Abstract
BackgroundPedomorphism is the retention of ancestrally juvenile traits by adults in a descendant taxon. Despite its importance for evolutionary change, there are few examples of a molecular basis for this phenomenon. Notothenioids represent one of the best described species flocks among marine fishes, but their diversity is currently threatened by the rapidly changing Antarctic climate. Notothenioid evolutionary history is characterized by parallel radiations from a benthic ancestor to pelagic predators, which was accompanied by the appearance of several pedomorphic traits, including the reduction of skeletal mineralization that resulted in increased buoyancy.ResultsWe compared craniofacial skeletal development in two pelagic notothenioids, Chaenocephalus aceratus and Pleuragramma antarcticum, to that in a benthic species, Notothenia coriiceps, and two outgroups, the threespine stickleback and the zebrafish. Relative to these other species, pelagic notothenioids exhibited a delay in pharyngeal bone development, which was associated with discrete heterochronic shifts in skeletal gene expression that were consistent with persistence of the chondrogenic program and a delay in the osteogenic program during larval development. Morphological analysis also revealed a bias toward the development of anterior and ventral elements of the notothenioid pharyngeal skeleton relative to dorsal and posterior elements.ConclusionsOur data support the hypothesis that early shifts in the relative timing of craniofacial skeletal gene expression may have had a significant impact on the adaptive radiation of Antarctic notothenioids into pelagic habitats.
Highlights
Pedomorphism is the retention of ancestrally juvenile traits by adults in a descendant taxon
The predicted amino acid sequence similarities among fishes were similar for all three collagen genes, with highest identities exhibited between the two notothenioids, the osteopenic C. aceratus and the strongly mineralized N. coriiceps (97%, 100%, and 95% for col1a1, col2a1b, and col10a1, respectively), whereas the lowest identities were generally found between fishes and tetrapod outgroups
Notothenioids dominate the near-shore habitat of Antarctica and are an important example of an adaptive radiation in marine fishes [1,5,46]
Summary
Pedomorphism is the retention of ancestrally juvenile traits by adults in a descendant taxon. Notothenioid evolutionary history is characterized by parallel radiations from a benthic ancestor to pelagic predators, which was accompanied by the appearance of several pedomorphic traits, including the reduction of skeletal mineralization that resulted in increased buoyancy. Antarctic notothenioids are endemic to the Southern Ocean and probably evolved in situ from a sluggish, benthic perciform species beginning 40-60 Mya in the temperate waters of the Antarctic continental shelf [1]. The rich, shallow-water, temperate fish fauna characteristic of the late Eocene (38 Mya) became largely extinct due to habitat destruction and changes in trophic structure, freeing ecological niches into which the notothenioids radiated [4]. A significant obstacle facing notothenioids as they radiated into pelagic habitats was the ancestral absence of a swim bladder, the gas-filled chamber that most teleosts use to maintain buoyancy. Natural selection favored compensatory changes in the musculoskeletal system to achieve neutral buoyancy, including the replacement of densely mineralized bone with cartilage and connective tissue, decreased bone mineralization, and the accumulation of lipid deposits in muscle and connective tissues
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