Background The comparative embryology of Chelicerata has greatly advanced in recent years with the integration of classical studies and genetics, prominently spearheaded by developmental genetic works in spiders. Nonetheless, the understanding of the evolution of development and polarization of embryological characters in Chelicerata is presently limited, as few non-spider species have been well studied. A promising focal species for chelicerate evo-devo is the daddy-long-legs (harvestman) Phalangium opilio, a member of the order Opiliones. Phalangium opilio, breeds prolifically and is easily accessible in many parts of the world, as well as tractable in a laboratory setting. Resources for this species include developmental transcriptomes, a draft genome, and protocols for RNA interference, but a modern staging system is critically missing for this emerging model system. Results We present a staging system of P. opilio embryogenesis that spans the most important morphogenetic events with respect to segment formation, appendage elongation and head development. Using time-lapse imaging, confocal microscopy, colorimetric in situ hybridization, and immunohistochemistry, we tracked the development of synchronous clutches from egg laying to adulthood. We describe key events in segmentation, myogenesis, neurogenesis, and germ cell formation. Conclusion Considering the phylogenetic position of Opiliones and the unduplicated condition of its genome (in contrast to groups like spiders and scorpions), this species is poised to serve as a linchpin for comparative studies in arthropod development and genome evolution. The staging system presented herein provides a valuable reference for P. opilio that we anticipate being useful to the arthropod evo-devo community, with the goal of revitalizing research in the comparative development of non-spider arachnids.
Despite an abundance of gene expression surveys, comparatively little is known about Hox gene function in Chelicerata. Previous investigations of paralogs of labial (lab) and Deformed (Dfd) in a spider have shown that these play a role in tissue maintenance of the pedipalpal segment (lab-1) and in patterning the first walking leg identity (Dfd-1), respectively. However, extrapolations of these data across chelicerates are hindered by the existence of duplicated Hox genes in arachnopulmonates (e.g., spiders and scorpions), which have resulted from an ancient whole genome duplication event. Here, we investigated the function of single-copy ortholog of lab in the harvestman Phalangium opilio, an exemplar of a lineage that was not subject of this whole genome duplication. Embryonic RNAi against lab resulted in two classes of phenotypes: homeotic transformations of pedipalps to chelicerae, as well as reduction and fusion of the pedipalpal segment with adjacent segments. To test for combinatorial function, we performed double knockdown of lab and Dfd, which results in homeotic transformation of both pedipalps and first walking legs into cheliceral identity, whereas the second walking leg is transformed into a pedipalpal identity. Taken together, these results elucidate a model for the Hox logic of head segments in Chelicerata. To substantiate the validity of this model, we performed expression surveys for lab and Dfd paralogs in scorpions and horseshoe crabs. We show that repetition of morphologically similar appendages is correlated with uniform expression levels of the Hox genes lab and Dfd, irrespective of the number of gene copies.
The chelicerate body plan is distinguished from other arthropod groups by its division of segments into two tagmata: the anterior prosoma (cephalothorax) and the posterior opisthosoma (abdomen). Little is understood about the genetic mechanisms that establish the prosomal-opisthosomal (PO) boundary. To discover these mechanisms, we created high-quality genomic resources for the large-bodied spiderAphonopelma hentzi. We sequenced specific territories along the antero-posterior axis of developing embryos and applied differential gene expression analyses to identify putative regulators of regional identity. After bioinformatic screening for candidate genes that were consistently highly expressed in the posterior segments, we validated the function of highly ranked candidates in the tractable spider modelParasteatoda tepidariorum. Here, we show that an arthropod homolog of the Iroquois complex of homeobox genes is required for proper formation of the boundary between arachnid tagmata. The function of this homolog had not been previously characterized, because it was lost in the common ancestor of Pancrustacea, precluding its investigation in well-studied insect model organisms. Knockdown of the spider copy of this gene, which we designate aswaist-less, inP. tepidariorumresulted in embryos with defects in the PO boundary, incurring discontinuous spider germ bands. We show thatwaist-lessis required for proper specification of dorso-ventral identity in the segments that span the prosoma-opisthosoma boundary, which in adult spiders corresponds to the narrowed pedicel. Our results suggest the requirement of an ancient, taxon-restricted paralog for the establishment of the tagmatic boundary that defines Chelicerata.
Despite an abundance of gene expression surveys, comparatively little is known about Hox gene function in Chelicerata, with emphasis on the Hox logic of the anterior prosomal segments, which bear the mouthparts. Previous investigations of individual paralogs oflabial(lab) andDeformed(Dfd) in the spiderParasteatoda tepidariorumhave shown that these play a role in tissue maintenance of the pedipalpal segment (labial-1) and in patterning the first walking leg identity (Deformed-1), respectively. However, broader extrapolations of these data points across chelicerates are hindered by the existence of duplicated copies of Hox genes in arachnopulmonates (e.g., spiders and scorpions), which have resulted from an ancient whole genome duplication event. Here, we investigated the function of single-copy orthologs oflabin the harvestmanPhalangium opilio, an exemplar of a lineage that was not subject of this whole genome duplication. Embryonic RNAi againstlabresulted in homeotic transformations of pedipalps to chelicerae, as well as reduction and fusion of the pedipalpal segment with adjacent segments. To test for combinatorial function, we performed double knockdown oflabandDfd, which results in homeotic transformation of both pedipalps and first walking legs into cheliceral identity, whereas the second walking leg is transformed into a pedipalpal identity. Taken together, these results elucidate a model for the Hox logic of head segments in Chelicerata. To substantiate the validity of this model, we additionally performed expression surveys for duplicated copies oflabandDfdin scorpions and horseshoe crabs, toward understanding the genetic basis of a heteronomous prosoma. We show that repetition of morphologically similar appendages is correlated with uniform expression levels of the Hox geneslabandDfd, irrespective of the number of gene copies.
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