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Morphology and evolutionary significance of phosphatic otoliths within the inner ears of cartilaginous fishes (Chondrichthyes).

ABSTRACT: BACKGROUND:Chondrichthyans 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. RESULTS:Dissections 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. CONCLUSIONS:Differences 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.

SUBMITTER: Schnetz L

PROVIDER: S-EPMC6937729 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Morphology and evolutionary significance of phosphatic otoliths within the inner ears of cartilaginous fishes (Chondrichthyes).

Schnetz Lisa L Pfaff Cathrin C Libowitzky Eugen E Johanson Zerina Z Stepanek Rica R Kriwet Jürgen J

BMC evolutionary biology 20191230 1

<h4>Background</h4>Chondrichthyans 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 (aggregation ...[more]

PMID: 31888446

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Project description:Reef fishes support important fisheries throughout the Caribbean, but a combination of factors in the tropics makes otolith microstructure difficult to interpret for age estimation. Therefore, validation of ageing methods, via application of Δ14C is a major research priority. Utilizing known-age otolith material from north Caribbean fishes, we determined that a distinct regional Δ14C chronology exists, differing from coral-based chronologies compiled for ageing validation from a wide-ranging area of the Atlantic and from an otolith-based chronology from the Gulf of Mexico. Our north Caribbean Δ14C chronology established a decline series with narrow prediction intervals that proved successful in ageing validation of three economically important reef fish species. In examining why our north Caribbean Δ14C chronology differed from some of the coral-based Δ14C data reported from the region, we determined differences among study objectives and research design impact Δ14C temporal relationships. This resulted in establishing the first of three important considerations relevant to applying Δ14C chronologies for ageing validation: 1) evaluation of the applicability of original goal/objectives and study design of potential Δ14C reference studies. Next, we determined differences between our Δ14C chronology and those from Florida and the Gulf of Mexico were explained by differences in regional patterns of oceanic upwelling, resulting in the second consideration for future validation work: 2) evaluation of the applicability of Δ14C reference data to the region/location where fish samples were obtained. Lastly, we emphasize the application of our north Caribbean Δ14C chronology should be limited to ageing validation studies of fishes from this region known to inhabit shallow water coral habitat as juveniles. Thus, we note the final consideration to strengthen findings of future age validation studies: 3) use of Δ14C analysis for age validation should be limited to species whose juvenile habitat is known to reflect the regional Δ14C reference chronology.

Dataset Information

Morphology and evolutionary significance of phosphatic otoliths within the inner ears of cartilaginous fishes (Chondrichthyes).

Publications

Morphology and evolutionary significance of phosphatic otoliths within the inner ears of cartilaginous fishes (Chondrichthyes).

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