Development of beak polymorphism in the African seedcracker, Pyrenestes ostrinus

The black-bellied African seedcracker, Pyrenestes ostrinus, exhibits a non-sex-related polymorphism in beak size that enables the small-, large-, and mega-billed morphs to utilize different trophic niches. The bill polymorphism between small- and large-billed individuals was previously shown to be under genetic control of a single autosomal locus with the allele for a large bill being dominant. African seedcrackers offer a novel opportunity to study the genetic basis of an adaptive polymorphism driven by disruptive selection and differential niche use in wild populations. In this study, we further explore the morphology and molecular development of the beak skeleton and of the cranial musculature in all morphs, both in adults and juveniles (nestlings). We find a close correlation in growth between the two tissues, even though juvenile birds (nestlings) of all morphs are fed a soft mostly insect diet by their parents until they fledge and become independent. Molecular and histological analyses suggest a heterochronic co-option of the mechanotransduction pathway into beak development program to produce the resource polymorphism. We also find that this plasticity is diminished after the nestling period. We suggest that a mutation affecting cranial muscle mass led to a corresponding change in jawbone morphology, allowing for apparent rapid evolution of novel functional adaptations of multiple tissues, a mechanism previously thought to be hard to achieve.