Modularity of the oral jaws is linked to repeated changes in the craniofacial shape of african cichlids

Abstract

The African cichlids of the East-African rift-lakes provide one of the most dramatic examples of adaptive radiation known. It has long been thought that functional decoupling of the oral and pharyngeal jaws in cichlids has facilitated their explosive evolution. Recent research has also shown that craniofacial evolution from radiations in lakes Victoria, Malawi, and Tanganyika has occurred along a shared primary axis of shape divergence, whereby the preorbital region of the skull changes in a manner that is, relatively independent from other head regions. We predicted that the preorbital region would comprise a variational module and used an extensive dataset from each lake that allowed us to test this prediction using a model selection approach. Our findings supported the presence of a preorbital module across all lakes, within each lake, and for Malawi, within sand and rock-dwelling clades. However, while a preorbital module was consistently present, notable differences were also observed among groups. Of particular interest, a negative association between patterns of variational modularity was observed between the sand and rock-dwelling clades, a patter consistent with character displacement. These findings provide the basis for further experimental research involving the determination of the developmental and genetic bases of these patterns of modularity.

Figure 1

Anatomical landmarks placed on the cichlid head. 1 = Tip of the anterior-most tooth on the premaxilla; 2 = Tip of the anterior-most tooth on the dentary; 3 = Maxillary-palatine joint (upper rotation point of the maxilla); 4 = Maxillary-articular joint (lower point of rotation of the maxilla); 5 = Articular-quadrate joint (lower jaw joint); 6 = Insertion of the interopercular ligament on the articular (point at which mouth opening forces are applied); 7 = Posterio-ventral corner of the preopercular; 8 = Most posteriorventral point of the eye socket; 9 = The most anterioventral point of the eye socket; 10 = Joint between the nasal bone and the neurocranium; 11 = Posterior tip of the ascending process of the premaxilla; 12 = Dorsal-most tip of the supraoccipital crest on the neurocranium; 13 = Most dorsal point on the origin of the A1 division of the adductor mandibulae jaw closing muscle on the preopercular; 14 = Most dorsal point on the origin of the A12 division of the adductor mandibulae jaw closing muscle on the preopercular; 15 = Insertion of the A1 division of the adductor mandibulae on the maxilla; 16 = Insertion of the A2 division of the adductor mandibulae on the articular process.

Figure 2

The best supported hypotheses of modularity for African cichlids as a whole (a) and their respective adaptive radiations within lakes Malawi (b), Tanganyika (c), and Victoria (d). Also shown are the best-supported patterns for rock (e), and sand dwellers (f, g) within Malawi. Two models are shown for rock dwellers, because our statistical analysis was unable to discern whether one hypotheses was significantly better at describing patterns of covariance. Note that despite differences among these hypothesis, each contains a preorbital module based in the oral jaws.