Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes

Abstract

East African cichlid fishes represent one of the most striking examples of rapid and convergent evolutionary radiation among vertebrates. Models of ecological speciation would suggest that functional divergence in feeding morphology has contributed to the origin and maintenance of cichlid species diversity. However, definitive evidence for the action of natural selection has been missing. Here we use quantitative genetics to identify regions of the cichlid genome responsible for functionally important shape differences in the oral jaw apparatus. The consistent direction of effects for individual quantitative trait loci suggest that cichlid jaws and teeth evolved in response to strong, divergent selection. Moreover, several chromosomal regions contain a disproportionate number of quantitative trait loci, indicating a prominent role for pleiotropy or genetic linkage in the divergence of this character complex. Of particular interest are genomic intervals with concerted effects on both the length and height of the lower jaw. Coordinated changes in this area of the oral jaw apparatus are predicted to have direct consequences for the speed and strength of jaw movement. Taken together, our results imply that the rapid and replicative nature of cichlid trophic evolution is the result of directional selection on chromosomal packages that encode functionally linked aspects of the craniofacial skeleton.

Figure 1

Morphological differences between LF and MZ. (a) LF is optimally designed for a biting mode of feeding with a short, robust, U-shaped oral jaw apparatus, an inferior subterminal mouth, and an outer row of closely spaced tricuspid teeth on both the upper and lower jaws. (b) In contrast, MZ is designed for a suction mode of feeding with a long, narrower lower jaw, a terminally oriented mouth, and an outer row of widely spaced bicuspid teeth on both jaws. LJ, lower jaw; MX, maxilla; NCM, neurocranium; PMX, premaxilla; SUS, suspensory apparatus.

Figure 2

QTL position on the genetic linkage map. Marker names are to the right of linkage groups, map positions (in centimorgans) are to the left. The map locations of QTL affecting feeding morphology are identified by illustrations of the corresponding structure. Individual bony elements indicate QTL affecting geometric variables. Red bars indicate QTL affecting linear measures. Where geometric and linear variables map to the same interval, red bars overlay stippled illustrations. When only linear measurements map to an interval, bars are shown with line drawings. Black bars indicate the regions exceeding the 95% genome-wide significance threshold for the corresponding QTL.

Figure 2

QTL position on the genetic linkage map. Marker names are to the right of linkage groups, map positions (in centimorgans) are to the left. The map locations of QTL affecting feeding morphology are identified by illustrations of the corresponding structure. Individual bony elements indicate QTL affecting geometric variables. Red bars indicate QTL affecting linear measures. Where geometric and linear variables map to the same interval, red bars overlay stippled illustrations. When only linear measurements map to an interval, bars are shown with line drawings. Black bars indicate the regions exceeding the 95% genome-wide significance threshold for the corresponding QTL.

Figure 3

The intersection of genetic architecture and functional biology in the lower jaw. (a) Jaw length (LJ) is negatively correlated with articular arm height (AAH) in the F₂. As the length of the jaw increases, the height of the articular arm decreases, and vice versa. The major muscle involved in jaw closing, the adductor mandibulae (AM2), inserts onto the articular arm. Thus, in the lexicon of functional morphology, the articular arm is the closing in-lever, and the length of the lower jaw is the closing out-lever. Altering the in- and out-lever ratio will affect the mechanical advantage of the lower jaw for the alternate food-gathering strategies of biting or sucking. QTL for the articular arm (b) and jaw length (c) map to the same interval on LG2. This interval also contains bmp4, a gene known to be involved in embryonic cartilage formation.