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Dev Biol. 2017 Oct 1;430(1):224-236. doi: 10.1016/j.ydbio.2017.07.016. Epub 2017 Jul 29.

Expression and function of spineless orthologs correlate with distal deutocerebral appendage morphology across Arthropoda.

Author information

1
Department of Integrative Biology, University of Wisconsin-Madison, 430 Lincoln Drive, Madison, WI 53706, USA.
2
Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA.
3
Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, NY, USA.
4
Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA; Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA.
5
Department of Integrative Biology, University of Wisconsin-Madison, 430 Lincoln Drive, Madison, WI 53706, USA. Electronic address: prashant.sharma@wisc.edu.

Abstract

The deutocerebral (second) head segment is putatively homologous across Arthropoda, in spite of remarkable disparity of form and function of deutocerebral appendages. In Mandibulata this segment bears a pair of sensory antennae, whereas in Chelicerata the same segment bears a pair of feeding appendages called chelicerae. Part of the evidence for the homology of deutocerebral appendages is the conserved function of homothorax (hth), which has been shown to specify antennal or cheliceral fate in the absence of Hox signaling, in both mandibulate and chelicerate exemplars. However, the genetic basis for the morphological disparity of antenna and chelicera is not understood. To test whether downstream targets of hth have diverged in a lineage-specific manner, we examined the evolution of the function and expression of spineless (ss), which in two holometabolous insects is known to act as a hth target and distal antennal determinant. Toward expanding phylogenetic representation of gene expression data, here we show that strong expression of ss is observed in developing antennae of a hemimetabolous insect, a centipede, and an amphipod crustacean. By contrast, ss orthologs are not expressed throughout the cheliceral limb buds of spiders or harvestmen during developmental stages when appendage fate is specified. RNA interference-mediated knockdown of ss in Oncopeltus fasciatus, which bears a simple plesiomorphic antenna, resulted in homeotic distal antenna-to-leg transformation, comparable to data from holometabolous insect counterparts. Knockdown of hth in Oncopeltus fasciatus abrogated ss expression, suggesting conservation of upstream regulation. These data suggest that ss may be a flagellar (distal antennal) determinant more broadly, and that this function was acquired at the base of Mandibulata.

KEYWORDS:

Appendages; Fate specification; Homology; Morphological novelty; Selector gene

PMID:
28764892
DOI:
10.1016/j.ydbio.2017.07.016
[Indexed for MEDLINE]
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