Adaptation to Single Resources and the Evolution of Crossbill (Loxia) Diversity

Abstract

I quantitatively test the hypothesis that four taxa or "types" (species or subspecies) of Red Crossbills (Loxia curvirostra) in the Pacific Northwest have diversified morphologically in bill characters in response to alternative adaptive peaks presented by their food: seeds in conifer cones. Hypothetically, each adaptive peak corresponds to one conifer species whose seeds are (1) produced regularly from year to year, (2) held in cones through late winter when seed is most limiting, and (3) protected from depletion by potential noncrossbill competitors. Four such conifers, termed "key conifers," are present (Tsuga heterophylla, Pseudotsuga menziesii, Pinus ponderosa, and Pinus contorta var. latifolia). I use data on foraging efficiency for 31 captive crossbills of four types to determine the optimal bill size and palate structure for foraging on the key conifers. As predicted, if each type is adapted for foraging on a key conifer, the observed morphology of a given type is often the predicted optimal size morphology of foraging on its respective key conifer. Two of the types have mean bill sizes (bill depth) equalling their predicted optimal size. For one of the remaining types, the observed differs from the optimum by 0.4 mm; I was unable to predict an optimal size for the remaining type. Optimal bill size varies with season. Bill sizes corresponded more closely to the optima for winter (lean period) than for summer. Observed mean width of the palate groove, in which crossbills hold conifer seeds while the seeds are being husked, was consistently close to the estimated optimal groove width. Optimal groove width was correlated (r2 = 1.00, n = 4) with seed size (cube root of mass), suggesting optimal groove width is determined by seed size. Overall, each crossbill type has either the optimal bill size or optimal husking groove width, or both, for foraging on their key conifers. Fitness set analyses indicate that there are substantial trade—offs in foraging efficiency. The best phenotype for foraging on one conifer is often only one—half as efficient on other conifers. All four fitness sets are concave, implying selection against intermediate phenotypes. I conclude, first, that reliability of seeds on key conifers during periods of food scarcity is a critical feature in the ecology and evolution of crossbills. Second, optimization of morphological traits occurs even in populations in highly variable environments. Third, disruptive selection against intermediate phenotypes is likely. This should maintain, if not reinforce, the distinctiveness of types. Fourth, the diversity of cone structure and seed size among key conifers is ultimately responsible for the diversification of crossbills.

Assortative flocking in crossbills and implications for ecological speciation

“…The different call types differ in average bill size (mean bill depths for each call type (mean of the two sexes) are 8.75, 9.34, 9.56 and 9.79 mm for types 4, 5, 2 and 9, respectively [14,29]). Types 2, 4 and 5 are nomadic and overlap broadly in distribution in the Pacific Northwest [20,46,47], whereas type 9 is restricted to two small mountain ranges in southern Idaho, the South Hills and Albion Mountains [29].…”

“…Crossbills use the foraging success of flock mates to more rapidly assess patch quality [28]; such information is termed public information, which is defined as the cues inadvertently produced by others that provide information about the environment [37] and even to choose mates [38]. Because the value of using the foraging success of flock mates depends on the similarity between the feeding capabilities of flock mates [28] and feeding capabilities increasingly differ as bill size diverges [14], assortative flocking by bill size is favoured [28]. Assortative flocking in turn could lead to assortative pairing and reproductive isolation as a by-product because crossbills, such as other cardueline finches, begin to pair while in flocks [12,17,39,40].…”

“…Crossbills have diversified in response to divergent selection favouring specialization on alternative adaptive peaks characterized by different seed resources [14,15], which in the case of crossbills are represented by seeds in the cones of different species of conifers [14 -18]. Because of this specialization on different conifers, habitat isolation is an important reproductive isolating barrier for crossbills [12] as different species of conifers are not completely intermingled.…”

“…Within North America, 10 taxa or call types are recognized [20,29,30]. Although the mean bill characteristics of the different call types reside near or on the adaptive peaks for foraging on alternative conifers [14,15], many individuals can be categorized only by differences in their vocalizations [20,23] because of considerable size overlap between the similarly plumaged call types [20]. The large size overlap between call types is not because different call types are highly variable morphologically, as might arise from hybridization [31,32].…”

“…This could provide a mechanism by which (behavioural) reproductive isolation increases with increasing divergent selection. Here, we use playbacks to test the prediction that discrimination against other call types increases with increasing divergence in bill size (depth), which is a measure of divergent selection [14,15].…”