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.
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.
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- NSF-PAR ID:
- 10291697
- Date Published:
- Journal Name:
- BMC Genomics
- Volume:
- 21
- Issue:
- 1
- ISSN:
- 1471-2164
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Synopsis -
The whip spider family Charinidae Quintero, 1986 is the most speciose and widely distributed in the arachnid order Amblypygi Thorell, 1883. It comprises three genera and 95 species distributed across all tropical continents and the eastern Mediterranean. Despite recent advances in the taxonomy of the family, a global revision of all its species, necessary to advance understanding of its systematics, biogeography and evolution, has never been conducted. In the present contribution, the family is revised in its entirety for the first time, including all previous names and 33 new species, 24 in the genus Charinus Simon, 1892: C. alagoanus sp. nov., C. apiaca sp. nov., C. carinae sp. nov., C. carioca sp. nov., C. carvalhoi sp. nov., C. cearensis sp. nov., C. diamantinus sp. nov., C. euclidesi sp. nov., C. goitaca sp. nov., C. guayaquil sp. nov., C. imperialis sp. nov., C. loko sp. nov., C. magalhaesi sp. nov., C. miskito sp. nov., C. mocoa sp. nov., C. monasticus sp. nov., C. palikur sp. nov., C. perquerens sp. nov., C. puri sp. nov., C. renneri sp. nov., C. sooretama sp. nov., C. souzai sp. nov., C. susuwa sp. nov., C. una sp. nov.; eight in the genus Sarax Simon, 1892: S. bilua sp. nov., S. dunni sp. nov., S. gravelyi sp. nov., S. indochinensis sp. nov., S. lembeh sp. nov., S. palau sp. nov., S. rahmadii sp. nov., S. tiomanensis sp. nov.; and one in the genus Weygoldtia Miranda et al., 2018: W. consonensis sp. nov. Taxonomic keys to the 132 species (excluding four nomina dubia) are presented and several taxonomic rearrangements implemented. Four subspecies are elevated to species level: Charinus cavernicolus Weygoldt, 2006, C. elegans Weygoldt, 2006, C. longipes Weygoldt, 2006, and Sarax bispinosus (Nair, 1934). Sarax batuensis Roewer, 1962 is removed from synonymy with Sarax buxtoni (Gravely, 1915) and S. buxtoni newly synonymized with Sarax rimosus (Simon, 1901). Stygophrynus moultoni Gravely, 1915 is transferred to Sarax, resulting in Sarax moultoni (Gravely, 1915) comb. nov. Ten species are transferred from Charinus to Sarax, resulting in new combinations: S. abbatei (Delle Cave, 1986) comb. nov., S. bengalensis (Gravely, 1911) comb. nov., S. dhofarensis (Weygoldt, Pohl & Polak, 2002) comb. nov., S. ioanniticus (Kritscher, 1959) comb. nov., S. israelensis (Miranda et al., 2016) comb. nov., S. omanensis (Delle Cave, Gardner & Weygoldt, 2009) comb. nov., S. pakistanus (Weygoldt, 2005) comb. nov., S. seychellarum (Kraepelin, 1898) comb. nov., S. socotranus (Weygoldt, Pohl & Polak, 2002) comb. nov. and S. stygochthobius (Weygoldt & Van Damme, 2004) comb. nov.more » « less
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Abstract The orb web is a remarkable example of animal architecture that is observed in families of spiders that diverged over 200 million years ago. While several genomes exist for araneid orb-weavers, none exist for other orb-weaving families, hampering efforts to investigate the genetic basis of this complex behavior. Here we present a chromosome-level genome assembly for the cribellate orb-weaving spider Uloborus diversus. The assembly reinforces evidence of an ancient arachnid genome duplication and identifies complete open reading frames for every class of spidroin gene, which encode the proteins that are the key structural components of spider silks. We identified the 2 X chromosomes for U. diversus and identify candidate sex-determining loci. This chromosome-level assembly will be a valuable resource for evolutionary research into the origins of orb-weaving, spidroin evolution, chromosomal rearrangement, and chromosomal sex determination in spiders.
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null (Ed.)Abstract Identifying the genetic factors that underlie complex traits is central to understanding the mechanistic underpinnings of evolution. Cave-dwelling Astyanax mexicanus populations are well adapted to subterranean life and many populations appear to have evolved troglomorphic traits independently, while the surface-dwelling populations can be used as a proxy for the ancestral form. Here we present a high-resolution, chromosome-level surface fish genome, enabling the first genome-wide comparison between surface fish and cavefish populations. Using this resource, we performed quantitative trait locus (QTL) mapping analyses and found new candidate genes for eye loss such as dusp26 . We used CRISPR gene editing in A. mexicanus to confirm the essential role of a gene within an eye size QTL, rx3 , in eye formation. We also generated the first genome-wide evaluation of deletion variability across cavefish populations to gain insight into this potential source of cave adaptation. The surface fish genome reference now provides a more complete resource for comparative, functional and genetic studies of drastic trait differences within a species.more » « less
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Abstract The present contribution addresses the phylogeny and biogeography of the pantropical whip spider family Charinidae Quintero, 1986, the most species-rich in the arachnid order Amblypygi Thorell, 1883, based on morphology and multilocus DNA sequences, analysed simultaneously using parsimony, maximum likelihood and Bayesian inference. The morphological matrix comprises 138 characters, scored for four outgroup taxa and 103 ingroup terminals representing all genera and 64% of the species of Charinidae. The multilocus dataset comprises sequences from two nuclear and three mitochondrial gene loci for four outgroup taxa and 48 ingroup representing 30 (23%) taxa of Charinidae. Charinidae are monophyletic, with Weygoldtia Miranda et al., 2018 sister to a monophyletic group comprising Charinus Simon, 1892 and Sarax Simon, 1892, neither of which are reciprocally monophyletic. Charinidae diverged from other amblypygid families in the Late Carboniferous, c. 318 Mya, on the supercontinent Pangaea. Weygoldtia diverged from the common ancestor of Charinus and Sarax during the Late Permian, c. 257 Mya, when changes in climate reduced tropical forests. The divergence of Charinus and Sarax coincides with the fragmentation of Pangaea, c. 216 Mya. Sarax colonized South-East Asia via Australia. The charinid fauna of New Caledonia originated before the Oligocene, when the island separated from Australia, c. 80 Mya.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1186/s12864-020-07149-x
