Abstract
BackgroundChondrichthyans represent a monophyletic group of crown group gnathostomes and are central to our understanding of vertebrate evolution. Like all vertebrates, cartilaginous fishes evolved concretions of material within their inner ears to aid with equilibrium and balance detection. Up to now, these materials have been identified as calcium carbonate-bearing otoconia, which are small bio-crystals consisting of an inorganic mineral and a protein, or otoconial masses (aggregations of otoconia bound by an organic matrix), being significantly different in morphology compared to the singular, polycrystalline otolith structures of bony fishes, which are solidified bio-crystals forming stony masses. Reinvestigation of the morphological and chemical properties of these chondrichthyan otoconia revises our understanding of otolith composition and has implications on the evolution of these characters in both the gnathostome crown group, and cartilaginous fishes in particular.ResultsDissections of Amblyraja radiata, Potamotrygon leopoldi, and Scyliorhinus canicula revealed three pairs of singular polycrystalline otolith structures with a well-defined morphology within their inner ears, as observed in bony fishes. IR spectroscopy identified the material to be composed of carbonate/collagen-bearing apatite in all taxa. These findings contradict previous hypotheses suggesting these otoconial structures were composed of calcium carbonate in chondrichthyans. A phylogenetic mapping using 37 chondrichthyan taxa further showed that the acquisition of phosphatic otolith structures might be widespread within cartilaginous fishes.ConclusionsDifferences in the size and shape of otoliths between taxa indicate a taxonomic signal within elasmobranchs. Otoliths made of carbonate/collagen-bearing apatite are reported for the first time in chondrichthyans. The intrinsic pathways to form singular, polycrystalline otoliths may represent the plesiomorphic condition for vertebrates but needs further testing. Likewise, the phosphatic composition of otoliths in early vertebrates such as cyclostomes and elasmobranchs is probably closely related to the lack of bony tissue in these groups, supporting a close relationship between skeletal tissue mineralization patterns and chemical otolith composition, underlined by physiological constraints.
Highlights
Chondrichthyans represent a monophyletic group of crown group gnathostomes and are central to our understanding of vertebrate evolution
We found a series of structures within the inner ear, which do not match the descriptions of otoconia but are here instead identified as otoliths
Otolith positioning and morphology During dissection, we found three well-defined otolithic structures in the vestibular cavities of the inner ears of all investigated specimens and extracted these structures from both left and right vestibula of the rays Amblyraja radiata and Potamotrygon leopoldi, and the shark Scyliorhinus canicula, described here for the first time (Fig. 2)
Summary
Chondrichthyans represent a monophyletic group of crown group gnathostomes and are central to our understanding of vertebrate evolution. The inner ear and vestibular system of marine vertebrates contain crystalline biocomposites of calcium carbonate and phosphate phases, which exist either as small separate microparticles (otoconia or statoconia), as an otoconial mass representing loose aggregates of multiple mono-crystals, or forming rigid polycrystalline otoliths (statoliths, “ear-stones”) in actinopterygians [e.g., 11]. These otoliths consist of agglutinated crystals or crystals precipitated around a nucleus that continuously grow forming concentric layers of organic matrix alternating with mineralized layers [12,13,14]. Both otoconia and otoliths can occur simultaneously in aquatic vertebrates [11]
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