Abstract

Embryonic anterior-posterior patterning is well understood in Drosophila, which uses 'long germ' embryogenesis, in which all segments are patterned before cellularization. In contrast, most insects use 'short germ' embryogenesis, wherein only head and thorax are patterned in a syncytial environment while the remainder of the embryo is generated after cellularization. We use the wasp Nasonia (Nv) to address how the transition from short to long germ embryogenesis occurred. Maternal and gap gene expression in Nasonia suggest long germ embryogenesis. However, the Nasonia pair-rule genes even-skipped, odd-skipped, runt and hairy are all expressed as early blastoderm pair-rule stripes and late-forming posterior stripes. Knockdown of Nv eve, odd or h causes loss of alternate segments at the anterior and complete loss of abdominal segments. We propose that Nasonia uses a mixed mode of segmentation wherein pair-rule genes pattern the embryo in a manner resembling Drosophila at the anterior and ancestral Tribolium at the posterior. DOI: http://dx.doi.org/10.7554/eLife.01440.001.

Highlights

  • Control of axial patterning and embryonic development is well understood in Drosophila

  • We used in situ hybridization to look at the expression pattern of Nasonia vitripennis (Nv) eve during Nasonia embryogenesis (Figure 1)

  • Nv eve expression becomes detectable as a broad early domain in the blastoderm embryo at around 3 hr after egg laying (AEL) (Figure 1A)

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Summary

Introduction

Control of axial patterning and embryonic development is well understood in Drosophila (reviewed in Liu and Kaufman, 2005b; Peel et al, 2005; Rosenberg et al, 2009; Pankratz and Jaj, 1993). For the A–P axis, maternally loaded mRNAs generate localized signaling centers at each pole of the egg to establish morphogenetic gradients These gradients instruct, in a concentration dependent manner, broad domains of expression of early zygotic genes, the ‘gap genes’ (Chen et al, 2012). This is made possible in part by the syncytial environment of the early blastoderm embryo where nuclei are not bounded by membranes, allowing diffusion of morphogen transcription factors through a shared cytoplasm without the need for cell–cell signaling. Forays into other insect models have revealed that the Drosophila paradigm is an evolutionarily derived state, and that insects generally undergo a very different type of embryogenesis and segmentation (reviewed in Liu and Kaufman, 2005b; Peel et al, 2005; Rosenberg et al, 2009)

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