Conserved and unique transcriptional features of pharyngeal arches in the skate (Leucoraja erinacea) and evolution of the jaw

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hirschberger, C., Sleight, V. A., Criswell, K. E., Clark, S. J., & Gillis, J. A. Conserved and unique transcriptional features of pharyngeal arches in the skate (Leucoraja erinacea) and evolution of the jaw. Molecular Biology and Evolution, (2021): msab123, https://doi.org/10.1093/molbev/msab123The 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 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 ventralising BMP and endothelin signalling pathways and their effectors, the joint markers nkx3.2 and gdf5 and pro-chondrogenic 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, while differences in notch signalling distinguish the mandibular and gill arches in skate. Comparative transcriptomic analyses of mandibular and gill arch tissues reveal additional genes differentially expressed along the dorsoventral 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.This work was supported by a Biotechnology and Biological Sciences Research Council Doctoral Training Partnership studentship to CH, by a Wolfson College Junior Research Fellowship and MBL Whitman Early Career Fellowship to VAS, and by a Royal Society University Research Fellowship (UF130182 and URF\R\191007), Royal Society Research Grant (RG140377) and University of Cambridge Sir Isaac Newton Trust Grant (14.23z) to JAG

Extraocular, rod-like photoreceptors in a flatworm express xenopsin photopigment.

Animals detect light using opsin photopigments. Xenopsin, a recently classified subtype of opsin, challenges our views on opsin and photoreceptor evolution. Originally thought to belong to the Gαi-coupled ciliary opsins, xenopsins are now understood to have diverged from ciliary opsins in pre-bilaterian times, but little is known about the cells that deploy these proteins, or if they form a photopigment and drive phototransduction. We characterized xenopsin in a flatworm, Maritigrella crozieri, and found it expressed in ciliary cells of eyes in the larva, and in extraocular cells around the brain in the adult. These extraocular cells house hundreds of cilia in an intra-cellular vacuole (phaosome). Functional assays in human cells show Maritigrella xenopsin drives phototransduction primarily by coupling to Gαi. These findings highlight similarities between xenopsin and c-opsin and reveal a novel type of opsin-expressing cell that, like jawed vertebrate rods, encloses the ciliary membrane within their own plasma membrane

A symmoriiform chondrichthyan braincase and the origin of chimaeroid fishes

Chimaeroid fishes (Holocephali) are one of the four principal divisions of modern gnathostomes (jawed vertebrates). Despite only 47 described living species1, chimaeroids are the focus of resurgent interest as potential archives of genomic data2 and for the unique perspective they provide on chondrichthyan and gnathostome ancestral conditions. Chimaeroids are also noteworthy for their highly derived body plan1,3,4. However, like other living groups with distinctive anatomies5, fossils have been of limited use in unravelling their evolutionary origin, as the earliest recognized examples already exhibit many of the specializations present in modern forms6,7. Here we report the results of a computed tomography analysis of Dwykaselachus, an enigmatic chondrichthyan braincase from the ~280 million year old Karoo sediments of South Africa8. Externally, the braincase is that of a symmoriid shark9,10,11,12,13and is by far the most complete uncrushed example yet discovered. Internally, the morphology exhibits otherwise characteristically chimaeroid specializations, including the otic labyrinth arrangement and the brain space configuration relative to exceptionally large orbits. These results have important implications for our view of modern chondrichthyan origins, add robust structure to the phylogeny of early crown group gnathostomes, reveal preconditions that suggest an initial morpho-functional basis for the derived chimaeroid cranium, and shed new light on the chondrichthyan response to the extinction at the end of the Devonian period

Figure 52. Character states for character 32 in The comparative osteology and phylogenetic relationships of African and South American lungfishes (Sarcopterygii: Dipnoi)

Figure 52. Character states for character 32 (contact between prearticular tooth plates). Prearticular in ventral view of: A, Neoceratodus forsteri, AMS I-40438-001; B, †Arganodus atlantis, KU 60710; and C, Protopterus aethiopicus, UF 137272. Anterior is to the top. †Dagger symbol represents extinct taxa. Scale bars: 5 mm.Published as part of <i>Criswell, Katharine E., 2015, The comparative osteology and phylogenetic relationships of African and South American lungfishes (Sarcopterygii: Dipnoi), pp. 801-858 in Zoological Journal of the Linnean Society 174 (4)</i> on page 851, DOI: 10.1111/zoj.12255, <a href="http://zenodo.org/record/10107235">http://zenodo.org/record/10107235</a&gt

Figure 27 in The comparative osteology and phylogenetic relationships of African and South American lungfishes (Sarcopterygii: Dipnoi)

Figure 27. Left suboperculum of Protopterus annectens, TMM M 2494: A, lateral view, anterior to the left; B, medial view, anterior to the right. Scale bar: 5 mm.Published as part of <i>Criswell, Katharine E., 2015, The comparative osteology and phylogenetic relationships of African and South American lungfishes (Sarcopterygii: Dipnoi), pp. 801-858 in Zoological Journal of the Linnean Society 174 (4)</i> on page 831, DOI: 10.1111/zoj.12255, <a href="http://zenodo.org/record/10107235">http://zenodo.org/record/10107235</a&gt

Figure 4 in The comparative osteology and phylogenetic relationships of African and South American lungfishes (Sarcopterygii: Dipnoi)

Figure 4. Computed tomography reconstruction of the skull of Protopterus amphibius, CAS 47408: A, lateral view; B, dorsal view. Scale bar: 10 mm. DE, dermal ethmoid; EO, exoccipital; FP, frontoparietal; PS, parasphenoid; PT, pterygoid; PTTa, anterior ridge of pterygoid tooth plate; PTTb, middle ridge of pterygoid tooth plate; PTTc, posterior ridge of pterygoid tooth plate; S, supraorbital; SQ, squamosal; V, vomerine tooth.Published as part of <i>Criswell, Katharine E., 2015, The comparative osteology and phylogenetic relationships of African and South American lungfishes (Sarcopterygii: Dipnoi), pp. 801-858 in Zoological Journal of the Linnean Society 174 (4)</i> on page 810, DOI: 10.1111/zoj.12255, <a href="http://zenodo.org/record/10107235">http://zenodo.org/record/10107235</a&gt

Figure 41 in The comparative osteology and phylogenetic relationships of African and South American lungfishes (Sarcopterygii: Dipnoi)

Figure 41. Left cleithrum and clavicle of Protopterus annectens, TMM M 2494: A, anterolateral view, anterior to the left; B, posteromedial view, anterior to the right. Scale bar: 5 mm. CL, cleithrum; CLA, clavicle.Published as part of <i>Criswell, Katharine E., 2015, The comparative osteology and phylogenetic relationships of African and South American lungfishes (Sarcopterygii: Dipnoi), pp. 801-858 in Zoological Journal of the Linnean Society 174 (4)</i> on page 843, DOI: 10.1111/zoj.12255, <a href="http://zenodo.org/record/10107235">http://zenodo.org/record/10107235</a&gt