Advertisement

Development Genes and Evolution

, Volume 221, Issue 1, pp 17–27 | Cite as

Decapentaplegic (dpp) regulates the growth of a morphological novelty, beetle horns

  • Bethany R. WasikEmail author
  • Armin P. Moczek
Original Article

Abstract

Studies focusing on the development of morphological novelties suggest that patterning genes underlying traditional appendage development (i.e. mouthparts, legs, and wings) also play important roles in patterning novel morphological structures. In this study, we examine whether the expression and function of a member of the TGF-β signaling pathway, decapentaplegic (dpp), promotes development of a morphologically novel structure: beetle horns. Beetle horns are complex secondary sexual structures that develop in the head and/or prothorax, lack obvious homology to other insect outgrowths, and vary remarkably between species and sexes. We studied dpp expression through in situ hybridization, performed functional analyses with RNA interference, and gathered allometric measurements to determine the role of dpp during both pronotal and head horn development in both sexes of two morphologically dissimilar species in the Onthophagus genus, Onthophagus binodis and Onthophagus sagittarius. Our findings show that in addition to affecting growth and patterning of traditional appendages, dpp regulates beetle horn growth and remodeling.

Keywords

Decapentaplegic Horned beetles Novelty Onthophagus RNA interference Appendage patterning 

Notes

Acknowledgments

We would like to thank David Angelini for providing primer sequences, Franck Simonnet for mouthpart dissection and imaging, Justin Kumar for access to a NanoDrop 1000 Spectrophotometer, and the Center for Genomics and Bioinformatics at Indiana University for quantitative RT-PCR resources. We would also like to thank Erin Yoder for expert beetle care and Will Haines for collecting and sending O. sagittarius from the field. Finally, we thank Emilie Snell-Rood and Amy Cash for constructive feedback and helpful comments on earlier versions of these results. This research was carried out while BRW was supported through NIH Genetics Training Grant (2T32 GMOO7757-29) and NSF-IGERT Grant (DGE-0504627). Additional support was provided by NSF grants IOS 0445661 and IOS 0718522 to APM.

Supplementary material

427_2011_355_MOESM1_ESM.doc (1.4 mb)
ESM 1 (DOC 1,413 kb)

References

  1. Abu-Shaar M, Mann R (1998) Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development 125:3821–3830PubMedGoogle Scholar
  2. Affolter M, Basler K (2007) The Decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat Rev Genet 8:663–674PubMedCrossRefGoogle Scholar
  3. Arrow GJ (1951) Horned beetles, a study of the fantastic in nature. W. Junk, The HagueGoogle Scholar
  4. Barmina O, Kopp A (2007) Sex-specific expression of a HOX gene associated with rapid morphological evolution. Dev Biol 311:277–286PubMedCrossRefGoogle Scholar
  5. Bowsher J, Nijhout H (2009) Partial co-option of the appendage patterning pathway in the development of abdominal appendages in the sepsid fly Themira biloba. Dev Genes Evol 219:577–587PubMedCrossRefGoogle Scholar
  6. Brunetti CR, Selegue JE, Monteiro A, French V, Brakefield PM, Carroll SB (2001) The generation and diversification of butterfly eyespot color patterns. Curr Biol 11:1578–1585PubMedCrossRefGoogle Scholar
  7. Bryant P (1988) Localized cell death caused by mutations in a Drosophila gene coding for a transforming growth factor-beta homolog. Dev Biol 128:386–395PubMedCrossRefGoogle Scholar
  8. Campbell G, Weaver T, Tomlinson A (1993) Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74:1113–1123PubMedCrossRefGoogle Scholar
  9. Cappelli K, Felicetti M, Capomaccio S, Spinsanti G, Silvestrelli M, Supplizi A (2008) Exercise induced stress in horses: selection of the most stable reference genes for quantitative RT-PCR normalization. BMC Mol Biol 9:49PubMedCrossRefGoogle Scholar
  10. Diaz-Benjumea F, Cohen B, Cohen S (1994) Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372:175–179PubMedCrossRefGoogle Scholar
  11. Fritsch C, Lanfear R, Ray RP (2010) Rapid evolution of a novel signalling mechanism by concerted duplication and divergence of a BMP ligand and its extracellular modulators. Dev Genes Evol 220(9–10):235–250PubMedCrossRefGoogle Scholar
  12. Hulo N, Bairoch A, Bulliard V, Cerutti L, De Castro E, Langendijk-Genevaux P, Pagni M, Sigrist C (2006) The PROSITE database. Nucleic Acids Res 34:D227–D230PubMedCrossRefGoogle Scholar
  13. Jiang J, Struhl G (1996) Complementary and mutually exclusive activities of decapentaplegic and wingless organize axial patterning during Drosophila leg development. Cell 86:401–409PubMedCrossRefGoogle Scholar
  14. Kijimoto T, Andrews JR, Moczek AP (2010) Programmed cell death shapes the expression of horns within and between species of horned beetles. Evol Dev 12(5):449–458PubMedCrossRefGoogle Scholar
  15. Kingsley D (1994) The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev 8:133–146PubMedCrossRefGoogle Scholar
  16. Lecuit T, Cohen S (1997) Proximal–distal axis formation in the Drosophila leg. Nature 388:139–145PubMedCrossRefGoogle Scholar
  17. Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  18. Manjón C, Sánchez-Herrero E, Suzanne M (2007) Sharp boundaries of Dpp signalling trigger local cell death required for Drosophila leg morphogenesis. Nat Cell Biol 9:57–63PubMedCrossRefGoogle Scholar
  19. Moczek AP (2006) Pupal remodeling and the development and evolution of sexual dimorphism in horned beetles. Am Nat 168:711–729PubMedCrossRefGoogle Scholar
  20. Moczek AP, Nagy LM (2005) Diverse developmental mechanisms contribute to different levels of diversity in horned beetles. Evol Dev 7:175–185PubMedCrossRefGoogle Scholar
  21. Moczek AP, Rose DJ (2009) Differential recruitment of limb patterning genes during development and diversification of beetle horns. Proc Natl Acad Sci USA 106:8992–8997PubMedCrossRefGoogle Scholar
  22. Moczek AP, Rose D, Sewell W, Kesselring BR (2006) Conservation, innovation, and the evolution of horned beetle diversity. Dev Genes Evol 216:655–665PubMedCrossRefGoogle Scholar
  23. Rozen S, Skaletsky HJ (1998) Primer3. Available at: http://www-genome.wi.mit.edu/genome_software/other/primer3.html
  24. Schmittgen T, Livak K (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108PubMedCrossRefGoogle Scholar
  25. Schwank G, Basler K (2010) Regulation of organ growth by morphogen gradients. Cold Spring Harb Perspect Biol 2:a001669PubMedCrossRefGoogle Scholar
  26. Segal D, Gelbart W (1985) Shortvein, a new component of the decapentaplegic gene complex in Drosophila melanogaster. Genetics 109:119–143PubMedGoogle Scholar
  27. Shen J, Dahmann C (2005) Extrusion of cells with inappropriate Dpp signaling from Drosophila wing disc epithelia. Science 307:1789–1790PubMedCrossRefGoogle Scholar
  28. Simonnet F, Moczek AP (2011) Conservation and diversification of gene function during mouthpart development in Onthophagus beetles. Evol Dev (in press)Google Scholar
  29. Spencer F, Hoffmann F, Gelbart W (1982) Decapentaplegic: a gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28:451–461PubMedCrossRefGoogle Scholar
  30. St Johnston R, Hoffmann F, Blackman R, Segal D, Grimaila R, Padgett R, Irick H, Gelbart W (1990) Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev 4:1114–1127PubMedCrossRefGoogle Scholar
  31. Theisen H, Haerry T, O’Connor M, Marsh J (1996) Developmental territories created by mutual antagonism between Wingless and Decapentaplegic. Development 122:3939–3948PubMedGoogle Scholar
  32. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  33. Wasik BR, Rose DJ, Moczek AP (2010) Beetle horns are regulated by the Hox gene, Sex combs reduced, in a species- and sex-specific manner. Evol Dev 12:353–362PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA

Personalised recommendations