The evolution and genetic basis of a functionally critical skull bone, the parasphenoid, among Lake Malawi cichlids.

Abstract

Adaptive radiation, whereby a clade pairs rapid speciation with rapid phenotypic evolution, can result in an uneven distribution of biodiversity across the Metazoan tree. The cichlid fishes of East Africa have undergone multiple adaptive radiations within the major rift lakes. Cichlid radiations are marked by divergence across distinct habitat gradients producing many morphological and behavioural adaptations. Here, we characterize the shape of the parasphenoid, a bone in the neurocranium that dissipates forces generated during feeding. We examine Tropheops, a group that has transitioned between deep and shallow habitats multiple times, to examine habitat-specific differences in parasphenoid shape. We find differences in the depth and length of the parasphenoid between Tropheops residing in each habitat, variation that may impact the ability of the cranium to resist force. We next use a hybrid cross between two cichlid species that differ in parasphenoid shape, Labeotropheus and Tropheops, to examine the genetic basis of these morphological differences. We perform genetic mapping and identify two genomic regions responsible for variation in parasphenoid shape. These regions are implicated in other functional traits including the oral jaws and neurocranium, indicating that the genetic landscape for adaptive evolution may be limited to a few loci with broad effects. Repurposing the same gene(s) for multiple traits via regulatory evolution may be sufficient for selection to drive transitions between habitats important for incipient stages of adaptive radiations.