Evolution and homology of leg segments in Chelicerata: Evo-devo solutions to century-old challenges

Abstract

A major theme in the evolution of Arthropoda is the origin and diversification of jointed appendages. One appealing framework for the evolution of arthropod appendage diversity has long been that a small network of homologous genes in the panarthropod ancestor established and subdivided the proximo-distal (PD) appendage axis, with lineage-specific modifications of these genes’ expression domains resulting in novel types of appendages. A corollary of this idea is the inference that each segment in the arthropod leg can be directly homologized to other such segments, based on anatomical or developmental genetic landmarks. Here, we explore the evolution of leg segments in Chelicerata, a group which exhibits marked diversity in leg architecture and number of leg segments, and thereby poses a greater challenge to the exercise of assigning segmental homologies. Focusing on the controversial nomenclature of leg segments in Pycnogonida (sea spiders), we identify potential markers of positional homology in different parts of the sea spider and arachnid PD axis, using comparative gene expression data. Nevertheless, we identify caveats to the use of transcription factor expression domains as landmarks for inference of positional homology, highlighting cases where datasets conflict in homology assignment. We postulate that the utility of gene expression data for inferring homologies is a function of phylogenetic distance.