hunchback functions as a segmentation gene in the spider Achaearanea tepidariorum

Abstract

Background: In insects, the gap gene hunchback (hb) is required for the formation of a set of adjacent segments through the regulation of downstream target genes of the pair rule and segment-polarity classes. In addition, hb is a major regulator of Hox genes and it has been suggested that this is the ancestral role of hb in insects or perhaps even arthropods. To date, however, hb function has been analyzed only in insects.

Results: Here we show that hb acts as a segmentation gene during anterior patterning of a noninsect arthropod, the spider Achaearanea tepidariorum. The leg-bearing segments L1, L2, and L4 are missing after downregulation of At-hb via RNAi. At-hb is required for the correct organization of target genes in this region of the embryo, suggesting that At-hb acts as a gap gene in the spider. In contrast to insects, hb does not control Hox gene expression in the spider. Furthermore, analysis of twist expression in At-hb knockdown embryos demonstrates that hb is not required for initiating the segmental organization of the mesoderm in the affected region, but only for its maintenance.

Conclusions: Our findings suggest that hb might have had a segmentation gene function in the arthropod ancestor and contradicts the suggestion that the control of Hox genes is the ancestral role of hb. Anterior spider segmentation thus utilizes a Drosophila-like genetic mode, whereas a vertebrate-like mechanism involving Wnt8 and Notch/Delta signaling is used to pattern posterior segments. These data support the hypothesis that short-germ arthropods employ two distinct mechanisms to segment their anterior and posterior body parts.