Novel function of Distal-less as a gap gene during spider segmentation.
Despite many aspects of the regulation of segmentation being conserved among arthropods, the evolution of novel gene functions has played an important role in the evolution of developmental regulation and the emergence of new segmental structures. Moreover the study of such novel gene functions can be informative with respect to the patterns and direction of evolutionary changes in developmental programs. The homeobox gene Distal-less (Dll) is known for its conserved function in appendage development in metazoans. In arthropods, Dll is required for the specification of distal appendage structures. Here we describe a novel and unexpected role of Dll in the spider Achaearanea tepidariorum. We detect At-Dll transcripts not only in the appendages, but unexpectedly also in an anterior domain during early development, prior to the specification of the limb primordia. A similar early Dll domain is present in the distantly related spider Pholcus phalangioides. In A. tepidariorum this early At-Dll expression is required for head segmentation. RNA interference results in spiders that lack either the first or the first and the second walking leg segments. The early At-Dll expression is also required for the activation of the segment polarity genes engrailed and hedgehog in this region. Our work identifies the Distal-less gene as a novel factor in anterior spider segmentation with a gap gene-like function. This novel role of Dll is interesting because Dll expression is reduced in this region in crustaceans and the homologous insect segment, the mandible segment, does not express Dll and does not require this gene for patterning. We therefore discuss the possible implications of our results for understanding the evolution and diversification of the mandible segment.
Georg-August-Universität Göttingen, Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abteilung für Entwicklungsbiologie, GZMB Ernst-Caspari-Haus, Göttingen, Germany.
Matthias
M
Pechmann
Sara
S
Khadjeh
Natascha
N
Turetzek
Alistair P
AP
McGregor
Wim G M
WG
Damen
Nikola-Michael
NM
Prpic
D000818:Animals; D005075:Biological Evolution; D019521:Body Patterning / Q000235:genetics*; D016764:Cell Polarity; D005121:Extremities / Q000033:anatomy & histology / Q000254:growth & development; D018507:Gene Expression Regulation, Developmental; D018398:Homeodomain Proteins / Q000235:genetics / Q000502:physiology*; D010641:Phenotype; D034622:RNA Interference; D013112:Spiders / Q000033:anatomy & histology / Q000235:genetics / Q000254:growth & development*; D014157:Transcription Factors / Q000235:genetics / Q000502:physiology*
D018398:Homeodomain Proteins; D014157:Transcription Factors; C117261:distal-less protein, insect