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Open Access Research article

Molecular pedomorphism underlies craniofacial skeletal evolution in Antarctic notothenioid fishes

R Craig Albertson1*, Yi-Lin Yan2, Tom A Titus2, Eva Pisano3, Marino Vacchi4, Pamela C Yelick5, H William Detrich6 and John H Postlethwait2

Author Affiliations

1 Department of Biology, Syracuse University, 130 College Place, Syracuse, NY, 13244, USA

2 Institute of Neuroscience, 1254 University of Oregon, Eugene, OR, 97403-1254, USA

3 Dipartimento di Biologia, Università di Genova, Viale Benedetto XV, 5, 16132 Genova, Italy

4 ICRAM, c/o Museo Nazionale dell'Antartide (MNA), Università di Genova, Viale Benedetto XV, 5, 16132 Genova, Italy

5 Department of Oral and Maxillofacial Pathology, Tufts University, 136 Harrison Avenue, Boston, MA, 02111, USA

6 Department of Biology, 134 Mugar Hall, Northeastern University, Boston, MA, 02115, USA

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BMC Evolutionary Biology 2010, 10:4  doi:10.1186/1471-2148-10-4

Published: 6 January 2010

Abstract

Background

Pedomorphism 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.

Results

We 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.

Conclusions

Our 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.