Development Genes and Evolution

, Volume 223, Issue 4, pp 247–251 | Cite as

The fate of the onychophoran antenna

Short Communication

Abstract

Recent gene expression data suggest that the region on which the onychophoran antenna is situated corresponds to the anteriormost, apparently appendage-less region of the arthropod head. The fate of the onychophoran antenna (or any appendage-like precursor), also called the primary antenna, has been discussed intensively, and there are conflicting suggestions that this anteriormost non-segmental appendage gave rise either to the arthropod labrum or, alternatively, to the so-called frontal filaments found in certain crustaceans. Our data on early axogenesis in anostracan crustaceans show that even in the earliest embryos, before the antennula and antennal nerves are developed, the circumoral anlagen of the brain display very prominent nerves which run into the frontal filament organ (also known as the cavity receptor organ). This situation resembles the development of the antennal nerves in onychophorans, which leads us to conclude that the frontal filaments are indeed homologous to the primary antenna. Frontal filaments also appear to be more common in crustaceans than previously thought, removing the need for a complicated scenario of transformation from a primary antenna into the labrum.

Keywords

Labrum Primary antenna Secondary antenna Frontal filament Organ of bellonci 

Notes

Acknowledgments

We would like to thank Martin Fritsch for the detailed discussions on the subject of frontal filament organs and the development of branchiopod nervous systems. We are grateful to Martin Schwentner who checked the species identity of A. franciscana by DNA barcoding. Lucy Cathrow improved the English which is gratefully acknowledged. Two anonymous reviewers provided helpful suggestions, which are also acknowledged.

References

  1. Andersson A (1977) The organ of Bellonci in ostracodes: an ultrastructural study of the rod-shaped, or frontal, organ. Acta Zool (Stockh) 58:197–204CrossRefGoogle Scholar
  2. Benesch R (1969) Zur Ontogenie und Morphologie von Artemia salina L. Zool Jb Abt Anat Ont 86:307–458Google Scholar
  3. Brenneis G, Arango CP, Scholtz G (2011) Morphogenesis of Pseudopallene sp. (Pycnogonida, Callipallenidae) I: embryonic development. Dev Genes Evol 221:309–328PubMedCrossRefGoogle Scholar
  4. Dunn CW, Hejnol A, Matus DQ et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749PubMedCrossRefGoogle Scholar
  5. Elofsson R (1971) The ultrastructure of a chemoreceptore organ in the head of copepod crustaceans. Acta Zool 52:200–315Google Scholar
  6. Elofsson R, Lake PS (1971) On the cavity receptor organ (X-organ or organ of Bellonci) of Artemia salina (Crustacea: Anostraca). Z Zellforsch Mikrosk Anat 326:319–326CrossRefGoogle Scholar
  7. Eriksson BJ, Budd GE (2000) Onychophoran cephalic nerves and their bearing on our understanding of head segmentation and stem-group evolution of Arthropoda. Arthropod Struct Dev 2ß:197–209Google Scholar
  8. Eriksson BJ, Tait NN, Budd GE (2003) Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system. J Morphol 255:1–23PubMedCrossRefGoogle Scholar
  9. Eriksson BJ, Tait NN, Budd GE et al (2010) Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem. Dev Genes Evol 220:117–122PubMedCrossRefGoogle Scholar
  10. Fritsch M, Richter S (2010) The formation of the nervous system during larval development in Triops cancriformis (Bosc) (Crustacea, Branchiopoda): an immunohistochemical survey. J Morphol 271:1457–1481PubMedCrossRefGoogle Scholar
  11. Fritsch M, Kaji T, Olesen J, Richter S (2013) Development of the nervous system in Laevicaudata (Crustacea, Branchiopoda): insights into the evolution and homologies of branchiopod limbs and “frontal organs”. Zoomorphology. doi:10.1007/s00435-012-0173-0
  12. Kimm MA, Prpic N-M (2006) Formation of the arthropod labrum by fusion of paired and rotated limb-bud-like primordia. Zoomorphology 125:147–155CrossRefGoogle Scholar
  13. Maas A, Waloszek D, Müller KJ (2003) Morphology, ontogeny and phylogeny of the Phosphatocopina (Crustacea) from the Upper Cambrian “Orsten” of Sweden. Fossils & Strata 49:1–239Google Scholar
  14. Mayer G, Whitington PM, Sunnucks P, Pflüger H-J (2010) A revision of brain composition in Onychophora (velvet worms) suggests that the tritocerebrum evolved in arthropods. BMC Evol Biol 10:255PubMedCrossRefGoogle Scholar
  15. Mittmann B, Wolff C (2012) Embryonic development and staging of the cobweb spider Parasteatoda tepidariorum C. L. Koch, 1841 (syn.: Achaearanea tepidariorum; Araneomorphae; Theridiidae). Dev Genes Evol 222:189–216PubMedCrossRefGoogle Scholar
  16. Møller OS, Olesen J, Høeg JT (2004) On the larval development of Eubranchipus grubii (Crustacea, Branchiopoda, Anostraca) with notes on the basal phylogeny of the Branchiopoda. Zoomorphology 123:107–123Google Scholar
  17. Panganiban G, Sebring A, Nagy L, Carroll S (1995) The development of crustacean limbs and the evolution of arthropods. Science 270:1363–1366PubMedCrossRefGoogle Scholar
  18. Patel NH (1994) Imaging neuronal subsets and other cell types in whole mount Drosophila embryos and larvae using antibody probes. In: Fryberg EA, Goldstein LSB (eds) Drosophila melanogaster: practical uses in cell and molecular biology. Academic press, San Diego, pp 446–488Google Scholar
  19. Popadíc A, Panganiban G, Rusch D et al (1998) Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Dev Genes Evol 208:142–150PubMedCrossRefGoogle Scholar
  20. Posnien N, Bashasab F, Bucher G (2009) The insect upper lip (labrum) is a nonsegmental appendage-like structure. Evol Dev 11:480–488PubMedCrossRefGoogle Scholar
  21. Raineri M, Falugi C (1983) Acetylcholinesterase activity in embryonic and larval development of Artemia salina Leach (Crustacea Phyllopoda). J Exp Zool 246:229–246CrossRefGoogle Scholar
  22. Regier J, Shultz J, Zwick A, Hussey A, Ball B, Wetzer R, Martin JW, Cunningham CW (2010) Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463:1079–1083Google Scholar
  23. Scholtz G, Edgecombe GD (2006) The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Dev Genes Evol 216:395–415PubMedCrossRefGoogle Scholar
  24. Semmler H, Wanninger A, Høeg JT, Scholtz G (2008) Immunocytochemical studies on the naupliar nervous system of Balanus improvisus (Crustacea, Cirripedia, Thecostraca). Arthropod Struct Dev 37:383–395PubMedCrossRefGoogle Scholar
  25. Sorgeloos P, Bossuyt E, Laviña E (1977) Decapsulation of Artemia cysts: a simple technique for the improvement of the use of brine shrimp in aquaculture. Aquaculture 12:311–315CrossRefGoogle Scholar
  26. Steinmetz PRH, Urbach R, Posnien N et al (2010) Six3 demarcates the anterior-most developing brain region in bilaterian animals. EvoDevo 1:14PubMedCrossRefGoogle Scholar
  27. Storch V, Ruhberg H (1977) Fine structure of the sensilla of Peripatopsis moseleyi (Onychophora). Cell Tissue Res 177:539–553PubMedCrossRefGoogle Scholar
  28. Strausfeld NJ (2012) Arthropod brains: evolution, functional elegance, and historical significance. Harvard University Press, Cambridge, pp 1–830Google Scholar
  29. Ungerer P, Wolff C (2005) External morphology of limb development in the amphipod Orchestia cavimana (Crustacea, Malacostraca, Peracarida). Zoomorphology 124:89–99CrossRefGoogle Scholar
  30. Waloszek D, Dunlop J (2002) A larval sea spider (Arthropoda: Pycnogonida) from the Upper Cambrian “Orsten”of Sweden, and the phylogenetic position of pycnogonids. Palaeontology 45:421–446CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Allgemeine und Spezielle Zoologie, Institut für BiowissenschaftenUniversität RostockRostockGermany

Personalised recommendations