Selection and constraint underlie irreversibility of tooth loss in cypriniform fishes

Aigler, S.R., Jandzik, D., Hatta, K., Uesugi, K., Stock, D.W.
Proceedings of the National Academy of Sciences of the United States of America   111(21): 7707-12 (Journal)
Registered Authors
Hatta, Kohei, Stock, David W.
Astyanax mexicanus, transgenic
MeSH Terms
  • Animals
  • Animals, Genetically Modified
  • Anthraquinones
  • Base Sequence
  • Biological Evolution*
  • Characidae/anatomy & histology
  • Characidae/genetics
  • Cloning, Molecular
  • Cypriniformes/anatomy & histology*
  • Cypriniformes/genetics
  • DNA Primers/genetics
  • Ectodysplasins/metabolism*
  • Gene Expression Regulation/genetics*
  • Genetics, Population/methods
  • Genotype
  • In Situ Hybridization
  • Microscopy, Fluorescence
  • Molecular Sequence Data
  • Reverse Transcriptase Polymerase Chain Reaction
  • Selection, Genetic*
  • Sequence Analysis, DNA
  • Tolonium Chloride
  • Tooth/anatomy & histology*
  • Zebrafish
24821783 Full text @ Proc. Natl. Acad. Sci. USA
The apparent irreversibility of the loss of complex traits in evolution (Dollo's Law) has been explained either by constraints on generating the lost traits or the complexity of selection required for their return. Distinguishing between these explanations is challenging, however, and little is known about the specific nature of potential constraints. We investigated the mechanisms underlying the irreversibility of trait loss using reduction of dentition in cypriniform fishes, a lineage that includes the zebrafish (Danio rerio) as a model. Teeth were lost from the mouth and upper pharynx in this group at least 50 million y ago and retained only in the lower pharynx. We identified regional loss of expression of the Ectodysplasin (Eda) signaling ligand as a likely cause of dentition reduction. In addition, we found that overexpression of this gene in the zebrafish is sufficient to restore teeth to the upper pharynx but not to the mouth. Because both regions are competent to respond to Eda signaling with transcriptional output, the likely constraint on the reappearance of oral teeth is the alteration of multiple genetic pathways required for tooth development. The upper pharyngeal teeth are fully formed, but do not exhibit the ancestral relationship to other pharyngeal structures, suggesting that they would not be favored by selection. Our results illustrate an underlying commonality between constraint and selection as explanations for the irreversibility of trait loss; multiple genetic changes would be required to restore teeth themselves to the oral region and optimally functioning ones to the upper pharynx.
Genes / Markers
Figure Gallery
Mutation and Transgenics
Human Disease / Model Data
Sequence Targeting Reagents
Engineered Foreign Genes
Errata and Notes