Macroevolutionary Divergence along Allometric Lines of Least Resistance in Frog Hindlimb Traits and Its Effect on Locomotor Evolution.

AbstractUnderstanding whether and why microevolutionary patterns of trait covariation match macroevolutionary divergence is essential for linking evolution at different timescales. However, recent work has focused on developmental constraints for alignment between intraspecific variation and divergence, neglecting a potential role of natural selection on function to connect these scales. Here, we compare the support for the selection and constraint hypotheses to explain both phenotypic trait covariation and species divergence. To test these hypotheses, we collected data on hindlimb and jumping performance traits within and across species of two frog genera. We compared patterns of within-species phenotypic variation (the matrix) with divergence and selective covariance matrices, from which we could extract the major axes of the realized adaptive landscape (AL), the directions in which adaptive peaks shifted the most over evolutionary time. We also tested whether the major axes of the AL were related to selection on jumping performance. We found high alignment between patterns of variation across scales. Most divergence occurred in allometric size, defined as the first eigenvector of the matrix. However, jumping performance gradients were unaligned with the major axes of the AL and the matrix. Across species, however, evolution of maximum acceleration showed a strong negative relationship with changes in allometric size. We infer that the jumping peak evolved under fluctuating selection, and species have tracked the peak along the direction of most within-species variation, allometric size. We conclude that long-term hindlimb divergence was constrained by developmental interactions among traits associated with growth and not net directional selection. Nonetheless, divergence on size indirectly influenced jumping evolution.