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Early Development and Diversity of Gryllus Appendages

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The Cricket as a Model Organism

Abstract

Among insects, orthopterans such as Gryllus bimaculatus display an extraordinary diversity regarding the arrangement and morphology of their appendages. In the head region, previous studies have shown that despite the superficial similarities in the morphology of mandibulate mouthparts between holometabolous and hemimetabolous species, the development of these appendages may be regulated in different ways. At present, a comprehensive analysis in any hemimetabolous mandibulate species is lacking; therefore studying the mouthparts in Gryllus will significantly improve the current understanding of the evolution of mouthparts in insects. Orthopteran wings are also quite distinct, featuring the hardened, leathery protective forewings (FWs) and the membranous flying hind wings (HWs). Furthermore, the FWs in Gryllus are characterized by a complex vein-intervein arrangement, similar to the ancestral hardened wings observed in fossils, providing a unique opportunity to understand the evolution of wing sclerotization in basal insects. Finally, orthopterans feature one of the best-known examples of appendage modification in insects – the presence of the greatly enlarged jumping hind leg. Studies of gene expression and functional analyses suggest that this enlargement is controlled by the Hox gene Ultrabithorax (Ubx), which acts as a “trigger” for differential leg growth. Furthermore, rather than acting on all genes in the leg development network, Ubx seems to selectively upregulate growth factors such as decapentaplegic (dpp) and Lowfat in Gryllus. Hence, cricket hind leg can serve as an exceptional model for combined studies of both tissue growth and segmental patterning during embryonic leg development. Overall, this review formulates a general framework that can be used for future studies on the development and diversification of insect appendages.

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References

  • Bando T, Hamada Y, Kurita K, Nakamura T, Mito T, Ohuchi H, Noji S (2011) Lowfat, a mammalian Lix1 homologue, regulates leg size and growth under the Dachsous/Fat signaling pathway during tissue regeneration. Dev Dyn 240(6):1440–1453. doi:10.1002/dvdy.22647

    Article  CAS  PubMed  Google Scholar 

  • Brown S, DeCamillis M, Gonzalez-Charneco K, Denell M, Beeman R, Nie W, Denell R (2000) Implications of the Tribolium Deformed mutant phenotype for the evolution of Hox gene function. Proc Natl Acad Sci U S A 97(9):4510–4514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chesebro J, Hrycaj S, Mahfooz N, Popadic A (2009) Diverging functions of Scr between embryonic and post-embryonic development in a hemimetabolous insect, Oncopeltus fasciatus. Dev Biol 329(1):142–151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curtis CD, Brisson JA, DeCamillis MA, Shippy TD, Brown SJ, Denell RE (2001) Molecular characterization of Cephalothorax, the Tribolium ortholog of Sex combs reduced. Genesis 30(1):12–20

    Article  CAS  PubMed  Google Scholar 

  • de Celis JF, Barrio R, Kafatos FC (1996) A gene complex acting downstream of dpp in Drosophila wing morphogenesis. Nature 381(6581):421–424. doi:10.1038/381421a0

    Article  PubMed  Google Scholar 

  • DeCamillis M, ffrench-Constant R (2003) Proboscipedia represses distal signaling in the embryonic gnathal limb fields of Tribolium castaneum. Dev Genes Evol 213(2):55–64. doi:10.1007/s00427-002-0291-7

    PubMed  Google Scholar 

  • DeCamillis MA, Lewis DL, Brown SJ, Beeman RW, Denell RE (2001) Interactions of the Tribolium Sex combs reduced and proboscipedia orthologs in embryonic labial development. Genetics 159(4):1643–1648

    CAS  PubMed  PubMed Central  Google Scholar 

  • Estella C, Voutev R, Mann RS (2012) A dynamic network of morphogens and transcription factors patterns the fly leg. Curr Top Dev Biol 98:173–198. doi:10.1016/B978-0-12-386499-4.00007-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamaratoglu F, de Lachapelle AM, Pyrowolakis G, Bergmann S, Affolter M (2011) Dpp signaling activity requires Pentagone to scale with tissue size in the growing Drosophila wing imaginal disc. PLoS Biol 9(10):e1001182. doi:10.1371/journal.pbio.1001182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hrycaj SM (2010) Unraveling the molecular mechanisms of insect diversity. Wayne State University, Detroit

    Google Scholar 

  • Hrycaj S, Chesebro J, Popadic A (2010) Functional analysis of Scr during embryonic and post-embryonic development in the cockroach, Periplaneta americana. Dev Biol 341(1):324–334. doi:10.1016/j.ydbio.2010.02.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huber F, Moore TE, Loher W (1989) Cricket behavior and neurobiology. Comstock Pub. Associates, Ithaca

    Google Scholar 

  • Hughes CL, Kaufman TC (2000) RNAi analysis of Deformed, proboscipedia and Sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the hemipteran head. Development 127(17):3683–3694

    CAS  PubMed  Google Scholar 

  • Inoue Y, Niwa N, Mito T, Ohuchi H, Yoshioka H, Noji S (2002) Expression patterns of hedgehog, wingless, and decapentaplegic during gut formation of Gryllus bimaculatus (cricket). Mech Dev 110(1–2):245–248

    Article  CAS  PubMed  Google Scholar 

  • Jockusch EL, Nulsen C, Newfeld SJ, Nagy LM (2000) Leg development in flies versus grasshoppers: differences in dpp expression do not lead to differences in the expression of downstream components of the leg patterning pathway. Development 127(8):1617–1626

    CAS  PubMed  Google Scholar 

  • Khila A, Abouheif E, Rowe L (2009) Evolution of a novel appendage ground plan in water striders is driven by changes in the Hox gene Ultrabithorax. PLoS Genet 5(7):e1000583. doi:10.1371/journal.pgen.1000583

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim J, Sebring A, Esch JJ, Kraus ME, Vorwerk K, Magee J, Carroll SB (1996) Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Nature 382(6587):133–138. doi:10.1038/382133a0

    Article  CAS  PubMed  Google Scholar 

  • Lecuit T, Cohen SM (1997) Proximal-distal axis formation in the Drosophila leg. Nature 388(6638):139–145. doi:10.1038/40563

    Article  CAS  PubMed  Google Scholar 

  • Mahfooz NS, Li H, Popadic A (2004) Differential expression patterns of the hox gene are associated with differential growth of insect hind legs. Proc Natl Acad Sci U S A 101(14):4877–4882. doi:10.1073/pnas.0401216101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahfooz N, Turchyn N, Mihajlovic M, Hrycaj S, Popadic A (2007) Ubx regulates differential enlargement and diversification of insect hind legs. PLoS One 2(9):e866. doi:10.1371/journal.pone.0000866

    Article  PubMed  PubMed Central  Google Scholar 

  • Manjon C, Sanchez-Herrero E, Suzanne M (2007) Sharp boundaries of Dpp signalling trigger local cell death required for Drosophila leg morphogenesis. Nat Cell Biol 9(1):57–63. doi:10.1038/ncb1518

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Arias A, Ingham PW, Scott MP, Akam ME (1987) The spatial and temporal deployment of Dfd and Scr transcripts throughout development of Drosophila. Development 100(4):673–683

    CAS  PubMed  Google Scholar 

  • Merrill VK, Turner FR, Kaufman TC (1987) A genetic and developmental analysis of mutations in the Deformed locus in Drosophila melanogaster. Dev Biol 122(2):379–395

    Article  CAS  PubMed  Google Scholar 

  • Montealegre ZF, Jonsson T, Robert D (2011) Sound radiation and wing mechanics in stridulating field crickets (Orthoptera: Gryllidae). J Exp Biol 214(Pt 12):2105–2117. doi:10.1242/jeb.056283

    Article  Google Scholar 

  • Morata G (2001) How Drosophila appendages develop. Nat Rev Mol Cell Biol 2(2):89–97. doi:10.1038/35052047

    Article  CAS  PubMed  Google Scholar 

  • Nakamura T, Mito T, Bando T, Ohuchi H, Noji S (2008a) Dissecting insect leg regeneration through RNA interference. Cell Mol Life Sci 65(1):64–72. doi:10.1007/s00018-007-7432-0

    Article  CAS  PubMed  Google Scholar 

  • Nakamura T, Mito T, Miyawaki K, Ohuchi H, Noji S (2008b) EGFR signaling is required for re-establishing the proximodistal axis during distal leg regeneration in the cricket Gryllus bimaculatus nymph. Dev Biol 319(1):46–55. doi:10.1016/j.ydbio.2008.04.002

    Article  CAS  PubMed  Google Scholar 

  • Neumann CJ, Cohen SM (1998) Boundary formation in Drosophila wing: Notch activity attenuated by the POU protein Nubbin. Science 281(5375):409–413

    Article  CAS  PubMed  Google Scholar 

  • Ng M, Diaz-Benjumea FJ, Vincent JP, Wu J, Cohen SM (1996) Specification of the wing by localized expression of wingless protein. Nature 381(6580):316–318. doi:10.1038/381316a0

    Article  CAS  PubMed  Google Scholar 

  • Niwa N, Inoue Y, Nozawa A, Saito M, Misumi Y, Ohuchi H, Yoshioka H, Noji S (2000) Correlation of diversity of leg morphology in Gryllus bimaculatus (cricket) with divergence in dpp expression pattern during leg development. Development 127(20):4373–4381

    CAS  PubMed  Google Scholar 

  • Passalacqua KD, Hrycaj S, Mahfooz N, Popadic A (2010) Evolving expression patterns of the homeotic gene Scr in insects. Int J Dev Biol 54(5):897–904. doi:10.1387/ijdb.082839kp

    Article  CAS  PubMed  Google Scholar 

  • Rentz DCF (1991) Orthoptera. In: CSIRO (ed) The insects of Australia, vol 1, 2nd edn. Melbourn University Press, Carlton, pp 369–393

    Google Scholar 

  • Rogers BT, Peterson MD, Kaufman TC (1997) Evolution of the insect body plan as revealed by the sex combs reduced expression pattern. Development 124(1):149–157

    CAS  PubMed  Google Scholar 

  • Rogers BT, Peterson MD, Kaufman TC (2002) The development and evolution of insect mouthparts as revealed by the expression patterns of gnathocephalic genes. Evol Dev 4(2):96–110

    Article  CAS  PubMed  Google Scholar 

  • Schwank G, Basler K (2010) Regulation of organ growth by morphogen gradients. Cold Spring Harb Perspect Biol 2(1):a001669. doi:10.1101/cshperspect.a001669

    Article  PubMed  PubMed Central  Google Scholar 

  • Shippy TD, Guo J, Brown SJ, Beeman RW, Denell RE (2000) Analysis of maxillopedia expression pattern and larval cuticular phenotype in wild-type and mutant tribolium. Genetics 155(2):721–731

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shippy TD, Rogers CD, Beeman RW, Brown SJ, Denell RE (2006) The Tribolium castaneum ortholog of Sex combs reduced controls dorsal ridge development. Genetics 174(1):297–307. doi:10.1534/genetics.106.058610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snodgrass RE (1930) Insects, their ways and means of living, vol 5, Smithsonian scientific series. Smithsonian Institution Series, New York

    Google Scholar 

  • Snodgrass RE (1993) Principles of insect morphology. Cornell University Press, Ithaca/New York

    Google Scholar 

  • Struhl G (1982) Genes controlling segmental specification in the Drosophila thorax. Proc Natl Acad Sci U S A 79(23):7380–7384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomoyasu Y, Wheeler SR, Denell RE (2005) Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433(7026):643–647. doi:10.1038/nature03272

    Article  CAS  PubMed  Google Scholar 

  • Tomoyasu Y, Arakane Y, Kramer KJ, Denell RE (2009) Repeated co-options of exoskeleton formation during wing-to-elytron evolution in beetles. Curr Biol 19(24):2057–2065. doi:10.1016/j.cub.2009.11.014

    Article  CAS  PubMed  Google Scholar 

  • Turchyn N (2010) The cellular and genetic mechanisms underlying the morphological diversity of insects. Wayne State University, Detroit

    Google Scholar 

  • Weatherbee SD, Halder G, Kim J, Hudson A, Carroll S (1998) Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Gene Dev 12(10):1474–1482. doi:10.1101/Gad.12.10.1474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weatherbee SD, Nijhout HF, Grunert LW, Halder G, Galant R, Selegue J, Carroll S (1999) Ultrabithorax function in butterfly wings and the evolution of insect wing patterns. Curr Biol 9(3):109–115

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Shinmyo Y, Mito T, Miyawaki K, Sarashina I, Ohuchi H, Noji S (2005) Expression patterns of the homeotic genes Scr, Antp, Ubx, and abd-A during embryogenesis of the cricket Gryllus bimaculatus. Gene Expr Patterns 5(4):491–502. doi:10.1016/j.modgep.2004.12.006

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Aleksandar Popadić .

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Liu, J., Popadić, A. (2017). Early Development and Diversity of Gryllus Appendages. In: Horch, H., Mito, T., Popadić, A., Ohuchi, H., Noji, S. (eds) The Cricket as a Model Organism. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56478-2_2

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