govern eye development in various bilaterians and the evolutionary conservation of these molecular pathways (Gehring, 2004, 2005) is ever more relevant to phylogenetic approaches. For these and related reasons, the editors of Arthropod Structure and Development decided that a Special Issue on the topic ‘‘Origin and Evolution of Arthropod Visual Systems’’ would be timely, particularly if it integrated both morphological and molecular approaches to the study of evolution of arthropod lateral and median eyes and their associated central visual pathways. It is most gratifying that the response from those with whom this project was discussed was so positive, and offers of articles were so generous. Because of this response, the Editors have agreed to split the Special issue into two separate parts. Almost all of those colleagues that we invited to contribute agreed to do so and several manuscripts 1467-8039/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.asd.2006.10.001
were ‘‘added along the way’’, as are others being added for Part 2. Here, then, is Part 1 bringing together the first set of 10 papers. The second volume, which is scheduled to appear in mid 2007, will focus on the visual systems of Tardigrada, Chelicerata, Myriapoda, and stomatopod crustaceans. It will discuss topics such as the functional evolution of arthropod ommatidia and the evolution of brain neuropils associated with central visual pathways, such as central unpaired neuropils and structures referred to as accessory medulla. The present volume begins with a contribution by Purschke et al. that reviews current knowledge pertaining to photoreceptor organization in an arthropod outgroup, the Annelida, and points out similarities and differences of their visual systems in comparison to the Arthropoda. The next paper by Mayer presents new data on the eyes of the Onychophora, a taxon that in many respects may represent the ancestral character state of the Arthropoda. Mayer forwards the challenging hypothesis that onychophoran eyes are homologous to Euarthropodan median eyes, suggesting that lateral compound eyes are an apomorphy of Euarthropoda. Clarksson et al., introduces the eyes of trilobites as ‘‘the oldest preserved visual systems’’ and offers thoughtful insights into how elaborate those lateral eyes and their optic mechanisms were in a line of the Euarthropoda that finally went extinct at the end of the Permian era. In a paper on Limulus polyphemus, Battelle illustrates the eye structure and the architecture of the central visual pathway the Xiphosura, a taxon that may or may not be close relatives of the trilobites. The topic of median eyes is continued in the following contribution by Elofsson, who explores the morphological diversity of crustacean frontal eyes and provides a balanced discussion of homology versus parallelism of these structures within the Crustacea. Warrant et al. extend the motif of the ‘‘median eyes’’ to the Insecta by providing a detailed overview of the ocellar morphology of diurnal wasps and bees and discuss the amazing physiological performance of these structures. Continuing with the insects, Stavenga and Arikawa introduce us to color vision of butterflies and point out aspects of a possible coevolution between wing coloration and the physiology of color vision in this group of neopteran insects. This Special Issue then changes gears to discuss developmental aspects, with Harzsch and Hafner exploring eye development from trilobites across Xiphosurans and from Myriapods to insects and crustaceans, with considerations of relevant phylogenetic perspectives. In
210
Introduction / Arthropod Structure & Development 35 (2006) 209e210
a comparative study on several insect species, Liu et al. document major changes in the expression of the early patterning gene wingless correlated to changes in visual system development during the transition to the Holometabola. Friedrich then presents comprehensive information on comparative molecular aspects of the genetic pathways that govern visual system development in insects and traces these pathways to their deep origins in bilaterian evolution. Finally, Callaerts et al., in reviewing the role of Pax6 during eye development in Arthropoda, bring us closer to a specific and conserved molecular developmental network and also explore the evolutionary novelties of that network during arthropod diversification. This issue is the third so far published by this journal devoted to aspects of arthropod evolution, emphasizing the nervous system and receptor organization. It is perhaps salutatory that ninety years ago the Swedish comparative anatomist Nils Holmgren (1916) published his comprehensive monograph, in which he claimed that based on his observations of brain structures the arthropods must be viewed as monophyletic. Although phylogenetic inferences have been of central concern in this and previous special issues, there have also been guarded comparisons with brain organization in other Phyla. Such concerns have historical precedents. Indeed, Santiago Ramon y Cajal was explicit in his fascination by the similarities of neural organization underlying very different types of eyes, such as those of vertebrates and insects (Cajal, 1917). So it is perhaps worth quoting, in closing this Introduction, the following passage from a paper published in an 1893 issue of the Quarterly Journal of Microscopical Science by W. Patten on the nervous system of Limulus. The author wrote, ‘‘After we have torn off the deceptive Arthropod mask that disguises Limulus we discover that the nervous system, with its complex intricate modifications, shows, as a whole, a profound structural similarity to that of vertebrates’’. Amusing and perhaps a little overwrought, the passage is nevertheless useful in reminding us that in searching for principles of neural organization that cut across Phyla, arthropods are key players. References Bitsch, C., Bitsch, J., 2005. Evolution of eye structure and arthropod phylogeny. In: Koenemann, S. (Ed.), Crustaceans & Arthropod Relationships. CRC Press, Taylor & Francis Book Inc., New York, pp. 185e214. Cajal, S.R., 1917. Recuerdos de Mi Vida. (Recollections of My Life). Translated by E. Horne Craigie, 1936. Published 1937. The M.I.T. Press, Cambridge Massachusetts. Dohle, W., 2001. Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name
‘‘Tetraconata’’ for the monophyletic unit Crustacea þ Hexapoda. Annals de la Societe´ Entomologique de France (NS) 37, 85e103. Friedrich, M., Tautz, D., 1995. rDNA phylogeny of the major extant arthropod classes and the evolution of Myriapods. Nature 376, 165e167. Gehring, W.J., 2004. Historical perspective on the development and evolution of eyes and photoreceptors. International Journal of Developmental Biology, 707e717. Gehring, W.J., 2005. New perspectives on eye development and the evolution of eyes and photoreceptors. Journal of Heredity 96 (3), 171e184. Harzsch, S., 2006. Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phylogeny. Comparative and Integrative Biology 46, 162e194. Holmgren, N., 1916. Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. Koniglig Svenska Vetenskaps Akademiens Handlingar 56, 1e303. Mallat, J., Giribet, G., 2006. Further use of nearly complete 28s and 18s rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Molecular Phylogenetics and Evoluction 40, 772e794. Mu¨ller, C.H.G., Meyer-Rochow, V.B., 2006a. Fine structural description of the lateral ocellus of Craterostigmus tasmanianus Pocock, 1902 (Chilopoda: Craterostigmophora) and phylogenetic considerations. Journal of Morphology 267, 850e865. Mu¨ller, C.H.G., Meyer-Rochow, V.B., 2006b. Fine structural organization of the lateral ocelli in two species of Scolopendra (Chilopoda: Pleurostigmophora): an evolutionary evaluation. Zoomorphology 125, 13e26. Mu¨ller, C.H.G., Rosenberg, J., Richter, S., Meyer-Rochow, V.B., 2003. The compound eye of Scutigera coleoptrata (Linnaeus, 1758) (Chilopoda: Notostigmophora): an ultrastructural re-investigation that adds support to the Mandibulata-concept. Zoomorphology 122, 191e209. Paulus, H.F., 1979. Eye structure and the monophyly of the Arthropoda. In: Gupta, A.P. (Ed.), Arthropod Phylogeny. van Nostrand Reinhold Co., New York, pp. 299e383. Paulus, H.F., 2000. Phylogeny of the Myriapoda e Crustacea e Insecta: a new attempt using photoreceptor structure. Journal of Zoological Systematics and Evolutionary Research 38, 189e208. Regier, J.C., Shulz, J.W., Kambic, R.E., 2005. Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proceedings of the Royal Society of London, Series B 272, 395e401. Strausfeld, N.J., 2005. The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthropod Structure and Development 34, 235e256. Warrant, E.J., Nilsson, D.-E., 2006. Invertebrate Vision. Cambridge University Press, ISBN 9780521830881.
Steffen Harzsch* Roland Melzer Universitat Ulm, Sektion Biosystematische Dokumentation and Abteilung Neurobiologie, Fakultat F. Naturwissenschaften, Helmholtzstrasse 20, 89081 Ulm, Germany *Corresponding author. Tel.: þ49 731 50 31018; fax: þ49 731 50 31009. E-mail address: [email protected] (S. Harzsch)
Introduction
Origin and evolution of arthropod visual systems Since the much cited contribution by Paulus (1979) more than 25 years ago, the architecture of Euarthropod median and lateral eyes has been discussed in the context of their diagnostic potential for reconstructing plausible evolutionary scenarios (Paulus, 2000; Dohle, 2001; Bitsch and Bitsch, 2005). Together, these works demonstrate the importance of compound eye characters for gaining insights into arthropod phylogeny. Likewise, molecular and neuroanatomical research allows a deeper appreciation of how different groups might relate to each other. A case in point is that the Myriapoda have traditionally been accepted as the closest relatives of the Hexapoda. However, this view has undergone major revision due to recent molecular phylogenetics, based on RNA data or protein coding nuclear genes (Friedrich and Tautz, 1995; Regier et al., 2005; Mallat and Giribet, 2006), as well as on comparative neuroanatomical studies of arthropod nervous systems (Harzsch, 2006; Strausfeld, 2005). There is now agreement from molecular phylogenetics and ‘‘neurophylogeny’’ for inferring a close relationship of the Hexapoda and Crustacea or even a position of the Hexapoda within the Crustacea. The name ‘‘Tetraconata’’ has been suggested for such a taxon that embraces the hexapods and crustaceans (Dohle, 2001), referring to the tetrapartite crystalline cone of the ommatidia as a feature uniting both taxa. A surge of recent papers on the eye structure of chilopods (Mu¨ller et al., 2003; Mu¨ller and Meyer-Rochow, 2006a,b) further attest that research on the morphology and physiology of arthropod visual systems is an active and prosperous field of research (see, Warrant and Nilsson, 2006). At the same time, progress in dissecting genetic networks that govern eye development in various bilaterians and the evolutionary conservation of these molecular pathways (Gehring, 2004, 2005) is ever more relevant to phylogenetic approaches. For these and related reasons, the editors of Arthropod Structure and Development decided that a Special Issue on the topic ‘‘Origin and Evolution of Arthropod Visual Systems’’ would be timely, particularly if it integrated both morphological and molecular approaches to the study of evolution of arthropod lateral and median eyes and their associated central visual pathways. It is most gratifying that the response from those with whom this project was discussed was so positive, and offers of articles were so generous. Because of this response, the Editors have agreed to split the Special issue into two separate parts. Almost all of those colleagues that we invited to contribute agreed to do so and several manuscripts 1467-8039/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.asd.2006.10.001
were ‘‘added along the way’’, as are others being added for Part 2. Here, then, is Part 1 bringing together the first set of 10 papers. The second volume, which is scheduled to appear in mid 2007, will focus on the visual systems of Tardigrada, Chelicerata, Myriapoda, and stomatopod crustaceans. It will discuss topics such as the functional evolution of arthropod ommatidia and the evolution of brain neuropils associated with central visual pathways, such as central unpaired neuropils and structures referred to as accessory medulla. The present volume begins with a contribution by Purschke et al. that reviews current knowledge pertaining to photoreceptor organization in an arthropod outgroup, the Annelida, and points out similarities and differences of their visual systems in comparison to the Arthropoda. The next paper by Mayer presents new data on the eyes of the Onychophora, a taxon that in many respects may represent the ancestral character state of the Arthropoda. Mayer forwards the challenging hypothesis that onychophoran eyes are homologous to Euarthropodan median eyes, suggesting that lateral compound eyes are an apomorphy of Euarthropoda. Clarksson et al., introduces the eyes of trilobites as ‘‘the oldest preserved visual systems’’ and offers thoughtful insights into how elaborate those lateral eyes and their optic mechanisms were in a line of the Euarthropoda that finally went extinct at the end of the Permian era. In a paper on Limulus polyphemus, Battelle illustrates the eye structure and the architecture of the central visual pathway the Xiphosura, a taxon that may or may not be close relatives of the trilobites. The topic of median eyes is continued in the following contribution by Elofsson, who explores the morphological diversity of crustacean frontal eyes and provides a balanced discussion of homology versus parallelism of these structures within the Crustacea. Warrant et al. extend the motif of the ‘‘median eyes’’ to the Insecta by providing a detailed overview of the ocellar morphology of diurnal wasps and bees and discuss the amazing physiological performance of these structures. Continuing with the insects, Stavenga and Arikawa introduce us to color vision of butterflies and point out aspects of a possible coevolution between wing coloration and the physiology of color vision in this group of neopteran insects. This Special Issue then changes gears to discuss developmental aspects, with Harzsch and Hafner exploring eye development from trilobites across Xiphosurans and from Myriapods to insects and crustaceans, with considerations of relevant phylogenetic perspectives. In
210
Introduction / Arthropod Structure & Development 35 (2006) 209e210
a comparative study on several insect species, Liu et al. document major changes in the expression of the early patterning gene wingless correlated to changes in visual system development during the transition to the Holometabola. Friedrich then presents comprehensive information on comparative molecular aspects of the genetic pathways that govern visual system development in insects and traces these pathways to their deep origins in bilaterian evolution. Finally, Callaerts et al., in reviewing the role of Pax6 during eye development in Arthropoda, bring us closer to a specific and conserved molecular developmental network and also explore the evolutionary novelties of that network during arthropod diversification. This issue is the third so far published by this journal devoted to aspects of arthropod evolution, emphasizing the nervous system and receptor organization. It is perhaps salutatory that ninety years ago the Swedish comparative anatomist Nils Holmgren (1916) published his comprehensive monograph, in which he claimed that based on his observations of brain structures the arthropods must be viewed as monophyletic. Although phylogenetic inferences have been of central concern in this and previous special issues, there have also been guarded comparisons with brain organization in other Phyla. Such concerns have historical precedents. Indeed, Santiago Ramon y Cajal was explicit in his fascination by the similarities of neural organization underlying very different types of eyes, such as those of vertebrates and insects (Cajal, 1917). So it is perhaps worth quoting, in closing this Introduction, the following passage from a paper published in an 1893 issue of the Quarterly Journal of Microscopical Science by W. Patten on the nervous system of Limulus. The author wrote, ‘‘After we have torn off the deceptive Arthropod mask that disguises Limulus we discover that the nervous system, with its complex intricate modifications, shows, as a whole, a profound structural similarity to that of vertebrates’’. Amusing and perhaps a little overwrought, the passage is nevertheless useful in reminding us that in searching for principles of neural organization that cut across Phyla, arthropods are key players. References Bitsch, C., Bitsch, J., 2005. Evolution of eye structure and arthropod phylogeny. In: Koenemann, S. (Ed.), Crustaceans & Arthropod Relationships. CRC Press, Taylor & Francis Book Inc., New York, pp. 185e214. Cajal, S.R., 1917. Recuerdos de Mi Vida. (Recollections of My Life). Translated by E. Horne Craigie, 1936. Published 1937. The M.I.T. Press, Cambridge Massachusetts. Dohle, W., 2001. Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name
‘‘Tetraconata’’ for the monophyletic unit Crustacea þ Hexapoda. Annals de la Societe´ Entomologique de France (NS) 37, 85e103. Friedrich, M., Tautz, D., 1995. rDNA phylogeny of the major extant arthropod classes and the evolution of Myriapods. Nature 376, 165e167. Gehring, W.J., 2004. Historical perspective on the development and evolution of eyes and photoreceptors. International Journal of Developmental Biology, 707e717. Gehring, W.J., 2005. New perspectives on eye development and the evolution of eyes and photoreceptors. Journal of Heredity 96 (3), 171e184. Harzsch, S., 2006. Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phylogeny. Comparative and Integrative Biology 46, 162e194. Holmgren, N., 1916. Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. Koniglig Svenska Vetenskaps Akademiens Handlingar 56, 1e303. Mallat, J., Giribet, G., 2006. Further use of nearly complete 28s and 18s rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Molecular Phylogenetics and Evoluction 40, 772e794. Mu¨ller, C.H.G., Meyer-Rochow, V.B., 2006a. Fine structural description of the lateral ocellus of Craterostigmus tasmanianus Pocock, 1902 (Chilopoda: Craterostigmophora) and phylogenetic considerations. Journal of Morphology 267, 850e865. Mu¨ller, C.H.G., Meyer-Rochow, V.B., 2006b. Fine structural organization of the lateral ocelli in two species of Scolopendra (Chilopoda: Pleurostigmophora): an evolutionary evaluation. Zoomorphology 125, 13e26. Mu¨ller, C.H.G., Rosenberg, J., Richter, S., Meyer-Rochow, V.B., 2003. The compound eye of Scutigera coleoptrata (Linnaeus, 1758) (Chilopoda: Notostigmophora): an ultrastructural re-investigation that adds support to the Mandibulata-concept. Zoomorphology 122, 191e209. Paulus, H.F., 1979. Eye structure and the monophyly of the Arthropoda. In: Gupta, A.P. (Ed.), Arthropod Phylogeny. van Nostrand Reinhold Co., New York, pp. 299e383. Paulus, H.F., 2000. Phylogeny of the Myriapoda e Crustacea e Insecta: a new attempt using photoreceptor structure. Journal of Zoological Systematics and Evolutionary Research 38, 189e208. Regier, J.C., Shulz, J.W., Kambic, R.E., 2005. Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proceedings of the Royal Society of London, Series B 272, 395e401. Strausfeld, N.J., 2005. The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthropod Structure and Development 34, 235e256. Warrant, E.J., Nilsson, D.-E., 2006. Invertebrate Vision. Cambridge University Press, ISBN 9780521830881.
Steffen Harzsch* Roland Melzer Universitat Ulm, Sektion Biosystematische Dokumentation and Abteilung Neurobiologie, Fakultat F. Naturwissenschaften, Helmholtzstrasse 20, 89081 Ulm, Germany *Corresponding author. Tel.: þ49 731 50 31018; fax: þ49 731 50 31009. E-mail address: [email protected] (S. Harzsch)