Developmental Biology, Animal Science and Zoology, Ecology, Evolution, Behavior and Systematics, Embryology
22
Scopus Publications
Scopus Publications
Genomic, transcriptomic and epigenomic signatures of ageing and cold adaptation in the Antarctic clam Laternula elliptica Victoria A. Sleight, Melody S. Clark, Meghan K. Yap-Chiongco, Frances Turner, Kevin M. Kocot Open Biology, 2025 Genomic data are lacking for most Antarctic marine invertebrates, predicating our ability to understand physiological adaptation and specific life-history traits, such as longevity. The environmental stress response of the Antarctic infaunal clam Laternula elliptica is much diminished in older adult animals compared with younger juvenile individuals. However, the mechanism underlying this reduced capacity is unknown. In this study, we describe and analyse the genome of L. elliptica and use it as a tool to understand transcriptomic responses to shell damage across different age cohorts. Gene expression data were combined with reduced representation enzymic methyl sequencing to identify if methylation was acting as an epigenetic mechanism driving age-dependent transcriptional profiles. Our transcriptomic results demonstrated a clear bipartite molecular response in L. elliptica , associated with a rapid growth phase in juveniles and a stabilization phase in reproductively mature adults. Genes active in the response to damage repair in juvenile animals are silent in adults but can be reactivated after several months following damage stimulus; however, these genes were not methylated. Hence, the trigger for this critical and imprinted change in physiological state is, as yet, unknown. While epigenetics is likely involved in this process, the mechanism is unlikely to be methylation.
A pre-vertebrate endodermal origin of calcitonin-producing neuroendocrine cells Jenaid M. Rees, Katie Kirk, Giacomo Gattoni, Dorit Hockman, Victoria A. Sleight, Dylan J. Ritter, Èlia Benito-Gutierrez, Ela W. Knapik, J. Gage Crump, Peter Fabian, J. Andrew Gillis Development Cambridge, 2024 Vertebrate calcitonin-producing cells (C-cells) are neuroendocrine cells that secrete the small peptide hormone calcitonin in response to elevated blood calcium levels. Whereas mouse C-cells reside within the thyroid gland and derive from pharyngeal endoderm, avian C-cells are located within ultimobranchial glands and have been reported to derive from the neural crest. We use a comparative cell lineage tracing approach in a range of vertebrate model systems to resolve the ancestral embryonic origin of vertebrate C-cells. We find, contrary to previous studies, that chick C-cells derive from pharyngeal endoderm, with neural crest-derived cells instead contributing to connective tissue intimately associated with C-cells in the ultimobranchial gland. This endodermal origin of C-cells is conserved in a ray-finned bony fish (zebrafish) and a cartilaginous fish (the little skate, Leucoraja erinacea). Furthermore, we discover putative C-cell homologs within the endodermally-derived pharyngeal epithelium of the ascidian Ciona intestinalis and the amphioxus Branchiostoma lanceolatum, two invertebrate chordates that lack neural crest cells. Our findings point to a conserved endodermal origin of C-cells across vertebrates and to a pre-vertebrate origin of this cell type along the chordate stem.
Cell type and gene regulatory network approaches in the evolution of spiralian biomineralisation Victoria A Sleight Briefings in Functional Genomics, 2023 Biomineralisation is the process by which living organisms produce hard structures such as shells and bone. There are multiple independent origins of biomineralised skeletons across the tree of life. This review gives a glimpse into the diversity of spiralian biominerals and what they can teach us about the evolution of novelty. It discusses different levels of biological organisation that may be informative to understand the evolution of biomineralisation and considers the relationship between skeletal and non-skeletal biominerals. More specifically, this review explores if cell type and gene regulatory network approaches could enhance our understanding of the evolutionary origins of biomineralisation.
The little skate genome and the evolutionary emergence of wing-like fins Ferdinand Marlétaz, Elisa de la Calle-Mustienes, Rafael D. Acemel, Christina Paliou, Silvia Naranjo, Pedro Manuel Martínez-García, Ildefonso Cases, Victoria A. Sleight, Christine Hirschberger, Marina Marcet-Houben, Dina Navon, Ali Andrescavage, Ksenia Skvortsova, Paul Edward Duckett, Álvaro González-Rajal, Ozren Bogdanovic, Johan H. Gibcus, Liyan Yang, Lourdes Gallardo-Fuentes, Ismael Sospedra, Javier Lopez-Rios, Fabrice Darbellay, Axel Visel, Job Dekker, Neil Shubin, Toni Gabaldón, Tetsuya Nakamura, Juan J. Tena, Darío G. Lupiáñez, Daniel S. Rokhsar, José Luis Gómez-Skarmeta Nature, 2023 Skates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments1,2. However, the molecular underpinnings of this unique trait remain unclear. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins—including gene expression, chromatin occupancy and three-dimensional conformation—we find skate-specific genomic rearrangements that alter the three-dimensional regulatory landscape of genes that are involved in the planar cell polarity pathway. Functional inhibition of planar cell polarity signalling resulted in a reduction in anterior fin size, confirming that this pathway is a major contributor to batoid fin morphology. We also identified a fin-specific enhancer that interacts with several hoxa genes, consistent with the redeployment of hox gene expression in anterior pectoral fins, and confirmed its potential to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganization and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait.
Ectodermal Wnt signaling, cell fate determination, and polarity of the skate gill arch skeleton Jenaid M Rees, Victoria A Sleight, Stephen J Clark, Tetsuya Nakamura, J Andrew Gillis Elife, 2023 The gill skeleton of cartilaginous fishes (sharks, skates, rays, and holocephalans) exhibits a striking anterior–posterior polarity, with a series of fine appendages called branchial rays projecting from the posterior margin of the gill arch cartilages. We previously demonstrated in the skate (Leucoraja erinacea) that branchial rays derive from a posterior domain of pharyngeal arch mesenchyme that is responsive to Sonic hedgehog (Shh) signaling from a distal gill arch epithelial ridge (GAER) signaling centre. However, how branchial ray progenitors are specified exclusively within posterior gill arch mesenchyme is not known. Here, we show that genes encoding several Wnt ligands are expressed in the ectoderm immediately adjacent to the skate GAER, and that these Wnt signals are transduced largely in the anterior arch environment. Using pharmacological manipulation, we show that inhibition of Wnt signalling results in an anterior expansion of Shh signal transduction in developing skate gill arches, and in the formation of ectopic anterior branchial ray cartilages. Our findings demonstrate that ectodermal Wnt signalling contributes to gill arch skeletal polarity in skate by restricting Shh signal transduction and chondrogenesis to the posterior arch environment and highlights the importance of signalling interactions at embryonic tissue boundaries for cell fate determination in vertebrate pharyngeal arches.
Evolutionary conservation and divergence of the transcriptional regulation of bivalve shell secretion across life-history stages Alessandro Cavallo, Melody S. Clark, Lloyd S. Peck, Elizabeth M. Harper, Victoria A. Sleight Royal Society Open Science, 2022 Adult molluscs produce shells with diverse morphologies and ornamentations, different colour patterns and microstructures. The larval shell, however, is a phenotypically more conserved structure. How do developmental and evolutionary processes generate varying diversity at different life-history stages within a species? Using live imaging, histology, scanning electron microscopy and transcriptomic profiling, we have described shell development in a heteroconchian bivalve, the Antarctic clam, Laternula elliptica, and compared it to adult shell secretion processes in the same species . Adult downstream shell genes, such as those encoding extracellular matrix proteins and biomineralization enzymes, were largely not expressed during shell development. Instead, a development-specific downstream gene repertoire was expressed. Upstream regulatory genes such as transcription factors and signalling molecules were largely conserved between developmental and adult shell secretion. Comparing heteroconchian data with recently reported pteriomorphian larval shell development data suggests that, despite being phenotypically more conserved, the downstream effectors constituting the larval shell ‘tool-kit’ may be as diverse as that of adults. Overall, our new data suggest that a larval shell formed using development-specific downstream effector genes is a conserved and ancestral feature of the bivalve lineage, and possibly more broadly across the molluscs.
ACME dissociation: a versatile cell fixation-dissociation method for single-cell transcriptomics Helena García-Castro, Nathan J. Kenny, Marta Iglesias, Patricia Álvarez-Campos, Vincent Mason, Anamaria Elek, Anna Schönauer, Victoria A. Sleight, Jakke Neiro, Aziz Aboobaker, Jon Permanyer, Manuel Irimia, Arnau Sebé-Pedrós, Jordi Solana Genome Biology, 2021 Single-cell sequencing technologies are revolutionizing biology, but they are limited by the need to dissociate live samples. Here, we present ACME (ACetic-MEthanol), a dissociation approach for single-cell transcriptomics that simultaneously fixes cells. ACME-dissociated cells have high RNA integrity, can be cryopreserved multiple times, and are sortable and permeable. As a proof of principle, we provide single-cell transcriptomic data of different species, using both droplet-based and combinatorial barcoding single-cell methods. ACME uses affordable reagents, can be done in most laboratories and even in the field, and thus will accelerate our knowledge of cell types across the tree of life.
Conserved and unique transcriptional features of pharyngeal arches in the skate (Leucoraja erinacea) and evolution of the jaw Christine Hirschberger, Victoria A Sleight, Katharine E Criswell, Stephen J Clark, J Andrew Gillis Molecular Biology and Evolution, 2021 The origin of the jaw is a long-standing problem in vertebrate evolutionary biology. Classical hypotheses of serial homology propose that the upper and lower jaw evolved through modifications of dorsal and ventral gill arch skeletal elements, respectively. If the jaw and gill arches are derived members of a primitive branchial series, we predict that they would share common developmental patterning mechanisms. Using candidate and RNAseq/differential gene expression analyses, we find broad conservation of dorsoventral (DV) patterning mechanisms within the developing mandibular, hyoid, and gill arches of a cartilaginous fish, the skate (Leucoraja erinacea). Shared features include expression of genes encoding members of the ventralizing BMP and endothelin signaling pathways and their effectors, the joint markers nkx3.2 and gdf5 and prochondrogenic transcription factor barx1, and the dorsal territory marker pou3f3. Additionally, we find that mesenchymal expression of eya1/six1 is an ancestral feature of the mandibular arch of jawed vertebrates, whereas differences in notch signaling distinguish the mandibular and gill arches in skate. Comparative transcriptomic analyses of mandibular and gill arch tissues reveal additional genes differentially expressed along the DV axis of the pharyngeal arches, including scamp5 as a novel marker of the dorsal mandibular arch, as well as distinct transcriptional features of mandibular and gill arch muscle progenitors and developing gill buds. Taken together, our findings reveal conserved patterning mechanisms in the pharyngeal arches of jawed vertebrates, consistent with serial homology of their skeletal derivatives, as well as unique transcriptional features that may underpin distinct jaw and gill arch morphologies.
Deciphering mollusc shell production: the roles of genetic mechanisms through to ecology, aquaculture and biomimetics Melody S. Clark, Lloyd S. Peck, Jaison Arivalagan, Thierry Backeljau, Sophie Berland, Joao C. R. Cardoso, Carlos Caurcel, Gauthier Chapelle, Michele De Noia, Sam Dupont, Karim Gharbi, Joseph I. Hoffman, Kim S. Last, Arul Marie, Frank Melzner, Kati Michalek, James Morris, Deborah M. Power, Kirti Ramesh, Trystan Sanders, Kirsikka Sillanpää, Victoria A. Sleight, Phoebe J. Stewart‐Sinclair, Kristina Sundell, Luca Telesca, David L. J. Vendrami, Alexander Ventura, Thomas A. Wilding, Tejaswi Yarra, Elizabeth M. Harper Biological Reviews, 2020 Most molluscs possess shells, constructed from a vast array of microstructures and architectures. The fully formed shell is composed of calcite or aragonite. These CaCO3 crystals form complex biocomposites with proteins, which although typically less than 5% of total shell mass, play significant roles in determining shell microstructure. Despite much research effort, large knowledge gaps remain in how molluscs construct and maintain their shells, and how they produce such a great diversity of forms. Here we synthesize results on how shell shape, microstructure, composition and organic content vary among, and within, species in response to numerous biotic and abiotic factors. At the local level, temperature, food supply and predation cues significantly affect shell morphology, whilst salinity has a much stronger influence across latitudes. Moreover, we emphasize how advances in genomic technologies [e.g. restriction site‐associated DNA sequencing (RAD‐Seq) and epigenetics] allow detailed examinations of whether morphological changes result from phenotypic plasticity or genetic adaptation, or a combination of these. RAD‐Seq has already identified single nucleotide polymorphisms associated with temperature and aquaculture practices, whilst epigenetic processes have been shown significantly to modify shell construction to local conditions in, for example, Antarctica and New Zealand. We also synthesize results on the costs of shell construction and explore how these affect energetic trade‐offs in animal metabolism. The cellular costs are still debated, with CaCO3 precipitation estimates ranging from 1–2 J/mg to 17–55 J/mg depending on experimental and environmental conditions. However, organic components are more expensive (~29 J/mg) and recent data indicate transmembrane calcium ion transporters can involve considerable costs. This review emphasizes the role that molecular analyses have played in demonstrating multiple evolutionary origins of biomineralization genes. Although these are characterized by lineage‐specific proteins and unique combinations of co‐opted genes, a small set of protein domains have been identified as a conserved biomineralization tool box. We further highlight the use of sequence data sets in providing candidate genes for in situ localization and protein function studies. The former has elucidated gene expression modularity in mantle tissue, improving understanding of the diversity of shell morphology synthesis. RNA interference (RNAi) and clustered regularly interspersed short palindromic repeats ‐ CRISPR‐associated protein 9 (CRISPR‐Cas9) experiments have provided proof of concept for use in the functional investigation of mollusc gene sequences, showing for example that Pif (aragonite‐binding) protein plays a significant role in structured nacre crystal growth and that the Lsdia1 gene sets shell chirality in Lymnaea stagnalis. Much research has focused on the impacts of ocean acidification on molluscs. Initial studies were predominantly pessimistic for future molluscan biodiversity. However, more sophisticated experiments incorporating selective breeding and multiple generations are identifying subtle effects and that variability within mollusc genomes has potential for adaption to future conditions. Furthermore, we highlight recent historical studies based on museum collections that demonstrate a greater resilience of molluscs to climate change compared with experimental data. The future of mollusc research lies not solely with ecological investigations into biodiversity, and this review synthesizes knowledge across disciplines to understand biomineralization. It spans research ranging from evolution and development, through predictions of biodiversity prospects and future‐proofing of aquaculture to identifying new biomimetic opportunities and societal benefits from recycling shell products.
The deep sea is a major sink for microplastic debris Lucy C. Woodall, Anna Sanchez-Vidal, Miquel Canals, Gordon L.J. Paterson, Rachel Coppock, Victoria Sleight, Antonio Calafat, Alex D. Rogers, Bhavani E. Narayanaswamy, Richard C. Thompson Royal Society Open Science, 2014
Contaminants, Pollution and Potential Anthropogenic Impacts in Chagos/BIOT James W. Readman, Francis DeLuna, Ralf Ebinghaus, AntenorNestor Guzman, Andrew R. G. Price, Emily E. Readman, Anne L. S. Sheppard, Victoria A. Sleight, Renate Sturm, Richard C. Thompson, Andrew Tonkin, Hendrik Wolschke, Robyn J. Wright, Charles R. C. Sheppard Coral Reefs of the World, 2013
