Big insight from the little skate: Leucoraja erinacea as a developmental model system

Gillis, J. Andrew; Bennett, Scott; Criswell, Katharine E.; Rees, Jenaid; Sleight, Victoria A.; Hirschberger, Christine; Calzarette, Dan; Kerr, Sarah E.; Dasen, Jeremy S.

doi:10.1016/bs.ctdb.2021.12.016

Cited by 6 publications

(7 citation statements)

References 68 publications

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“…All extant jawed vertebrates belong to one of two lineages: bony vertebrates (including bony fishes and tetrapods) and cartilaginous fishes (sharks, skates, rays and holocephalans). To test whether an endodermal origin of C-cells is conserved in cartilaginous fishes, we carried out a series of cell lineage tracing experiments in a cartilaginous fish outgroup to the bony vertebrates, the little skate ( Leucoraja erinacea ) 44 . In skate embryos, UBs are located between the caudal gill arches and the pectoral girdle (Fig.…”

Section: Resultsmentioning

confidence: 99%

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A pre-vertebrate endodermal origin of calcitonin-producing neuroendocrine cells

Rees,

Kirk,

Gattoni

et al. 2024

Preprint

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SummaryVertebrate calcitonin-producing cells (C-cells) are neuroendocrine cells that secrete the small peptide hormone calcitonin in response to elevated blood calcium levels. C-cells are crucial for maintenance of calcium homeostasis, yet the embryonic and evolutionary origins of this cell type remain contentious. Whereas mouse C-cells reside within the thyroid gland and derive from pharyngeal endoderm, avian C-cells are located within ultimobranchial glands and were 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 homologues within the endodermally-derived pharyngeal epithelium of the ascidianCiona intestinalisand the amphioxusBranchiostoma 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.

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Section: Resultsmentioning

confidence: 99%

“…Skate ( L. erinacea ) embryos were obtained from the Marine Resources Center at the Marine Biological Laboratory (MBL) in Woods Hole, MA, U.S.A., were reared and stages as described in Gillis et al (2022) 44 . All skate experiments were conducted according to protocols approved by the Institutional Animal Care and Use Committee of the MBL.…”

Section: Methodsmentioning

confidence: 99%

A pre-vertebrate endodermal origin of calcitonin-producing neuroendocrine cells

Rees,

Kirk,

Gattoni

et al. 2024

Preprint

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“…Although several studies have called for a reliable phylogenetic hypothesis of skates [10], the monophyly within these two (and further) rajid genera has not yet been examined comprehensively, neither morphologically nor genetically. Several studies from different fields of research have focused on a single species, particularly the model organism L. erinacea (Mitchill, 1825) [11][12][13][14], as well as L. naevus (Müller and Henle, 1841) [15]. Phylogenetic studies examining Leucoraja or Rajella species include those by McEachran and Dunn [8], Turan [16], Aschliman et al [17], Naylor et al [18,19], Chiquillo et al [20], and Lynghammar et al [21].…”

Section: Introductionmentioning

confidence: 99%

Description of a Remarkable New Skate Species of Leucoraja Malm, 1877 (Rajiformes, Rajidae) from the Southwestern Indian Ocean: Introducing 3D Modeling as an Innovative Tool for the Visualization of Clasper Characters

Weigmann,

Stehmann,

Séret

et al. 2024

Biology

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A remarkable new deep-water skate, Leucoraja longirostris n. sp., is described based on eight specimens caught during different expeditions to the southern Madagascar Ridge in the southwestern Indian Ocean. The new species differs from all congeners by its remarkably long and acutely angled snout (horizontal preorbital length 17.2–22.6% TL vs. 8.5–11.9% TL and 4.2–6.1 vs. 1.7–3.5 times orbit length, snout angle 65–85° vs. 90–150°). Furthermore, it is apparently endemic to the Madagascar Ridge, distant from the known distribution areas of all congeners. In addition to L. fullonica and L. pristispina, L. longirostris n. sp. is also the only species with plain dorsal coloration. Furthermore, the new species is the only Leucoraja species with an external clasper component dike and, besides L. wallacei, the only one with four dorsal terminal (dt) cartilages. The shape of the accessory terminal 1 (at1) cartilage with four tips is also unique within the genus. A new approach for the visualization of the clasper characters is introduced based on 3D models of all skeletal and external features. This enables a much easier and much more precise interpretation of every single clasper component, of the entire structure, and, in particular, the relationship between external features and skeletal cartilages. A new English translation of the first diagnosis of Leucoraja is provided, along with a revised generic diagnosis and a key to the species of Leucoraja in the Indian Ocean.

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“…While aspects of elasmobranch development have long been of interest, 13,14 publications featuring developmental staging series tracking the growth of elasmobranchs have only appeared in the past 30 years. including the small-spotted catshark Scyliorhinus canicula, 15,16 the winter skate Leucoraja ocellata, 17 the little skate Leucoraja erinacea, 18 the Atlantic sharpnose Rhizoprionodon terraenovae, 19 the brownbanded bamboo shark Chiloscyllium punctata, 20 and the frilled shark Chlamydoselachus anguineus. 21 Such work has been particularly valuable for the catshark and little skate, which have become popular models in experimental biology, in part because their eggs can be easily produced, collected, maintained, and observed in captivity, 18,22,23 making them widely used in multiple studies.…”

Section: Introductionmentioning

confidence: 99%

“…including the small-spotted catshark Scyliorhinus canicula, 15,16 the winter skate Leucoraja ocellata, 17 the little skate Leucoraja erinacea, 18 the Atlantic sharpnose Rhizoprionodon terraenovae, 19 the brownbanded bamboo shark Chiloscyllium punctata, 20 and the frilled shark Chlamydoselachus anguineus. 21 Such work has been particularly valuable for the catshark and little skate, which have become popular models in experimental biology, in part because their eggs can be easily produced, collected, maintained, and observed in captivity, 18,22,23 making them widely used in multiple studies. Developmental staging series allows for the identification of emerging features for experimentation and provide a comparative reference for other published work.…”

Section: Introductionmentioning

confidence: 99%

Embryonic development in the bonnethead (Sphyrna tiburo), a viviparous hammerhead shark

Byrum,

Frazier,

Grubbs

et al. 2023

Developmental Dynamics

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BackgroundThe hammerhead sharks (family Sphyrnidae) are an immediately recognizable group of sharks due to their unique head shape. Though there has long been an interest in hammerhead development, there are currently no explicit staging tables published for any members of the group. The bonnethead Sphyrna tiburo is the smallest member of Sphyrnidae and is abundant in estuarine and nearshore waters in the Gulf of Mexico and Western North Atlantic Ocean. Due to their relative abundance, close proximity to shore, and brief gestation period, it has been possible to collect and document multiple embryonic specimens at progressive stages of development.ResultsWe present the first comprehensive embryonic staging series for the Bonnethead, a viviparous hammerhead shark. Our stage series covers a period of development from stages that match the vertebrate phylotypic period, from Stage 23, through stages of morphological divergence to complete development at birth—Stage 35). Notably, we use a variety of techniques to document crucial stages that lead to their extreme craniofacial diversity, resulting in the formation of one of the most distinctive characters of any shark species, the cephalofoil or hammer‐like head.ConclusionDocumenting the development of hard‐to‐access vertebrates, like this viviparous shark species, offers important information about how new and diverse morphologies arise that otherwise may remain poorly studied. This work will serve as a platform for future comparative developmental research both within sharks and across the phylogeny of vertebrates, underpinning the extreme potential of craniofacial development and morphological diversity in vertebrate animals.

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Big insight from the little skate: Leucoraja erinacea as a developmental model system

Cited by 6 publications

References 68 publications

A pre-vertebrate endodermal origin of calcitonin-producing neuroendocrine cells

A pre-vertebrate endodermal origin of calcitonin-producing neuroendocrine cells

Description of a Remarkable New Skate Species of Leucoraja Malm, 1877 (Rajiformes, Rajidae) from the Southwestern Indian Ocean: Introducing 3D Modeling as an Innovative Tool for the Visualization of Clasper Characters

Embryonic development in the bonnethead (Sphyrna tiburo), a viviparous hammerhead shark

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