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Development Genes and Evolution

, Volume 224, Issue 2, pp 87–96 | Cite as

Expression of arthropod distal limb-patterning genes in the onychophoran Euperipatoides kanangrensis

  • Marta Bastos Oliveira
  • Simon Eckerström Liedholm
  • Jordi Estefa Lopez
  • Annalena A. Lochte
  • Magdalena Pazio
  • Jesus Pena Martin
  • Patrik Rödin Mörch
  • Seela Salakka
  • Julia York
  • Andrew Yoshimoto
  • Ralf JanssenEmail author
Original Article

Abstract

A current hypothesis states that the ancestral limb of arthropods is composed of only two segments. The proximal segment represents the main part of the modern leg, and the distal segment represents the tarsus and claw of the modern leg. If the distal part of the limb is an ancestral feature, one would expect conserved regulatory gene networks acting in distal limb development in all arthropods and possibly even their sister group, the onychophorans. We investigated the expression patterns of six genes known to function during insect distal limb development in the onychophoran Euperipatoides kanangrensis, i.e., clawless (cll), aristaless (al), spineless (ss), zinc finger homeodomain 2 (zfh2), rotund (rn), and Lim1. We find that all investigated genes are expressed in at least some of the onychophoran limbs. The expression patterns of most of these genes, however, display crucial differences to the known insect patterns. The results of this study question the hypothesis of conserved distal limb evolution in arthropods and highlight the need for further studies on arthropod limb development.

Keywords

Arthropod limb development Evolution Limb patterning 

Notes

Acknowledgments

The experiments were conducted during the “Evolution and Development” course at Uppsala University in the spring of 2013. We gratefully acknowledge the support of the New South Wales government Department of Environment and Climate Change by provision of a permit SL100159 to collect onychophorans at the Kanangra Boyd National Park and the Australian government Department of the Environment, Water, Heritage, and the Arts for export permits WT2009-4598 and WT2012-4704. The authors wish to thank Jean Joss, Rolf Ericsson, Robyn Stutchbury, and especially Noel Tait, for their help during onychophoran collection. Mattias Hogvall is thanked for his help as laboratory assistant. Nico Posnien and Alistair McGregor helped with the analysis of the embryonic transcriptome.

Supplementary material

427_2014_466_MOESM1_ESM.doc (36 kb)
ESM 1 (DOC 35 kb)
427_2014_466_MOESM2_ESM.doc (28 kb)
ESM 2 (DOC 27 kb)
427_2014_466_MOESM3_ESM.psd (4 mb)
Fig. S1 Alignments. Aligned are the conserved regions. For CLL, AL and LIM1 this is the HOMEODOMAINS; for RN this is the ZINC FINGER DOMAIN; for ZFH2 these are the three HOMEODOMAINS; for SS these are the two PAS domains. Dashes (-) indicate identical amino acids as in the onychophoran. Dots (.) indicate gaps in the alignment. Note the differences between the orthologs and other closely related genes. Abbreviations: Am, Apis mellifera (Insecta: Hymenoptera); Dm, Drosophila melanogaster (Insecta: Diptera); Dp, Daphnia pulex (Crustacea: Branchiopoda); Ek, Euperipatoides kanangrensis (Onychophora: Peripatopsidae); Gb, Gryllus bimaculatus (Insecta: Orthoptera); Gm, Glomeris marginata (Myriapoda: Diplopoda); Ma, Megaselia abdita (Insecta: Diptera); Nv, Nasonia vitripennis (Insecta: Hymenoptera); Tc, Tribolium castaneum (Insecta: Coleoptera). (PSD 4082 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Marta Bastos Oliveira
    • 2
  • Simon Eckerström Liedholm
    • 2
  • Jordi Estefa Lopez
    • 2
  • Annalena A. Lochte
    • 2
  • Magdalena Pazio
    • 2
  • Jesus Pena Martin
    • 2
  • Patrik Rödin Mörch
    • 2
  • Seela Salakka
    • 2
  • Julia York
    • 2
  • Andrew Yoshimoto
    • 2
  • Ralf Janssen
    • 1
    Email author
  1. 1.Department of Earth Sciences, PalaeobiologyUppsala UniversityUppsalaSweden
  2. 2.Uppsala UniversityUppsalaSweden

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