Diversifying coevolution between crossbills and black spruce on Newfoundland.

Coevolution is increasingly recognized as an important process structuring geographic variation in the form of selection for many populations. Here we consider the importance of a geographic mosaic of coevolution to patterns of crossbill (Loxia) diversity in the northern boreal forests of North America. We examine the relationships between geographic variation in cone morphology, bill morphology, and feeding performance to test the hypothesis that, in the absence of red squirrels (Tamiasciurus hudsonicus), black spruce (Picea mariana) has lost seed defenses directed at Tamiasciurus and that red crossbills (L curvirostra) and black spruce have coevolved in an evolutionary arms race. Comparisons of cone morphology and several indirect lines of evidence suggest that black spruce has evolved defenses in response to Tamiasciurus on mainland North America but has lost these defenses on Newfoundland. Cone traits that deter crossbills, including thicker scales that require larger forces to separate, are elevated in black spruce on Newfoundland, and larger billed crossbills have higher feeding performances than smaller billed crossbills on black spruce cones from Newfoundland. These results imply that the large bill of the Newfoundland crossbill (L. c. percna) evolved as an adaptation to the elevated cone defenses on Newfoundland and that crossbills and black spruce coevolved in an evolutionary arms race on Newfoundland during the last 9000 years since glaciers retreated. On the mainland where black spruce is not as well defended against crossbills, the small-billed white-winged crossbill (L leucoptera leucoptera) is more efficient and specializes on seeds in the partially closed cones. Finally, reciprocal adaptations between crossbills and conifers are replicated in black spruce and Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia), with coevolution most pronounced in isolated populations where Tamiasciurus are absent as a competitor. This study further supports the role of Tamiasciurus in determining the selection mosaic for crossbills and suggests that a geographic mosaic of coevolution has been a prominent factor underlying the diversification of North American crossbills.