The beak of the other finch: coevolution of genetic covariance structure and developmental modularity during adaptive evolution

摘要

The link between adaptation and evolutionary change remains the most central and least under-stood evolutionary problem. Rapid evolution and diversification of avian beaks is a textbookexample of such a link, yet the mechanisms that enable beak's precise adaptation and extensiveadaptability are poorly understood. Often observed rapid evolutionary change in beaks is particu-larly puzzling in light of the neo-Darwinian model that necessitates coordinated changes indevelopmentally distinct precursors and correspondence between functional and genetic modular-ity, which should preclude evolutionary diversification. I show that during first 19 generations aftercolonization of a novel environment, house finches (Carpodacus mexicanus) express an array of dis-tinct, but adaptively equivalent beak morphologies—a result of compensatory developmentalinteractions between beak length and width in accommodating microevolutionary change in beakdepth. Directional selection was largely confined to the elimination of extremes formed by thesedevelopmental interactions, while long-term stabilizing selection along a single axis—beakdepth—was mirrored in the structure of beak's additive genetic covariance. These results emphasizethree principal points. First, additive genetic covariance structure may represent a historical recordof the most recurrent developmental and functional interactions. Second, adaptive equivalence ofbeak configurations shields genetic and developmental variation in individual components fromdepletion by natural selection. Third, compensatory developmental interactions among beak com-ponents can generate rapid reorganization of beak morphology under novel conditions and thusgreatly facilitate both the evolution of precise adaptation and extensive diversification, therebylinking adaptation and adaptability in this classic example of Darwinian evolution.