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.
This is a preview of subscription content, log in via an institution to check access.
References
Budd GE (2002) A palaeontological solution to the arthropod head problem. Nature 417:271–275
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 95:10665–10670
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 452:745–749
Eriksson BJ, Tait NN, Budd GE (2003) Head Development in the Onychophoran Euperipatoides kanangrensis With Particular Reference to the Central Nervous System. J Morphol 255:1–23
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 219:249–264
Hughes CL, Kaufman TC (2002) Hox genes and the evolution of the arthropod body plan. Evol Dev 4:459–499
Janssen R, Damen WGM (2006) The ten Hox genes of the millipede Glomeris marginata. Dev Genes Evol 216:451–465
Kimm MA, Prpic NM (2006) Formation of the arthropod labrum by fusion of paired and rotated limb-bud-like primordia. Zoomorphology 125:147–155
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 38:271–291
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 134:471–480
Papillon D, Telford MJ (2007) Evolution of Hox3 and ftz in arthropods: insights from the crustacean Daphnia pulex. Dev Genes Evol 217:315–322
Posnien NF, Bashasab, Bucher G (2009) The insect upper lip (labrum) is a nonsegmental appendage-like structure. Evol Dev 11:479–487
Scholtz G, Edgecombe GD (2006) The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Dev Genes Evol 216:395–415
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 135:169–196
Telford MJ, Thomas RH (1998) Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc Natl Acad Sci USA 95:10671–10675
Walker MH, Tait NN (2004) Studies of embryonic development and the reproductive cycle in ovoviviparous Australian Onychophora (Peripatopsidae). J Zool Lond 264:333–354
Acknowledgements
This work was funded by the Marie Curie Training Network ZOONET and BBSRC grant BBS/B/07519 to MEA. We thank Leyli Samadi (University of Vienna) for carrying out the phylogenetic analysis.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Roth
Electronic supplementary materials
Below is the link to the electronic supplementary material.
ESM 1
(PDF 351 kb)
Rights and permissions
About this article
Cite this article
Eriksson, B.J., Tait, N.N., Budd, G.E. et al. Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem. Dev Genes Evol 220, 117–122 (2010). https://doi.org/10.1007/s00427-010-0329-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-010-0329-1