Complex adaptive landscape for a "Simple" structure: The role of trade-offs in the evolutionary dynamics of mandibular shape in ground squirrels.

Abstract

Trade‐offs are inherent features of many biomechanical systems and are often seen as evolutionary constraints. Structural decoupling may provide a way to escape those limits in some systems but not for structures that transmit large forces, such as mammalian mandibles. For such structures to evolve in multiple directions on a complex adaptive landscape, different regions must change shape while maintaining structural integrity. We evaluated the complexity of the adaptive landscape for mandibular shape in Marmotini, a lineage of ground squirrels that varies in the proportions of seeds and foliage in their diets, by comparing the fit of models based on traits that predict changes in mandibular loading. The adaptive landscape was more complex than predicted by a two‐peak model with a single dietary shift. The large number of adaptive peaks reflects a high diversity of directions of shape evolution. The number of adaptive peaks also reflects a multiplicity of functional trade‐offs posed by the conflicting demands of processing foods with various combinations of material properties. The ability to balance trade‐offs for diets with different proportions of the same foods may account for diversification and disparity of lineages in heterogeneous environments. Rather than constraints, trade‐offs may be the impetus of evolutionary change.