The Integrated Genomic Architecture and Evolution of Dental Divergence in East African Cichlid Fishes (Haplochromis chilotes x H. nyererei)

Abstract

The independent evolution of the two toothed jaws of cichlid fishes is thought to have promoted their unparalleled ecological divergence and species richness. However, dental divergence in cichlids could exhibit substantial genetic covariance and this could dictate how traits like tooth numbers evolve in different African Lakes and on their two jaws. To test this hypothesis, we used a hybrid mapping cross of two trophically divergent Lake Victoria species (Haplochromis chilotes × Haplochromis nyererei) to examine genomic regions associated with cichlid tooth diversity. Surprisingly, a similar genomic region was found to be associated with oral jaw tooth numbers in cichlids from both Lake Malawi and Lake Victoria. Likewise, this same genomic location was associated with variation in pharyngeal jaw tooth numbers. Similar relationships between tooth numbers on the two jaws in both our Victoria hybrid population and across the phylogenetic diversity of Malawi cichlids additionally suggests that tooth numbers on the two jaws of haplochromine cichlids might generally coevolve owing to shared genetic underpinnings. Integrated, rather than independent, genomic architectures could be key to the incomparable evolutionary divergence and convergence in cichlid tooth numbers.

Keywords: QTL; adaptive radiation; key innovation; natural selection; trophic evolution.

Figure 1

The toothed oral and pharyngeal jaws of cichlids (A). Dorsal view of the pharyngeal tooth plate of an F2 hybrid is displayed (B) and the large numbers of teeth that can be counted on the jaw are readily seen. The oral jaw dentition (C) of an F2 hybrid cichlid in lateral view.

Figure 2

Correlation of tooth numbers in the oral and pharyngeal jaws of 227 F2 hybrids. The number of teeth in the first row on the right hand side of the lower tooth region of the oral jaw and all of the teeth on the dorsal surface of the lower pharyngeal jaw were counted in the F2 individuals. Tooth numbers on the two jaws were significantly correlated (r_q = 0.35, P < 0.0001).

Figure 3

Tooth number QTL in the oral and the pharyngeal jaws. Linkage group numbers are given as the homologized regions of the Tilapia cichlid genome. The level of significance determined from permutations is shown with a dotted line. Both the oral (A) and pharyngeal jaws (B) have a large-effect QTL on chromosome 11. The 1.5 LOD intervals are highlighted with a black line. These QTL are colocalized to the same region in which Bloomquist et al. (2015) found their largest-effect QTL for oral jaw tooth number in Lake Malawi cichlids.

Figure 4

The effect plots of the marker showing the highest LOD score on chromosome 11 for oral jaw tooth number. The B alleles are from H. nyererei. The effects in the cross of alleles at this locus are in the same direction for both the oral (A) and pharyngeal jaw (B) tooth numbers.