Hox genes in sea spiders (Pycnogonida) and the homology of arthropod head segments

Abstract

The pycnogonids (or sea spiders) are an enigmatic group of arthropods, classified in recent phylogenies as a sister-group of either euchelicerates (horseshoe crabs and arachnids), or all other extant arthropods. Because of their bizarre morpho-anatomy, homologies with other arthropod taxa have been difficult to assess. We review the main morphology-based hypotheses of correspondence between anterior segments of pycnogonids, arachnids and mandibulates. In an attempt to provide new relevant data to these controversial issues, we performed a PCR survey of Hox genes in two pycnogonid species, Endeis spinosa and Nymphon gracile, from which we could recover nine and six Hox genes, respectively. Phylogenetic analyses allowed to identify their orthology relationships. The Deformed gene from E. spinosa and the abdominal-A gene from N. gracile exhibit unusual sequence divergence in their homeodomains, which, in the latter case, may be correlated with the extreme reduction of the posterior region in pycnogonids. Expression patterns of two Hox genes (labial and Deformed) in the E. spinosa protonymphon larva are discussed. The anterior boundaries of their expression domains favour homology between sea spider chelifores, euchelicerates chelicerae and mandibulate (first) antennae, in contradistinction with previously proposed alternative schemes such as the protocerebral identity of sea spider chelifores or the absence of a deutocerebrum in chelicerates. In addition, while anatomical and embryological evidences suggest the possibility that the ovigers of sea spiders could be a duplicated pair of pedipalps, the Hox data support them as modified anterior walking legs, consistent with the classical views.

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Acknowledgements

We thank the Station Biologique de Roscoff for providing lab facilities for specimen collection and preparation. We are grateful to Jean Deutsch, Eric Quéinnec and Nicolas Rabet for advice and discussion, to Pierrette Lamarre for technical help, and to Thierry Jafredo for lab facilities. This work was founded by CNRS and the French Ministry of Research.

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Correspondence to Michaël Manuel.

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Guest editors Jean Deutsch and Gerhard Scholtz

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Fig. S1
figurea

Colossendeis bicincta, picture showing the proximal part of the proboscis and the anterior region of the cephalosoma, with the insertion of pedipalps (pd) and ovigers (ov) on a common basis (JPEG 183 kb)

Fig. S2
figureb

The position of Endeis and Nymphon in the pycnogonid tree derived from the combined analysis of 18S and 28S rDNA and morphological data (Arango 2003). The two species investigated in the present study, Endeis spinosa (male individual) and Nymphon gracile, are illustrated on the right side of the tree. cho chelifore, ov oviger, pd pedipalp (JPEG 284 kb)

Fig. S4
figured

Maximum Likelihood analysis of the 60-aa (homeodomain) Hox gene dataset. Genes from Endeis spinosa are labelled in red; genes from Nymphon gracile are labelled in blue. ML bootstraps (300 replicates) are indicated above the branches. The scale bar indicates the number of nucleotide substitutions per position in the sequences. LogL=−2262.20753, gamma shape=0.457, proportion of invariant sites=0.041 (JPEG 464 kb)

Fig S3

Amino-acid sequence alignment of pycnogonid Hox genes with representative genes from several panarthropods and other bilaterians, classified by groups of orthology. The alignment comprises, from left to right, eight positions of the hexapeptide region, six positions in the N-terminal region flanking the homeodomain, the 60 aa of the homeodomain, and ten positions in the C-terminal region flanking the homeodomain. Dashes indicate gaps inserted to align the sequences; blanks correspond to missing data. Black shading indicates amino-acid identity; grey shading indicate amino-acid similarity (for both, the threshold for shading was 40% of the sequences). In the homeodomain, helix 1 spans from position 10 to position 22, helix 2 from 28 to 37 and helix 3 from 42 to 58. Abbreviations of taxon names as in Fig. 3 (DOC 84 kb)

Table S1

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Manuel, M., Jager, M., Murienne, J. et al. Hox genes in sea spiders (Pycnogonida) and the homology of arthropod head segments. Dev Genes Evol 216, 481–491 (2006). https://doi.org/10.1007/s00427-006-0095-2

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Keywords

  • Arthropoda
  • Chelicerata
  • Development
  • Evolution
  • Homology
  • Hox genes
  • Pycnogonida
  • Segments