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Segment polarity gene expression in a myriapod reveals conserved and diverged aspects of early head patterning in arthropods

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Abstract

Arthropods show two kinds of developmental mode. In the so-called long germ developmental mode (as exemplified by the fly Drosophila), all segments are formed almost simultaneously from a preexisting field of cells. In contrast, in the so-called short germ developmental mode (as exemplified by the vast majority of arthropods), only the anterior segments are patterned similarly as in Drosophila, and posterior segments are added in a single or double segmental periodicity from a posterior segment addition zone (SAZ). The addition of segments from the SAZ is controlled by dynamic waves of gene activity. Recent studies on a spider have revealed that a similar dynamic process, involving expression of the segment polarity gene (SPG) hedgehog (hh), is involved in the formation of the anterior head segments. The present study shows that in the myriapod Glomeris marginata the early expression of hh is also in a broad anterior domain, but this domain corresponds only to the ocular and antennal segment. It does not, like in spiders, represent expression in the posterior adjacent segment. In contrast, the anterior hh pattern is conserved in Glomeris and insects. All investigated myriapod SPGs and associated factors are expressed with delay in the premandibular (tritocerebral) segment. This delay is exclusively found in insects and myriapods, but not in chelicerates, crustaceans and onychophorans. Therefore, it may represent a synapomorphy uniting insects and myriapods (Atelocerata hypothesis), contradicting the leading opinion that suggests a sister relationship of crustaceans and insects (Pancrustacea hypothesis). In Glomeris embryos, the SPG engrailed is first expressed in the mandibular segment. This feature is conserved in representatives of all arthropod classes suggesting that the mandibular segment may have a special function in anterior patterning.

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Acknowledgments

I would like to thank two anonymous reviewers for their helpful comments on the manuscript and John Peel for proofreading of the manuscript.

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  1. Department of Earth Sciences, Uppsala University, Palaeobiology, Villavägen 16, 75236, Uppsala, Sweden

    Ralf Janssen

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Correspondence to Ralf Janssen.

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Communicated by: S. Roth

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Fig. S1

Expression of Glomeris hedgehog at stage 0.3. Embryos are oriented with anterior to the left. a Stage 0.3. Same complement of hh stripes as in a slightly older stage 0.4 embryo (cf. Fig. 1d). a′ DAPI counterstaining of the same embryo shown in a (JPEG 153 kb)

High-resolution image (TIFF 4124 kb)

Fig. S2

Additional aspects of engrailed expression. Embryos are oriented with anterior to the left. a Embryo of intermediate stage between stage 0 and stage 0.1 (cf. Janssen et al. (2004)). Weak expression of en which is in the mandibular segment primordium (arrowhead) precedes expression in the other segment primordia. a′ Same embryo as shown in a. DAPI counterstaining. Arrowhead as in a (JPEG 150 kb)

High Resolution image (TIFF 3789 kb)

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Janssen, R. Segment polarity gene expression in a myriapod reveals conserved and diverged aspects of early head patterning in arthropods. Dev Genes Evol 222, 299–309 (2012). https://doi.org/10.1007/s00427-012-0413-9

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