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Wing serial homologs and the origin and evolution of the insect wing
ARTICLE IN PRESS
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Zoology xxx (2013) xxx–xxx
Contents lists available at ScienceDirect
Zoology journal homepage: www.elsevier.com/locate/zool
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Invited Perspectives
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Wing serial homologs and the origin and evolution of the insect wing夽
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Takahiro Ohde, Toshinobu Yaginuma, Teruyuki Niimi ∗ Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan
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Article history: Received 6 November 2013 Accepted 11 November 2013 Available online xxx
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Keywords: Insect wing Serial homology Appendage evolution Hox gene
The origin and evolution of insect wings has been the subject of extensive debate. The issue has remained controversial largely because of the absence of definitive fossil evidence or direct developmental evidence of homology between wings and a putative wing origin. Recent identification of wing serial homologs (WSHs) has provided researchers with a potential strategy for identifying WSHs in other species. Future comparative developmental analyses between wings and WSHs may clarify the important steps underlying the evolution of insect wings. © 2013 The Authors. Published by Elsevier GmbH. All rights reserved.
Comparative analysis between serially homologous structures, both within and between species, has contributed significantly to our understanding of animal body plan evolution. Specifically, comparative developmental genetics has illustrated the evolutionary origin and diversification of the serially homologous ventral appendages of insects, such as walking legs, antennae and mouthparts (Shubin et al., 1997). In contrast, the origin and evolution of dorsal appendages is not as clear. The wing is a unique and novel insect trait. Compared to the limb-derived wings of birds and bats, the evolutionary origin of insect wings is not as obvious. After two centuries of discussion on the issue, two theories explaining the origin of insect wings have been proposed. One theory proposes that an articulated lateral organ, such as the stylus of bristletails or the tracheal gills of mayflies, is the origin of the wing (limb branch theory) (e.g., Wigglesworth, 1973). The other theory proposes that wings were originally derived from the paranotum, a de novo extension of the dorsolateral plate (paranotum theory) (e.g., Hamilton, 1971). Although both hypotheses have been appraised within the context of morphology, paleontology, and evolutionary biology, the origin of the insect wing is still an open question, largely for the following two reasons. First, a definitive fossil record of an insect with intermediate morphology, i.e. between non-winged and winged forms, has not been discovered. Second, there is no direct evidence of developmental
夽 This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited. ∗ Corresponding author. Tel.: +81 52 789 5504; fax: +81 52 789 4036. E-mail address: [email protected] (T. Niimi).
homology between wings and a putative wing origin. As studies of ventral appendages have shown, comparative molecular analyses of wings and their homologs would provide important information regarding the molecular basis of the origin and diversification of the wing and its derivatives. However, even the existence of a wing serial homolog (WSH) in modern insects has not yet been resolved. We recently proposed that the hypomeron of the prothorax and denticular outgrowths of the pupal abdomen of the mealworm beetle (Tenebrio molitor) are WSHs by demonstrating that these structures are both transformable and that they share a central developmental mechanism (Ohde et al., 2013; Fig. 1). More specifically, we demonstrated the transformation potential of a WSH into a wing in Hox RNAi beetles. Hox genes specify segment identity (Heffer and Pick, 2013). For example, the Hox gene Ultrabithorax (Ubx) regulates the development of the third thoracic segment in a variety of insect taxa (Heffer and Pick, 2013). In a Ubx mutant of the red flour beetle (Tribolium castaneum), the third thoracic dorsal appendage (i.e., a membranous wing) was observed to transform into a second thoracic dorsal appendage (i.e., an elytron-like structure) (Tomoyasu et al., 2005). Thus, if a structure on a segment without wings is transformed into a wing under Hox knockdown conditions, then the structure could be considered to correspond to the dorsal appendage of that segment. To clarify this hypothesis, we investigated the expression and function of vestigial and scalloped, which play a central role in Drosophila wing formation, in the putative WSHs of T. molitor. The findings showed that both genes are crucially important for both wing and WSH development, which suggests that both structures share a central developmental mechanism (Ohde et al., 2013). Taken together, we concluded that the WSHs of non-winged segments correspond to wings in this beetle. Given the conserved nature of Hox genes and the availability of RNAi techniques for insects, approaches similar to those described
0944-2006/$ – see front matter © 2013 The Authors. Published by Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.zool.2013.11.001
Please cite this article in press as: Ohde, T., et al., Wing serial homologs and the origin and evolution of the insect wing. Zoology (2013), http://dx.doi.org/10.1016/j.zool.2013.11.001
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ARTICLE IN PRESS T. Ohde et al. / Zoology xxx (2013) xxx–xxx
independently and repeatedly over time. However, it is possible that the latter may have occurred, because retention of a particular developmental gene network by a serial homolog could facilitate the reappearance of serial homologs in other segments through co-opting of that gene network. Indeed, derepression of abdominal proleg development, which shares some of the gene regulatory network associated with thoracic leg development, has been reported in taxonomically independent insect lineages (Nagy and Grbic, 1999). In order to elucidate the evolutionary history of WSHs, identification of these structures in different insect lineages is necessary. As studies on ventral appendages demonstrated, comparative developmental genetic analyses combined with an increase in the diversity of species surveyed would improve our understanding of the distinct developmental factors affecting wing and WSH development. Indeed, it is through such surveys that crucial developmental factor(s) responsible for evolving functional wings will be identified. Acknowledgements We thank Dr. Y. Ishikawa for critical reading of this manuscript. This study was supported by a Grant-in-Aid from the Japan Society for the Promotion of Science. Fig. 1. Simplified illustration showing the transformability and shared developmental mechanism of serial homologs. If the structure in segment B is serially homologous to the structure in segment A, it could be transformable if the Hox gene function is repressed (Hox off), even after development has been initiated (Hox on) (transformability). Serially homologous structures should share the same developmental mechanisms (e.g., cell fate determination, development initiation signal, or growth regulators) as the ancestral trait.
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here could be applied to the identification of WSHs in other insect taxa with relative ease. For example, a relationship between the wing and the posterior lateral terga of the prothoracic plate has been suggested based on functional analysis of the Hox gene, Sex combs reduced in the cockroach (Periplaneta americana) (Hrycaj et al., 2010). It is not known whether WSHs have been conserved over evolutionary time, or whether they have been lost and then developed
References Hamilton, K.G.A., 1971. The insect wing. I. Origin and development of wings from notal lobes. J. Kansas Entomol. Soc. 44, 421–433. Heffer, A., Pick, L., 2013. Conservation and variation in Hox genes: how insect models pioneered the evo-devo field. Annu. Rev. Entomol. 58, 161–179. ´ A., 2010. Functional analysis of Scr during embryonic Hrycaj, S., Chesebro, J., Popadic, and post-embryonic development in the cockroach, Periplaneta americana. Dev. Biol. 341, 324–334. Nagy, L.M., Grbic, M., 1999. Cell lineages in larval development and evolution of holometabolous insects. In: Hall, B.K., Wake, M.H. (Eds.), The Origin and Evolution of Larval Forms. Academic Press, San Diego, pp. 275–300. Ohde, T., Yaginuma, T., Niimi, T., 2013. Insect morphological diversification through the modification of wing serial homologs. Science 340, 495–498. Shubin, N., Tabin, C., Carroll, S., 1997. Fossils, genes and the evolution of animal limbs. Nature 388, 639–648. Tomoyasu, Y., Wheeler, S.R., Denell, R.E., 2005. Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433, 643–647. Wigglesworth, V., 1973. Evolution of insect wings and flight. Nature 246, 127–129.
Please cite this article in press as: Ohde, T., et al., Wing serial homologs and the origin and evolution of the insect wing. Zoology (2013), http://dx.doi.org/10.1016/j.zool.2013.11.001
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G Model ZOOL 25369 1–2
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Zoology xxx (2013) xxx–xxx
Contents lists available at ScienceDirect
Zoology journal homepage: www.elsevier.com/locate/zool
2
Invited Perspectives
3
Wing serial homologs and the origin and evolution of the insect wing夽
4 5
Q1
Takahiro Ohde, Toshinobu Yaginuma, Teruyuki Niimi ∗ Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan
6
7
a r t i c l e
i n f o
a b s t r a c t
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Article history: Received 6 November 2013 Accepted 11 November 2013 Available online xxx
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Keywords: Insect wing Serial homology Appendage evolution Hox gene
The origin and evolution of insect wings has been the subject of extensive debate. The issue has remained controversial largely because of the absence of definitive fossil evidence or direct developmental evidence of homology between wings and a putative wing origin. Recent identification of wing serial homologs (WSHs) has provided researchers with a potential strategy for identifying WSHs in other species. Future comparative developmental analyses between wings and WSHs may clarify the important steps underlying the evolution of insect wings. © 2013 The Authors. Published by Elsevier GmbH. All rights reserved.
Comparative analysis between serially homologous structures, both within and between species, has contributed significantly to our understanding of animal body plan evolution. Specifically, comparative developmental genetics has illustrated the evolutionary origin and diversification of the serially homologous ventral appendages of insects, such as walking legs, antennae and mouthparts (Shubin et al., 1997). In contrast, the origin and evolution of dorsal appendages is not as clear. The wing is a unique and novel insect trait. Compared to the limb-derived wings of birds and bats, the evolutionary origin of insect wings is not as obvious. After two centuries of discussion on the issue, two theories explaining the origin of insect wings have been proposed. One theory proposes that an articulated lateral organ, such as the stylus of bristletails or the tracheal gills of mayflies, is the origin of the wing (limb branch theory) (e.g., Wigglesworth, 1973). The other theory proposes that wings were originally derived from the paranotum, a de novo extension of the dorsolateral plate (paranotum theory) (e.g., Hamilton, 1971). Although both hypotheses have been appraised within the context of morphology, paleontology, and evolutionary biology, the origin of the insect wing is still an open question, largely for the following two reasons. First, a definitive fossil record of an insect with intermediate morphology, i.e. between non-winged and winged forms, has not been discovered. Second, there is no direct evidence of developmental
夽 This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited. ∗ Corresponding author. Tel.: +81 52 789 5504; fax: +81 52 789 4036. E-mail address: [email protected] (T. Niimi).
homology between wings and a putative wing origin. As studies of ventral appendages have shown, comparative molecular analyses of wings and their homologs would provide important information regarding the molecular basis of the origin and diversification of the wing and its derivatives. However, even the existence of a wing serial homolog (WSH) in modern insects has not yet been resolved. We recently proposed that the hypomeron of the prothorax and denticular outgrowths of the pupal abdomen of the mealworm beetle (Tenebrio molitor) are WSHs by demonstrating that these structures are both transformable and that they share a central developmental mechanism (Ohde et al., 2013; Fig. 1). More specifically, we demonstrated the transformation potential of a WSH into a wing in Hox RNAi beetles. Hox genes specify segment identity (Heffer and Pick, 2013). For example, the Hox gene Ultrabithorax (Ubx) regulates the development of the third thoracic segment in a variety of insect taxa (Heffer and Pick, 2013). In a Ubx mutant of the red flour beetle (Tribolium castaneum), the third thoracic dorsal appendage (i.e., a membranous wing) was observed to transform into a second thoracic dorsal appendage (i.e., an elytron-like structure) (Tomoyasu et al., 2005). Thus, if a structure on a segment without wings is transformed into a wing under Hox knockdown conditions, then the structure could be considered to correspond to the dorsal appendage of that segment. To clarify this hypothesis, we investigated the expression and function of vestigial and scalloped, which play a central role in Drosophila wing formation, in the putative WSHs of T. molitor. The findings showed that both genes are crucially important for both wing and WSH development, which suggests that both structures share a central developmental mechanism (Ohde et al., 2013). Taken together, we concluded that the WSHs of non-winged segments correspond to wings in this beetle. Given the conserved nature of Hox genes and the availability of RNAi techniques for insects, approaches similar to those described
0944-2006/$ – see front matter © 2013 The Authors. Published by Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.zool.2013.11.001
Please cite this article in press as: Ohde, T., et al., Wing serial homologs and the origin and evolution of the insect wing. Zoology (2013), http://dx.doi.org/10.1016/j.zool.2013.11.001
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ARTICLE IN PRESS T. Ohde et al. / Zoology xxx (2013) xxx–xxx
independently and repeatedly over time. However, it is possible that the latter may have occurred, because retention of a particular developmental gene network by a serial homolog could facilitate the reappearance of serial homologs in other segments through co-opting of that gene network. Indeed, derepression of abdominal proleg development, which shares some of the gene regulatory network associated with thoracic leg development, has been reported in taxonomically independent insect lineages (Nagy and Grbic, 1999). In order to elucidate the evolutionary history of WSHs, identification of these structures in different insect lineages is necessary. As studies on ventral appendages demonstrated, comparative developmental genetic analyses combined with an increase in the diversity of species surveyed would improve our understanding of the distinct developmental factors affecting wing and WSH development. Indeed, it is through such surveys that crucial developmental factor(s) responsible for evolving functional wings will be identified. Acknowledgements We thank Dr. Y. Ishikawa for critical reading of this manuscript. This study was supported by a Grant-in-Aid from the Japan Society for the Promotion of Science. Fig. 1. Simplified illustration showing the transformability and shared developmental mechanism of serial homologs. If the structure in segment B is serially homologous to the structure in segment A, it could be transformable if the Hox gene function is repressed (Hox off), even after development has been initiated (Hox on) (transformability). Serially homologous structures should share the same developmental mechanisms (e.g., cell fate determination, development initiation signal, or growth regulators) as the ancestral trait.
74 75 76 77 78 79 80
here could be applied to the identification of WSHs in other insect taxa with relative ease. For example, a relationship between the wing and the posterior lateral terga of the prothoracic plate has been suggested based on functional analysis of the Hox gene, Sex combs reduced in the cockroach (Periplaneta americana) (Hrycaj et al., 2010). It is not known whether WSHs have been conserved over evolutionary time, or whether they have been lost and then developed
References Hamilton, K.G.A., 1971. The insect wing. I. Origin and development of wings from notal lobes. J. Kansas Entomol. Soc. 44, 421–433. Heffer, A., Pick, L., 2013. Conservation and variation in Hox genes: how insect models pioneered the evo-devo field. Annu. Rev. Entomol. 58, 161–179. ´ A., 2010. Functional analysis of Scr during embryonic Hrycaj, S., Chesebro, J., Popadic, and post-embryonic development in the cockroach, Periplaneta americana. Dev. Biol. 341, 324–334. Nagy, L.M., Grbic, M., 1999. Cell lineages in larval development and evolution of holometabolous insects. In: Hall, B.K., Wake, M.H. (Eds.), The Origin and Evolution of Larval Forms. Academic Press, San Diego, pp. 275–300. Ohde, T., Yaginuma, T., Niimi, T., 2013. Insect morphological diversification through the modification of wing serial homologs. Science 340, 495–498. Shubin, N., Tabin, C., Carroll, S., 1997. Fossils, genes and the evolution of animal limbs. Nature 388, 639–648. Tomoyasu, Y., Wheeler, S.R., Denell, R.E., 2005. Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433, 643–647. Wigglesworth, V., 1973. Evolution of insect wings and flight. Nature 246, 127–129.
Please cite this article in press as: Ohde, T., et al., Wing serial homologs and the origin and evolution of the insect wing. Zoology (2013), http://dx.doi.org/10.1016/j.zool.2013.11.001
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