Convergent Patterns in the Selection Mosaic for Two North American Bird-dispersed Pines

The strength and outcome of interspecific interactions often vary across the landscape because of differences in community context. We investigated how the presence or absence of pine squirrels (Tamiasciurus spp.) influences the ecology and (co)evolution of seeddispersal mutualisms between Clark’s Nutcrackers (Nucifraga columbiana) and limber (Pinus flexilis) and whitebark (P. albicaulis) pines. Nutcrackers are the primary seed dispersers of these pines. Therefore both nutcrackers and pines potentially benefit from the evolution of a cone structure that enhances seed harvest by nutcrackers. Pine squirrels are the dominant predispersal seed predator of these pines throughout the Sierra Nevada–Cascades and Rocky Mountains and do not disperse seeds, so that pines benefit from deterring seed harvest by pine squirrels. To determine whether pines have evolved in response to selection by nutcrackers and pine squirrels, we conducted studies in ranges with pine squirrels and in ranges in the Great Basin and northern Montana where populations of the pines have apparently evolved without pine squirrels for 10 000 years or more. Cone evolution was convergent between both pines and among phylogeographically independent populations with and without pine squirrels, consistent with variation in selection by nutcrackers and pine squirrels. Where pine squirrels were present, they out-competed nutcrackers for seeds, nutcrackers were less abundant, and selection by pine squirrels constrained the evolution of cone and seed traits that facilitate seed dispersal by nutcrackers. In the absence of pine squirrels, nutcrackers were more than twice as abundant, selection by pine squirrels on cone structure was relaxed, and selection on cone structure by nutcrackers resulted in cones that increased the foraging efficiency of nutcrackers and improved their potential for seed dispersal.