Selection and constraint underlie irreversibility of tooth loss in cypriniform fishes

Abstract

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.Astyanax mexicanus | transgenic

Evolved tooth gain in sticklebacks is associated with acis-regulatory allele ofBmp6

“…The mixed direction of effects of benthic alleles could alternatively result from pleiotropy (35), with QTL controlling other adaptive benthic phenotypes that might secondarily affect tooth patterning. For example, the large-effect toothspacing QTL on chromosome 4 overlaps the Ectodysplasin (Eda) gene which controls adaptive reductions in armor plate patterning (36) and is also well known to affect vertebrate tooth patterning (37,38). Interestingly, Eda also plays a role in the spacing of hair placodes and tooth cusps in mice (39,40), making Eda an excellent candidate for underlying the tooth-spacing QTL on chromosome 4.…”

Early development and replacement of the stickleback dentition

“…For example, both oral and pharyngeal tooth formation require Ectodysplasin signaling (reviewed in Sadier et al, ). Furthermore, ectopic expression of Ectodysplasin is remarkably sufficient to restore dorsal pharyngeal tooth formation in zebrafish (Aigler et al, ). A previous study found evidence for the conservation of a dental gene network between oral and pharyngeal teeth in two species of cichlids, M. zebra and L. fuelleborni (Fraser et al, ).…”

Distinct developmental and genetic mechanisms underlie convergently evolved tooth gain in sticklebacks

“…Modularity of the dentition can be seen across vertebrate lineages, as in Cypriniformes such as zebrafish, which have uncoupled tooth patterning in the dorsal and ventral pharynx, completely losing dorsal pharyngeal teeth while retaining ventral pharyngeal teeth (Stock, 2007). In zebrafish, the addition of a single transgene driving ubiquitous Ectodysplasin is sufficient to drive the formation of ancestrally lost dorsal pharyngeal teeth (Aigler et al, 2014). In mice, strong support for genetic modularity of the dentition has also been found.…”