The Influence of a Competitor on the Geographic Mosaic of Coevolution Between Crossbills and Lodgepole Pine

Abstract

Abstract. The geographic mosaic theory of coevolution posits that the form of selection between interacting species varies across a landscape with coevolution important and active in some locations (i.e., coevolutionary hotspots) but not in others (i.e., coevolutionary coldspots). We tested the hypothesis that the presence of red squirrels (Tamiasciurus hudsonicus) affects the occurrence of coevolution between red crossbills (Loxia curvirostra complex) and Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia) and thereby provides a mechanism giving rise to a geographic mosaic of selection. Red squirrels are the predominant predispersal seed predator and selective agent on lodgepole pine cones. However, in four isolated mountain ranges east and west of the Rocky Mountains, red squirrels are absent and red crossbills are the main predispersal seed predator. These isolated populations of pine have apparently evolved without Tamiasciurus for about 10,000 to 12,000 years. Based on published morphological, genetic, and paleobotanical studies, we infer that cone traits in these isolated populations that show parallel differences from cones in the Rocky Mountains have changed in parallel. We used data on crossbill and conifer cone morphology and feeding preferences and efficiency to detect whether red crossbills and lodgepole pine exhibit reciprocal adaptations, which would imply coevolution. Cone traits that act to deter Tamiasciurus and result in high ratios of cone mass to seed mass were less developed in the isolated populations. Cone traits that act to deter crossbills include larger and thicker scales and perhaps increased overlap between successive scales and were enhanced in the isolated populations. In the larger, isolated mountain ranges crossbills have evolved deeper, shorter, and therefore more decurved bills to exploit these cones. This provides crossbills with higher feeding rates, and the change in bill shape has improved efficiency by reducing the concomitant increases in body mass and daily energy expenditures that would have resulted if only bill size had increased. These parallel adaptations and counter adaptations in red crossbills and lodgepole pine are interpreted as reciprocal adaptations and imply that these crossbills and pine are in coevolutionary arms races where red squirrels are absent (i.e., coevolutionary hotspots) but not where red squirrels are present (i.e., coevolutionary coldspots). The view that coevolution is a prominent evolutionary process has been contentious. Nonetheless, evidence from diverse areas of evolutionary biology indicate that coevolution is a fundamental process in evolution and that a better understanding of the coevolutionary process is critical for progress in evolutionary biology, conservation, and health-related issues (Thompson 1994(Thompson , 1999a. One recent advance in coevolutionary theory has risen from the recognition that the form of an interaction between species often varies across a landscape (e.g., Thompson and Pellmyr 1992). This geographic v...

Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play

“…However, this pattern is disrupted by the presence of another seed predator, the red squirrel. Where present, red squirrels, not crossbills, serve as the primary agent of selection on lodgepole pine cones (Benkman 1999;Benkman et al 2001Benkman et al , 2003. Thus, the presence of red squirrels can decouple the coevolutionary feedback between crossbills and pines.…”

Complex selection on life-history traits and the maintenance of variation in exaggerated rostrum length in acorn weevils

“…Ecological interactions play an important role in generating and maintaining the biological diversity of living organisms, as they influence adaptive morphological traits and thus species diversification Farrell and Mitter 1998;Benkman et al 2001). Where species interactions are mediated by overlapping feeding interactions, morphological divergence in foragingrelated traits permits the coexistence of species with different modes of resource utilization (Ruber et al 1999;Schluter 2000).…”

A seed predator drives the evolution of a seed dispersal mutualism

“…However, the large expanses of mostly treeless basins between the mountain ranges in the Great Basin would have prevented pine squirrels from colonizing in the past 10 000 years (Arbogast et al 2001). Given the 'successful' introductions of pine squirrels to other isolated areas (see Benkman et al 2001), we suspect that the absence of pine squirrels from the more forested mountain ranges is the result of biogeographic barriers rather than habitat unsuitability.…”