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The proliferation of genomic resources for Chelicerata in the past 10 years has revealed that the evolution of chelicerate genomes is more dynamic than previously thought, with multiple waves of ancient whole genome duplications affecting separate lineages. Such duplication events are fascinating from the perspective of evolutionary history because the burst of new gene copies associated with genome duplications facilitates the acquisition of new gene functions (neofunctionalization), which may in turn lead to morphological novelties and spur net diversification. While neofunctionalization has been invoked in several contexts with respect to the success and diversity of spiders, the overall impact of whole genome duplications on chelicerate evolution and development remains imperfectly understood. The purpose of this review is to examine critically the role of whole genome duplication on the diversification of the extant arachnid orders, as well as assess functional datasets for evidence of subfunctionalization or neofunctionalization in chelicerates. This examination focuses on functional data from two focal model taxa: the spider Parasteatoda tepidariorum, which exhibits evidence for an ancient duplication, and the harvestman Phalangium opilio, which exhibits an unduplicated genome. I show that there is no evidence that taxa with genome duplications are more successful than taxa with unduplicated genomes. I contend that evidence for sub- or neofunctionalization of duplicated developmental patterning genes in spiders is indirect or fragmentary at present, despite the appeal of this postulate for explaining the success of groups like spiders. Available expression data suggest that the condition of duplicated Hox modules may have played a role in promoting body plan disparity in the posterior tagma of some orders, such as spiders and scorpions, but functional data substantiating this postulate are critically missing. Spatiotemporal dynamics of duplicated transcription factors in spiders may represent cases of developmental system drift, rather than neofunctionalization. Developmental system drift may represent an important, but overlooked, null hypothesis for studies of paralogs in chelicerate developmental biology. To distinguish between subfunctionalization, neofunctionalization, and developmental system drift, concomitant establishment of comparative functional datasets from taxa exhibiting the genome duplication, as well as those that lack the paralogy, is sorely needed.
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Eggs to long-legs: embryonic staging of the harvestman Phalangium opilio (Opiliones), an emerging model arachnid
Abstract 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.
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- Award ID(s):
- 2016141
- PAR ID:
- 10353761
- Date Published:
- Journal Name:
- Frontiers in Zoology
- Volume:
- 19
- Issue:
- 1
- ISSN:
- 1742-9994
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)Chelicerate arthropods exhibit dynamic genome evolution, with ancient whole-genome duplication (WGD) events affecting several orders. Yet, genomes remain unavailable for a number of poorly studied orders, such as Opiliones (daddy-long-legs), which has hindered comparative study. We assembled the first harvestman draft genome for the species Phalangium opilio , which bears elongate, prehensile appendages, made possible by numerous distal articles called tarsomeres. Here, we show that the genome of P. opilio exhibits a single Hox cluster and no evidence of WGD. To investigate the developmental genetic basis for the quintessential trait of this group—the elongate legs—we interrogated the function of the Hox genes Deformed ( Dfd ) and Sex combs reduced ( Scr ), and a homologue of Epidermal growth factor receptor ( Egfr ). Knockdown of Dfd incurred homeotic transformation of two pairs of legs into pedipalps, with dramatic shortening of leg segments in the longest leg pair, whereas homeosis in L3 is only achieved upon double Dfd + Scr knockdown. Knockdown of Egfr incurred shortened appendages and the loss of tarsomeres. The similarity of Egfr loss-of-function phenotypic spectra in insects and this arachnid suggest that repeated cooption of EGFR signalling underlies the independent gains of supernumerary tarsomeres across the arthropod tree of life.more » « less
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True, John (Ed.)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 pedipalp 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 (WGD) event. Here, we investigated the function of the single-copy ortholog of lab in the harvestman Phalangium opilio, an exemplar of a lineage that was not subject to this WGD. Embryonic RNA interference against lab resulted in two classes of phenotypes: homeotic transformations of pedipalps to chelicerae, as well as reduction and fusion of the pedipalp and leg 1 segments. To test for combinatorial function, we performed a double knockdown of lab and Dfd, which resulted in a homeotic transformation of both pedipalps and the 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.more » « less
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True, John (Ed.)Neofunctionalization of duplicated gene copies is thought to be an important process underlying the origin of evolutionary novelty and provides an elegant mechanism for the origin of new phenotypic traits. One putative case where a new gene copy has been linked to a novel morphological trait is the origin of the arachnid patella, a taxonomically restricted leg segment. In spiders, the origin of this segment has been linked to the origin of the paralog dachshund-2, suggesting that a new gene facilitated the expression of a new trait. However, various arachnid groups that possess patellae do not have a copy of dachshund-2, disfavoring the direct link between gene origin and trait origin. We investigated the developmental genetic basis for patellar patterning in the harvestman Phalangium opilio, which lacks dachshund-2. Here, we show that the harvestman patella is established by a novel expression domain of the transcription factor extradenticle. Leveraging this definition of patellar identity, we surveyed targeted groups across chelicerate phylogeny to assess when this trait evolved. We show that a patellar homolog is present in Pycnogonida (sea spiders) and various arachnid orders, suggesting a single origin of the patella in the ancestor of Chelicerata. A potential loss of the patella is observed in Ixodida. Our results suggest that the modification of an ancient gene, rather than the neofunctionalization of a new gene copy, underlies the origin of the patella. Broadly, this work underscores the value of comparative data and broad taxonomic sampling when testing hypotheses in evolutionary developmental biology.more » « less
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1186/s12983-022-00454-z
