Systemic paralogy and function of retinal determination network homologs in arachnids

Abstract

Background Arachnids are important components of cave ecosystems and display many examples of troglomorphisms, such as blindness, depigmentation, and elongate appendages. Little is known about how the eyes of arachnids are specified genetically, let alone the mechanisms for eye reduction and loss in troglomorphic arachnids. Additionally, duplication of Retinal Determination Gene Network (RDGN) homologs in spiders has convoluted functional inferences extrapolated from single-copy homologs in pancrustacean models. Results We investigated a sister species pair of Israeli cave whip spiders, Charinus ioanniticus and C. israelensis (Arachnopulmonata, Amblypygi), of which one species has reduced eyes. We generated embryonic transcriptomes for both Amblypygi species, and discovered that several RDGN homologs exhibit duplications. We show that duplication of RDGN homologs is systemic across arachnopulmonates (arachnid orders that bear book lungs), rather than being a spider-specific phenomenon. A differential gene expression (DGE) analysis comparing the expression of RDGN genes in field-collected embryos of both species identified candidate RDGN genes involved in the formation and reduction of eyes in whip spiders. To ground bioinformatic inference of expression patterns with functional experiments, we interrogated the function of three candidate RDGN genes identified from DGE using RNAi in the spider Parasteatoda tepidariorum. We provide functional evidence that one of these paralogs, sine oculis/Six1 A (soA), is necessary for the development of all arachnid eye types. Conclusions Our work establishes a foundation to investigate the genetics of troglomorphic adaptations in cave arachnids, and links differential gene expression to an arthropod eye phenotype for the first time outside of Pancrustacea. Our results support the conservation of at least one RDGN component across Arthropoda and provide a framework for identifying the role of gene duplications in generating arachnid eye diversity.

Taxonomic Sampling and Rare Genomic Changes Overcome Long-Branch Attraction in the Phylogenetic Placement of Pseudoscorpions

“…A previous comprehensive analysis of homeobox genes by Leite et al. (2018) showed that the retention of duplicates is systemic in two arachnopulmonate lineages (spiders and scorpions), an inference subsequently supported by the first whip spider developmental transcriptomes ( Gainett and Sharma 2020 ; Gainett et al. 2020 ) and by embryonic gene expression data ( Gainett and Sharma 2020 ; Nolan et al.…”

“…The systemic duplication of developmental patterning genes and gene expression patterns together constitute a highly complex character that unites Arachnopulmonata ( Leite et al. 2016 ; Gainett and Sharma 2020 ; Gainett et al. 2020 ; Nolan et al.…”

The genome of a daddy-long-legs (Opiliones) illuminates the evolution of arachnid appendages and chelicerate genome architecture

“…Through manual annotation, we separately examined the genome for evidence of duplicates in genes with known arachnopulmonate-specific paralogs and distinguishable embryonic gene expression patterns, focusing on four leg patterning genes (dachshund (Battelle et al, 2016), homothorax (Gong et al, 2019), extradenticle (Schwager et al, 2017), spineless (Setton et al, 2017)) and the retinal determination gene network (sine oculis, Optix, orthodenticle (Gainett et al, 2020;Samadi, Schmid, & Eriksson, 2015;Schomburg et al, 2015)). All of these genes, known to exhibit arachnopulmonate-specific duplications and spatiotemporal subdivision of expression patterns, were discovered as single-copy in the harvestman genome (Table S2).…”

Molecular evolutionary trends and biosynthesis pathways in the Oribatida revealed by the genome ofArchegozetes longisetosus

“…Another peculiarity of Archegozetes is that these mites lack eyes (see more details below). Eye loss has been documented in other arachnid clades, including independently in other members of Acari (Evans 1992; Walter and Proctor 1999), and it has been recently demonstrated that a species of whip spider has reduced its eyes by reducing the expression of retinal determination genes that are shared throughout arthropods (Gainett et al 2020). We sought to determine if eye loss in Archegozetes also is associated with the reduced expression of these genes (see also analysis of photoreceptor genes below).…”

“…We sought to determine if eye loss in Archegozetes also is associated with the reduced expression of these genes (see also analysis of photoreceptor genes below). The genes, which have been shown to be expressed in the developing eyes of spiders and whip scorpions, include Pax-6, six1/sine oculis (so), eyes absent (eya), Eyegone, Six3/Optix, and atonal (Gainett et al 2020; Samadi et al 2015; Schomburg et al 2015). We also followed the expression of Al-orthodenticle, a gene previously shown to be expressed in the ocular segment of Archegozetes (Telford and Thomas 1998).…”