Biomechanical Specialization Acts as an Asymmetrical Constraint on the Phenotype.

Abstract

Vertebrate jaws involve trade-offs between the transmission of velocity and force, which underlies their feeding performance and potentially their evolution. We investigate the velocity-force trade-off and its implications for adaptation of the anatomically complex fish jaw system among 89 species of percid fishes (Percidae). We test alternative hypotheses about how the trade-off may symmetrically or asymmetrically constrain jaw diversity. We find that the trade-off has a strong impact on the structural diversity of the jaws, indicating that specialization acts as a constraint on the phenotype. Force-modified jaws are compact with short snouts and a small oral cavity, while velocity-modified jaws are more robust with elongate snouts and a large oral cavity. The distribution of craniofacial diversity along the extremes is asymmetrical, as species with velocity-modified jaws are more phenotypically dissimilar than those with force-modified jaws. The rate of phenotypic evolution is also asymmetrical, as lineages with velocity- and force-modified jaws evolve slower and faster than unspecialized jaws, respectively. This discrepancy between phenotypic diversity and rate of evolution is explained by time to evolve, as force-modified jaws arose comparatively nearer the present. We expand recent literature linking trade-offs to asymmetrical macroevolutionary patterns, which may be an underappreciated cause of the uneven distribution of vertebrate diversity.