Homeobox genes are key toolkit genes that regulate the development of metazoans and changes in their regulation and copy number have contributed to the evolution of phenotypic diversity. We recently identified a whole genome duplication (WGD) event that occurred in an ancestor of spiders and scorpions (Arachnopulmonata), and that many homeobox genes, including two Hox clusters, appear to have been retained in arachnopulmonates. To better understand the consequences of this ancient WGD and the evolution of arachnid homeobox genes, we have characterized and compared the homeobox repertoires in a range of arachnids. We found that many families and clusters of these genes are duplicated in all studied arachnopulmonates (Parasteatoda tepidariorum, Pholcus phalangioides, Centruroides sculpturatus, and Mesobuthus martensii) compared with nonarachnopulmonate arachnids (Phalangium opilio, Neobisium carcinoides, Hesperochernes sp., and Ixodes scapularis). To assess divergence in the roles of homeobox ohnologs, we analyzed the expression of P. tepidariorum homeobox genes during embryogenesis and found pervasive changes in the level and timing of their expression. Furthermore, we compared the spatial expression of a subset of P. tepidariorum ohnologs with their single copy orthologs in P. opilio embryos. We found evidence for likely subfunctionlization and neofunctionalization of these genes in the spider. Overall our results show a high level of retention of homeobox genes in spiders and scorpions post-WGD, which is likely to have made a major contribution to their developmental evolution and diversification through pervasive subfunctionlization and neofunctionalization, and paralleling the outcomes of WGD in vertebrates.
Animal visual systems are enormously diverse, but their development appears to be controlled by a set of conserved retinal determination genes (RDGs). Spiders are particular masters of visual system innovation, and offer an excellent opportunity to study the evolution of animal eyes. Several RDGs have been identified in spider eye primordia, but their interactions and regulation remain unclear. From our knowledge of RDG network regulation in Drosophila melanogaster, we hypothesize that orthologs of Pax6, eyegone, Wnt genes, hh, dpp, and atonal could play important roles in controlling eye development in spiders. We analyzed the expression of these genes in developing embryos of the spider Parasteatodatepidariorum, both independently and in relation to the eye primordia, marked using probes for the RDG sine oculis. Our results support conserved roles for Wnt genes in restricting the size and position of the eye field, as well as for atonal initiating photoreceptor differentiation. However, we found no strong evidence for an upstream role of Pax6 in eye development, despite its label as a master regulator of animal eye development; nor do eyg, hh or dpp compensate for the absence of Pax6. Conversely, our results indicate that hh may work with Wnt signaling to restrict eye growth, a role similar to that of Sonichedgehog (Shh) in vertebrates.
The Sox family of transcription factors regulate many processes during metazoan development, including stem cell maintenance and nervous system specification. Characterising the repertoires and roles of these genes can therefore provide important insights into animal evolution and development. We further characterised the Sox repertoires of several arachnid species with and without an ancestral whole genome duplication (WGD), and compared their expression between the spider Parasteatoda tepidariorum and the harvestman Phalangium opilio. We also found that most Sox families have been retained as ohnologs after WGD and evidence for potential subfunctionalization and/or neofunctionalization events. Our results also suggest that Sox21b-1 likely regulated segmentation ancestrally in arachnids, playing a similar role to the closely related SoxB gene, Dichaete, in insects. We previously showed that Sox21b-1 is required for the simultaneous formation of prosomal segments and sequential addition of opisthosomal segments in P. tepidariorum. We studied the expression and function of Sox21b-1 further in this spider and found that while this gene regulates the generation of both prosomal and opisthosomal segments, it plays different roles in the formation of these tagmata reflecting their contrasting modes of segmentation and deployment of gene regulatory networks with different architectures.
Spiders are a diverse order of chelicerates that diverged from other arthropods over 500 million years ago. Research on spider embryogenesis has made important contributions to understanding the evolution of animal development. In particular, studies of the common house spider Parasteatoda tepidariorum using developmental candidate gene approaches have provided key insights into the regulation and evolution of many processes including axis formation, segmentation and patterning. However, there remains a paucity of knowledge about the cells that build spider embryos, their gene expression profiles and fate. Single-cell transcriptomic analyses have been revolutionary in describing these complex landscapes of cellular genetics in a range of animals. Therefore, we carried out single-cell RNA sequencing of P. tepidariorum embryos at stages 7, 8 and 9, which encompass the establishment and patterning of the body plan, and initial differentiation of many tissues and organs. We identified 23 cell clusters marked by many developmental toolkit genes, as well as a plethora of non-candidate genes not previously investigated. We found many Hox genes were markers of cell clusters, and Hox gene paralogs often were present in different clusters. This provided further evidence of sub- and/or neo-functionalisation of these important developmental genes after the whole genome duplication in the arachnopulmonate ancestor. We also examined the spatial expression of marker genes for each cluster to generate a comprehensive cell atlas of these embryonic stages. This revealed new insights into the cellular basis and genetic regulation of head patterning, hematopoiesis, limb development, gut development and posterior segmentation. This atlas will serve as a platform for future analysis of spider cell specification and fate, and the evolution of these processes among animals at cellular resolution.
In the last 240,000 years, males of the Drosophila simulans species clade have evolved striking differences in the morphology of their epandrial posterior lobes and claspers (surstyli). These appendages are used for grasping the female during mating and so their divergence is most likely driven by sexual selection. Mapping studies indicate a highly polygenic and generally additive genetic basis for these morphological differences. However, we have limited understanding of the gene regulatory networks that control the development of genital structures and how they evolved to result in this rapid phenotypic diversification. Here, we used new D. simulans/D. mauritiana introgression lines on chromosome 3L to generate higher resolution maps of posterior lobe and clasper differences between these species. We then carried out RNA-seq on the developing genitalia of both species to identify the expressed genes and those that are differentially expressed between the two species. This allowed us to test the function of expressed positional candidates during genital development in D. melanogaster. We identified several new genes involved in the development and possibly the evolution of these genital structures, including the transcription factors Hairy and Grunge. Furthermore, we discovered that during clasper development Hairy negatively regulates tartan (trn), a gene known to contribute to divergence in clasper morphology. Taken together, our results provide new insights into the regulation of genital development and how this has evolved between species.
Pairs of duplicated genes generally display a combination of conserved expression patterns inherited from their unduplicated ancestor and newly acquired domains. However, how the cis-regulatory architecture of duplicated loci evolves to produce these expression patterns is poorly understood. We have directly examined the gene-regulatory evolution of two tandem duplicates, the Drosophila Ly6 genes CG9336 and CG9338, which arose at the base of the drosophilids between 40 and 60 Ma. Comparing the expression patterns of the two paralogs in four Drosophila species with that of the unduplicated ortholog in the tephritid Ceratitis capitata, we show that they diverged from each other as well as from the unduplicated ortholog. Moreover, the expression divergence appears to have occurred close to the duplication event and also more recently in a lineage-specific manner. The comparison of the tissue-specific cis-regulatory modules (CRMs) controlling the paralog expression in the four Drosophila species indicates that diverse cis-regulatory mechanisms, including the novel tissue-specific enhancers, differential inactivation, and enhancer sharing, contributed to the expression evolution. Our analysis also reveals a surprisingly variable cis-regulatory architecture, in which the CRMs driving conserved expression domains change in number, location, and specificity. Altogether, this study provides a detailed historical account that uncovers a highly dynamic picture of how the paralog expression patterns and their underlying cis-regulatory landscape evolve. We argue that our findings will encourage studying cis-regulatory evolution at the whole-locus level to understand how interactions between enhancers and other regulatory levels shape the evolution of gene expression.
The Sox family of transcription factors regulate many different processes during metazoan development, including stem cell maintenance, nervous system specification and germline development. In addition, it has recently become apparent that SoxB genes are involved in embryonic segmentation in several arthropod species. Segmentation in arthropods occurs in two main ways: long germ animals form all segments at once, best exemplified in the well-studied Drosophila melanogaster system, and short germ animals form anterior segments simultaneously, with posterior segments added sequentially from a segment addition zone. In both D. melanogaster and the short germ beetle Tribolium castaneum, the SoxB gene Dichaete is required for correct segmentation and, more recently, we showed that a close relative of Dichaete, Sox21b-1, is required for the simultaneous formation of prosomal segments and sequential addition of opisthosomal segments in the spider Parasteatoda tepidariorum. Here we further analysed the function and expression of Sox21b-1 in P. tepidariorum. We found that while this gene regulates the generation of both prosomal and opisthosomal segments, it plays different roles in the formation of these tagma reflecting their contrasting modes of segmentation and deployment of gene regulatory networks with different architectures. To further investigate the evolution of Sox genes and their roles we characterised the repertoire of the gene family across several arachnid species with and without an ancestral whole genome duplication, and compared Sox expression between P. tepidariorum and the harvestman Phalangium opilio. The results suggest that Sox21b-1 was likely involved in segmentation ancestrally in arachnids, but that other Sox genes could also regulate this process in these animals. We also found that most Sox families have been retained as duplicates or ohnologs after WGD and evidence for potential subfunctionalisation and/or neofunctionalization events. 4References Akiyama-Oda, Y. and Oda, H. (2003). Early patterning of the spider embryo: a cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells. Development 130, 1735-1747. Akiyama-Oda, Y. and Oda, H. (2006). Axis specification in the spider embryo: Dpp is required for radial-to-axial symmetry transformation and sog for ventral patterning. Development 133, . Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev. Biol. 227, 239-255. Chipman, A. D. (2010). Parallel evolution of segmentation by co-option of ancestral gene regulatory networks. BioEssays 32, 60-70. Clark, E. and Akam, M. (2016). Odd-paired controls frequency doubling in Drosophila segmentation by altering the pair-rule gene regulatory network. Elife 5, e18215. Clark, E. and Peel, A. D. (2018). Evidence for the temporal regulation of insect segmentation by a conserved sequence of transcription factors. Dev. 145, 1-15. Clark, E., Peel, A. D. and Akam, M. (2019). Arthropod segmentation. Dev. 14...
Corresponding authors: msantos-nunes@brookes.ac.uk (MDSN) and amcgregor@brookes.ac.uk (APM). AbstractIn the last 240,000 years, males of the Drosophila simulans species clade have evolved striking differences in the morphology of their epandrial posterior lobes and claspers (surstyli). These changes have most likely been driven by sexual selection and mapping studies indicate a highly polygenic and generally additive genetic basis. However, we have limited understanding of the gene regulatory networks that control the development of genital structures and how they evolved to result in this rapid phenotypic diversification. Here, we used new D. simulans / D. mauritiana introgression lines on chromosome 3L to generate higher resolution maps of posterior lobe and clasper differences between these species. We then carried out RNA-seq on the developing genitalia of both species to identify the genes expressed during this process and those that are differentially expressed between the two species. This allowed us to test the function of expressed positional candidates during genital development in D. melanogaster. We identified several new genes involved in the development and possibly the evolution of these genital structures, including the transcription factors Hairy and Grunge. Furthermore, we discovered that during clasper development Hairy negatively regulates tartan, a gene known to contribute to divergence in clasper morphology. Taken together our results provide new insights into the regulation of genital development and how this evolves between species.
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