Coming into clear sight at last: Ancestral and derived events during chelicerate visual system development

Abstract

Pioneering molecular work on chelicerate visual system development in the horseshoe crab Limulus polyphemus surprised with the possibility that this process may not depend on the deeply conserved retinal determination function of Pax6 transcription factors. Genomic, transcriptomic, and developmental studies in spiders now reveal that the arthropod Pax6 homologs eyeless and twin of eyeless act as ancestral determinants of the ocular head segment in chelicerates, which clarifies deep gene regulatory and structural homologies and recommends more unified terminologies in the comparison of arthropod visual systems. Following this phylotypic stage, chelicerate visual system development differs fundamentally from other arthropods during the compartmentalization of the ocular segment in that eye and optic neuropil primordia originate independently from each other. Comparative analyses of this phase identified further gene regulatory homologies but also major differences, most notably the possibly compensatory replacement of Pax6 by Pax2 in lateral eye specification. Also see the video

Development and patterning of a highly versatile visual system in spiders

“…One mystery that persists is how eye development is initiated in spiders (Friedrich 2022). Our expression data for six new species spread across the spider phylogeny demonstrate that there is no clear evidence for Pax6 expression within the developing eye primordia.…”

“…Similarly, in P. tepidariorum Pax6.1 and Pax6.2 are co-expressed from stage 6 to 8 in a stripe that moves away from the anterior rim of the germ band to a more posterior position in the precheliceral lobes (Leite et al 2022). Although Pax6 and RDG expression never overlap, components of the spider visual system likely originate from the same early embryonic field of Pax6 -expressing cells as in other arthropods (Friedrich 2022). Our detection of eya and so1 expression as early as stage 8.2 provides possible insight to the initiation of the visual system.…”

“…Similarly, in P. tepidariorum Pax6.1 and Pax6.2 are expressed in stripes from stage 6 to 8 that moves away from the anterior rim of the germ band to more posterior positions in the precheliceral lobes (Leite et al 2022). Thus, components of the spider visual system likely originate from within the same early embryonic field of Pax6 -expressing cells as in other arthropods (Friedrich 2022). Recent findings by Janeschik et al (2022) identified Pax2 as a new marker for the secondary eye primordia.…”

Evolutionary Conservation of Five Pax6 Homologs under Strong Purifying Selection in the Horseshoe Crab Species Cluster

“…Previous BLAST searches identified three distinct homologs of ey in L. polyphemus, which contrasted with the conservation of a singleton homolog of ey throughout all other arthropods investigated so far, including other chelicerates [8]. To probe for the conservation of all three L. polyphemus ey homologs in other horseshoe crab species, we searched the genome assemblies of C. rotundicauda, T. tridentatus, and T. gigas by tBLASTn with the L. polyphemus ey1, ey2, and ey3 homologs as queries.…”

“…Comparative analyses of the past 15 years revealed that the presence of two Pax6 genes in Drosophila and other arthropods, including species from Pancrustacea, Myriapoda, and Chelicerata, is due to a gene duplication that must have taken place over 500 million years ago in the arthropod stem lineage [7]. Given this deep conservation of singleton homologs of ey and toy in arthropods, it came as a surprise to find not only one Pax6 ortholog in L. polyphemus that was originally uncovered by gene cloning efforts [5] but three orthologs of ey and two orthologs of toy in the whole genome assembly of L. polyphemus [8].…”