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Synopsis Mechanical tradeoffs in performance are predicted to sculpt macroevolutionary patterns of morphological diversity across environmental gradients. Water depth shapes the amount of wave energy organisms’ experience, which should result in evolutionary tradeoffs between speed and maneuverability in fish swimming morphology. Here, we tested whether morphological evolution would reflect functional tradeoffs in swimming performance in 131 species of wrasses and parrotfish (Family: Labridae) across a water depth gradient. We found that maximum water depth predicts variation in pectoral fin aspect ratio (AR) in wrasses, but not in parrotfish. Shallow-water wrasses exhibit wing-like pectoral fins that help with “flapping,” which allows more efficient swimming at faster speeds. Deeper water species, in contrast, exhibit more paddle-like pectoral fins associated with enhanced maneuverability at slower speeds. Functional morphology responds to a number of different, potentially contrasting selective pressures. Furthermore, many-to-one mapping may release some traits from selection on performance at the expense of others. As such, deciphering the signatures of mechanical tradeoffs on phenotypic evolution will require integrating multiple aspects of ecological and morphological variation. As the field of evolutionary biomechanics moves into the era of big data, we will be uniquely poised to disentangle the intrinsic and extrinsic predictors of functional diversity.

Weak Relationships Between Swimming Morphology and Water Depth in Wrasses and Parrotfish Belie Multiple Selective Demands on Form–Function Evolution