Development Genes and Evolution

, Volume 220, Issue 3–4, pp 117–122 | Cite as

Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem

  • Bo Joakim Eriksson
  • Noel N. Tait
  • Graham E. Budd
  • Ralf Janssen
  • Michael Akam
Short Communication

Abstract

The arthropod head problem has puzzled zoologists for more than a century. The head of adult arthropods is a complex structure resulting from the modification, fusion and migration of an uncertain number of segments. In contrast, onychophorans, which are the probable sister group to the arthropods, have a rather simple head comprising three segments that are well defined during development, and give rise to the adult head with three pairs of appendages specialised for sensory and food capture/manipulative purposes. Based on the expression pattern of the anterior Hox genes labial, proboscipedia, Hox3 and Deformed, we show that the third of these onychophoran segments, bearing the slime papillae, can be correlated to the tritocerebrum, the most anterior Hox-expressing arthropod segment. This implies that both the onychophoran antennae and jaws are derived from a more anterior, Hox-free region corresponding to the proto and deutocerebrum of arthropods. Our data provide molecular support for the proposal that the onychophoran head possesses a well-developed appendage that corresponds to the anterior, apparently appendage-less region of the arthropod head.

Keywords

Onychophora Hox genes Head segmentation Arthropoda 

Supplementary material

427_2010_329_MOESM1_ESM.pdf (351 kb)
ESM 1(PDF 351 kb)

References

  1. Budd GE (2002) A palaeontological solution to the arthropod head problem. Nature 417:271–275CrossRefPubMedGoogle Scholar
  2. Damen WGM, Hausdorf M, Seyfarth E-A, Tautz DA (1998) Conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc Natl Acad Sci USA 95:10665–10670CrossRefPubMedGoogle Scholar
  3. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sorensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749CrossRefPubMedGoogle Scholar
  4. Eriksson BJ, Tait NN, Budd GE (2003) Head Development in the Onychophoran Euperipatoides kanangrensis With Particular Reference to the Central Nervous System. J Morphol 255:1–23CrossRefPubMedGoogle Scholar
  5. Eriksson BJ, Tait NN, Budd GE, Akam M (2009) The involvement of engrailed and wingless during segmentation in the onychophoran Euperipatoides kanangrensis (Peripatopsidae: Onychophora) (Reid 1996). Dev Genes Evol 219:249–264CrossRefPubMedGoogle Scholar
  6. Hughes CL, Kaufman TC (2002) Hox genes and the evolution of the arthropod body plan. Evol Dev 4:459–499CrossRefPubMedGoogle Scholar
  7. Janssen R, Damen WGM (2006) The ten Hox genes of the millipede Glomeris marginata. Dev Genes Evol 216:451–465CrossRefGoogle Scholar
  8. Kimm MA, Prpic NM (2006) Formation of the arthropod labrum by fusion of paired and rotated limb-bud-like primordia. Zoomorphology 125:147–155CrossRefGoogle Scholar
  9. Ma X, Hou X, Bergström J (2009) Morphology of Luolishania longicruris (Lower Cambrian, Chengjiang Lagerstätte, SW China) and the phylogenetic relationships within lobopodians. Arthropod Struct Dev 38:271–291CrossRefPubMedGoogle Scholar
  10. Mayer G, Koch M (2005) Ultrastructure and fate of the nephridial anlagen in the antennal segment of Epiperipatus biolleyi (Onychophora, Peripatidae)—evidence for the onychophoran antennae being modified legs. Arthropod Struct Dev 134:471–480CrossRefGoogle Scholar
  11. Papillon D, Telford MJ (2007) Evolution of Hox3 and ftz in arthropods: insights from the crustacean Daphnia pulex. Dev Genes Evol 217:315–322CrossRefPubMedGoogle Scholar
  12. Posnien NF, Bashasab, Bucher G (2009) The insect upper lip (labrum) is a nonsegmental appendage-like structure. Evol Dev 11:479–487CrossRefGoogle Scholar
  13. Scholtz G, Edgecombe GD (2006) The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Dev Genes Evol 216:395–415CrossRefPubMedGoogle Scholar
  14. Strausfeld NJ, Strausfeld MC, Stowe S, Rowell D, Loesel R (2006) The organization and evolutionary implications of neuropils and their neurons in the brain of the onychophorans Euperipatoides rowelli. Arthropod Struct Dev 135:169–196CrossRefGoogle Scholar
  15. Telford MJ, Thomas RH (1998) Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc Natl Acad Sci USA 95:10671–10675CrossRefPubMedGoogle Scholar
  16. Walker MH, Tait NN (2004) Studies of embryonic development and the reproductive cycle in ovoviviparous Australian Onychophora (Peripatopsidae). J Zool Lond 264:333–354CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Bo Joakim Eriksson
    • 1
    • 4
  • Noel N. Tait
    • 2
  • Graham E. Budd
    • 3
  • Ralf Janssen
    • 3
  • Michael Akam
    • 1
  1. 1.University Museum of Zoology and Department of ZoologyCambridgeUK
  2. 2.Department of Biological SciencesMacquarie UniversitySydneyAustralia
  3. 3.Dept Earth Sciences, PaleobiologyUppsala UniversityUppsalaSweden
  4. 4.School of Biological and Chemical SciencesQueen Mary University of LondonLondonUK

Personalised recommendations