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A 4D-microscopic analysis of the germ band in the isopod crustacean Porcellio scaber (Malacostraca, Peracarida)—developmental and phylogenetic implications

Abstract

Malacostracan crustaceans have evolved a conserved stereotyped cell division pattern in the post-naupliar germ band. This cleavage pattern is unique in arthropods investigated so far, and allows a combined analysis of gene expression and cell lineage during segmentation and organ development at the level of individual cells. To investigate the cell lineage in the germ band of the isopod Porcellio scaber, we used a 4D-microscopy system, which enables us to analyse every cell event in the living embryo. The study was combined with the analysis of the expression of the gene engrailed (en) at different stages of germ band formation. Our findings confirm the results of earlier investigations of the cell division pattern in the posterior part of the isopod germ band. Furthermore, we can show that in the anterior region, in contrast to the posterior part, cleavage directions are variable and cell sorting takes place—similar to other arthropod germ bands. Additionally, the gene expression pattern of en in this region is not as regular as in the post-naupliar germ band, and only later becomes regulated into its characteristic stripe pattern. The comparison of the cell lineage of P. scaber with that of other malacostracan crustaceans shows an enhancement in the velocity of cell divisions relative to the arrangement of these cells in rows in the isopod germ band. The striking similarity of the formation of the genealogical units in the anterior part suggests a sister group relationship between the peracarid taxa Tanaidacea and Isopoda.

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Acknowledgements

We thank Nipam Patel and Harald Saumweber for the monoclonal Antibody 4D9 and Craig Magie for improving the manuscript. This work was supported by the DFG (Scho 442/5-2,3).

Author information

Correspondence to Andreas Hejnol.

Additional information

Communicated by S. Roth

Electronic supplementary material

Below is the link to the electronic supplentary material.

Time lapse of the gastrulation in Porcellio scaber. 30 h in 60 s. View on the cells of the germ disc. The cells divide in two division waves and start to sink into the gastrulation center on the left. The future anterior orientated to the top/left. (MOV 22 MB)

Time lapse of the division of the cells in row A and B in Porcellio scaber. 32 h in 60 s. The SIMI°BioCell reconstruction in the left upper corner. Every sphere represents the cells described as in the publication. Anterior is to the left. (MOV 26 MB)

Time lapse of the division of the cells in the genealogical unit E(2) and E(3) in Porcellio scaber. 20 h in 42 s. The SIMI°BioCell reconstruction in the right corner. The ectoteloblasts give off their derivates to anterior (left). (MOV 11 MB)

Time lapse of the differential divisions in the right half of a thoracal segment in Porcellio scaber. 33 h in 80 s. During the movie, a reconstruction of the differential cleavages with SIMI°BioCell shows up in the lower left corner. The movie ends during limb bud formation. Anterior is to the top. (MOV 22 MB)

S1

Time lapse of the gastrulation in Porcellio scaber. 30 h in 60 s. View on the cells of the germ disc. The cells divide in two division waves and start to sink into the gastrulation center on the left. The future anterior orientated to the top/left. (MOV 22 MB)

S2

Time lapse of the division of the cells in row A and B in Porcellio scaber. 32 h in 60 s. The SIMI°BioCell reconstruction in the left upper corner. Every sphere represents the cells described as in the publication. Anterior is to the left. (MOV 26 MB)

S3

Time lapse of the division of the cells in the genealogical unit E(2) and E(3) in Porcellio scaber. 20 h in 42 s. The SIMI°BioCell reconstruction in the right corner. The ectoteloblasts give off their derivates to anterior (left). (MOV 11 MB)

S4

Time lapse of the differential divisions in the right half of a thoracal segment in Porcellio scaber. 33 h in 80 s. During the movie, a reconstruction of the differential cleavages with SIMI°BioCell shows up in the lower left corner. The movie ends during limb bud formation. Anterior is to the top. (MOV 22 MB)

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Hejnol, A., Schnabel, R. & Scholtz, G. A 4D-microscopic analysis of the germ band in the isopod crustacean Porcellio scaber (Malacostraca, Peracarida)—developmental and phylogenetic implications. Dev Genes Evol 216, 755–767 (2006). https://doi.org/10.1007/s00427-006-0105-4

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Keywords

  • Cell lineage
  • Cell clones
  • engrailed
  • Differentiation
  • Segmentation