CAN SELECTION BY AN ECTOPARASITE DRIVE A POPULATION OF RED CROSSBILLS FROM ITS ADAPTIVE PEAK?

The bill structures of different call types of red crossbills (Loxia curvirostra complex) in western North America usually approximate the predicted optima for foraging on single species of conifers. One clear exception is the call type in the South Hills, Idaho, that is coevolving in an evolutionary arms race with Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia). Although South Hills crossbills forage only on the cones of these lodgepole pines, their average bill depth is smaller than that predicted to be optimal. Because preliminary data showed that large-billed males were more likely to exhibit symptoms of ectoparasitic mite (Knemidokoptes jamaicensis) infestation, the goal of our study was to further quantify the incidence of mite infestation and determine whether selection by mites may have favored smaller-billed crossbills and thus driven crossbills away from the foraging optimum. We estimated annual survival of both infected and uninfected South Hills crossbills using program MARK, which allows for auxiliary variables such as bill size and sex to be included in survival analyses. Mite infestation depressed crossbill survival and, especially for males, caused directional selection against larger-billed individuals. Such selection may explain why South Hills crossbills have smaller bills than the optimum and why average bill size for males has decreased from 1998 to 2003. This selection may also explain why the degree of sexual size dimorphism has decreased by nearly 50% since 1998.     

Genome divergence and diversification within a geographic mosaic of coevolution

Despite substantial interest in coevolution's role in diversification, examples of coevolution contributing to speciation have been elusive. Here, we build upon past studies that have shown both coevolution between South Hills crossbills and lodgepole pine (Pinus contorta), and high levels of reproductive isolation between South Hills crossbills and other ecotypes in the North American red crossbill (Loxia curvirostra) complex. We used genotyping by sequencing to generate population genomic data and applied phylogenetic and population genetic analyses to characterize the genetic structure within and among nine of the ecotypes. Although genome‐wide divergence was slight between ecotypes (F_ST = 0.011–0.035), we found evidence of relative genetic differentiation (as measured by F_ST) between and genetic cohesiveness within many of them. As expected for nomadic and opportunistic breeders, we detected no evidence of isolation by distance. The one sedentary ecotype, the South Hills crossbill, was genetically most distinct because of elevated divergence at a small number of loci rather than pronounced overall genome‐wide divergence. These findings suggest that mechanisms related to recent local coevolution between South Hills crossbills and lodgepole pine (e.g. strong resource‐based density dependence limiting gene flow) have been associated with genome divergence in the face of gene flow. Our results further characterize a striking example of coevolution driving speciation within perhaps as little as 6000 years.     

Coevolution,local adaptation and ecological speciation

Coevolution is one of the major processes organizing the earth's biodiversity, but it remains unclear when and how it may generate species diversity. The study by Parchman et al. ( 2016 ) in this issue of Molecular Ecology provides the clearest evidence to date that divergent local adaptation in a coevolving interaction may lead to speciation on one side of an interaction but not necessarily on the other side. Red crossbills in North America have diversified into ecotypes that specialize on different conifer species, use different calls and vary in the extent to which they are nomadic or sedentary. This new study evaluated genomic divergence among nine crossbill ecotypes. The authors found low overall genomic divergence among many of the ecotypes, but the sedentary South Hills crossbills, which are specialized to eat the seeds of a unique population of lodgepole pines, showed substantial divergence from other crossbills at a small number of genomic regions. These results corroborate past studies showing local coadaptation of the morphological traits of South Hills crossbills and lodgepole pines, and premating isolation of the South Hills crossbills from other populations. Together, the past and new results suggest that local coevolution with lodgepole pines has led to reduced gene flow between South Hills crossbills and other crossbills.     

Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine

Few studies have shown both reciprocal selection and reciprocal adaptations for a coevolving system in the wild. The goal of our study was to determine whether the patterns of selection on Rocky Mountain lodgepole pine (Pinus contorta spp. latifolia) and red crossbills (Loxia curvirostra complex) were concordant with earlier published evidence of reciprocal adaptations in lodgepole pine and crossbills on isolated mountain ranges in the absence of red squirrels (Tamiasciurus hudsonicus). We found that selection (directional) by crossbills on lodgepole pine where Tamiasciurus are absent was divergent from the selection (directional) exerted by Tamiasciurus on lodgepole pine. This resulted in divergent selection between areas with and without Tamiasciurus that was congruent with the geographic patterns of cone variation. In the South Hills, Idaho, where Tamiasciurus are absent and red crossbills are thought to be coevolving with lodgepole pine, crossbills experienced stabilizing selection on bill size, with cone structure as the agent of selection. These results show that crossbills and lodgepole pine exhibit reciprocal adaptations in response to reciprocal selection, and they provide insight into the traits mediating and responding to selection in a coevolutionary arms race.     

Replicated population divergence caused by localized coevolution? A test of three hypotheses in the red crossbill‐lodgepole pine system

Several lines of evidence support the hypothesis that local populations of red crossbills (Loxia curvirostra complex) enter into a predator-prey arms race with lodgepole pine (Pinus contorta latifolia) in the absence of competing pine squirrels (Tamiasciurus hudsonicus). Nevertheless, the alternative hypotheses that neutral evolution or factors other than squirrels have caused crossbill population differentiation have not been thoroughly tested. We compared crossbill and pine cone morphology between island populations where squirrels are absent or present, and mainland sites where squirrels are present, in order to distinguish among these hypotheses. All comparisons supported an effect of squirrel absence, not island status, on crossbill and cone morphology. Hence our results provide further evidence that strong localized coevolutionary interactions in a geographic mosaic have driven adaptive population differentiation. In addition, vocal differentiation of crossbills was related to the absence of squirrels, but not to island status. As morphological and vocal differentiation is correlated with reproductive isolation in crossbills, the geographic mosaic of coevolution also seems to promote ecological speciation.     

Assortative flocking in crossbills and implications for ecological speciation

How reproductive isolation is related to divergent natural selection is a central question in speciation. Here, we focus on several ecologically specialized taxa or 'call types' of red crossbills (Loxia curvirostra complex), one of the few groups of birds providing much evidence for ecological speciation. Call types differ in bill sizes and feeding capabilities, and also differ in vocalizations, such that contact calls provide information on crossbill phenotype. We found that two call types of red crossbills were more likely to approach playbacks of their own call type than those of heterotypics, and that their propensity to approach heterotypics decreased with increasing divergence in bill size. Although call similarity also decreased with increasing divergence in bill size, comparisons of responses to familiar versus unfamiliar call types indicate that the decrease in the propensity to approach heterotypics with increasing divergence in bill size was a learned response, and not a by-product of calls diverging pleiotropically as bill size diverged. Because crossbills choose mates while in flocks, assortative flocking could lead indirectly to assortative mating as a by-product. These patterns of association therefore provide a mechanism by which increasing divergent selection can lead to increasing reproductive isolation.     

Diversifying Coevolution between Crossbills and Conifers

Coevolution between granivorous crossbills (Loxia spp.) and conifers has been a prominent process in the diversification of crossbills. A striking example occurs in western North America where coevolution between crossbills and Rocky Mountain lodgepole pine (Pinus contorta latifolia) is ongoing in isolated ranges without the crossbill’s dominant competitor for seeds, the red squirrel (Tamiasciurus hudsonicus). Preferential foraging by crossbills on lodgepole pine cones in the South Hills and Albion Mountains, two small mountain ranges in southern Idaho where red squirrels are absent, has led to the evolution of larger, thicker-scaled cones than in nearby ranges where red squirrels are present. This in turn has favored the evolution of larger-billed crossbills that have diverged from other crossbills in the region. However, such diversifying coevolution, resulting from geographic variation in the distribution of strongly interacting species, is vulnerable to species introductions. For example, the introduction of red squirrels caused the precipitous decline and perhaps extinction of the Newfoundland crossbill and perhaps a crossbill endemic to the Cypress Hills, Canada. In general, species introductions act to reduce the geographic variation in species interactions, which may be critical for the diversification of many taxa.     

Patterns of genetic variation in the adaptive radiation of New World crossbills (Aves: Loxia)

Incipient species groups or young adaptive radiations such as crossbills (Aves: Loxia) present the opportunity to investigate directly the processes occurring during speciation. New World crossbills include white-winged crossbills (Loxia leucoptera), Hispaniolan crossbills (Loxia megaplaga), and red crossbills (Loxia curvirostra complex), the last of which is comprised of at least nine morphologically and vocally differentiated forms ('call types') where divergent natural selection for specialization on different conifer resources has been strongly implicated as driving diversification. Here we use amplified fragment length polymorphism (AFLP) markers to investigate patterns of genetic variation across populations, call types, and species of New World crossbills. Tree-based analyses using 440 AFLP loci reveal strongly supported clustering of the formally recognized species, but did not separate individuals from the eight call types in the red crossbill complex, consistent with recent divergence and ongoing gene flow. Analyses of genetic differentiation based on inferred allele frequency variation however, reveal subtle but significant levels of genetic differentiation among the different call types of the complex and indicate that between call-type differentiation is greater than that found among different geographic locations within call types. Interpreted in light of evidence of divergent natural selection and strong premating reproductive isolation, the observed genetic differentiation suggests restricted gene flow among sympatric call types consistent with the early stages of ecological speciation.     

A role for habitat area in the geographic mosaic of coevolution between red crossbills and lodgepole pine

Understanding how resource abundance limits adaptive evolution and influences species interactions is an important step towards developing insight into the role of microevolutionary processes in establishing macroevolutionary patterns. We examined how variation in resource abundance (forest area of lodgepole pine Pinus contorta ssp. latifolia) influenced patterns of co-adaptation and coevolution between red crossbill (Loxia curvirostra complex) and lodgepole pine populations. First, we found that crossbill abundance increased logarithmically as forest area increased in mountain ranges lacking a preemptive competitor (pine squirrels Tamiasciurus hudsonicus). Second, seed defences against predation by crossbills increased with increases in crossbill density, suggesting that seed defences have likely evolved in proportion to the intensity of selection that crossbills exert. Third, the average bill size of crossbill populations increased with increasing seed defences, which implies that crossbill offenses increased with increases in seed defences. The large bill size on the largest range is the result of coevolution with lodgepole pine with this crossbill population perhaps speciating. Local adaptation of crossbill populations on smaller ranges, however, is more likely the result of resident crossbills representing a subset of the potential colonists (phenotypic sorting) than of local evolution. In the smallest range, migration and possibly more frequent extinction likely impede local adaptation and may result in maladaptation.     

CONSISTENCY AND VARIATION IN PHENOTYPIC SELECTION EXERTED BY A COMMUNITY OF SEED PREDATORS

Phenotypic selection that is sustained over time underlies both anagenesis and cladogenesis, but the conditions that lead to such selection and what causes variation in selection are not well known. We measured the selection exerted by three species of predispersal seed predators of lodgepole pine (Pinus contorta latifolia) in the South Hills, Idaho, and found that net selection on different cone and seed traits exerted by red crossbills (Loxia curvirostra) and cone borer moths (Eucosma recissoriana) over 10 years of seed crops was similar to that measured in another mountain range. We also found that the strength of selection increased as seed predation increased, which provides a mechanism for the correlation between the escalation of seed defenses and the density of seed predators. Red crossbills consume the most seeds and selection they exert accounts for much of the selection experienced by lodgepole pine, providing additional support for a coevolutionary arms race between crossbills and lodgepole pine in the South Hills. The third seed predator, hairy woodpeckers (Picoides villosus), consumed less than one‐sixth as many seeds as crossbills. Across the northern Rocky Mountains, woodpecker abundance and therefore selective impact appears limited by the elevated seed defenses of lodgepole pine.     

Survival and population size of a resident bird species are declining as temperature increases

1. A large number of migratory bird species appear to be declining as the result of climate change, but whether resident bird species have or will be adversely affected by climate change is less clear. We focus on the South Hills crossbill (Loxia curvirostra complex), which is endemic to about 70 km(2) of Rocky Mountain lodgepole pine (Pinus contorta latifolia) forest in southern Idaho, USA. 2. Our results indicate that the South Hills crossbill has declined by over 60% between 2003 and 2008, and that decreasing adult survival drives this population decline. 3. We evaluated the relative support for multiple hypotheses linking crossbill survival to climate, an ectoparasitic mite (scaly-leg mites Knemidokoptes jamaicensis), and the recent emergence of West Nile virus. Changes in adult apparent survival rate were closely associated with average spring and annual temperatures, and with high temperatures (≥32 °C) during summer, which have increased during the last decade. In contrast, there was little evidence that scaly-leg mites or West Nile virus contributed to recent declines in adult survival. 4. The most probable mechanism causing the decline in adult survival and population size is a decrease in the availability of their primary food resource, seeds in serotinous pine cones. Cone production has declined with increasing annual temperatures, and these cones appear to be prematurely opening owing to increasingly hot summer conditions releasing their seeds and reducing the carrying capacity for crossbills later in the year. 5. In light of regional climate change forecasts, which include an increase in both annual temperature and hot days (>32 °C), and the likely disappearance of lodgepole pine from southern Idaho by the end of this century, additional research is needed to determine how to maintain lodgepole pine forests and their supply of seeds to conserve one of the few bird species endemic to the continental United States.     

Divergent selection drives the adaptive radiation of crossbills

Abstract Knowledge of how phenotype influences fitness is necessary if we are to understand the basis of natural selection and how natural selection contributes to adaptive radiations. Here I quantify selection on a wild population of red crossbills ( Loxia curvirostra complex) in the South Hills, Idaho. Bill depth is the target of selection and selection on bill depth is stabilizing. I then show how fitness is related to both bill depth and performance. I use these and previously published relationships to estimate a fitness surface for five species of red crossbills that are part of an ongoing adaptive radiation in western North America. The fitness surface for crossbills has distinct peaks and valleys, with each crossbill species residing on or very near the summits. This work strongly supports a key tenet of the ecological theory of adaptive radiations; namely, divergent selection for utilizing alternative resources is the ultimate cause of adaptive radiations.     

Interactions among moths, crossbills, squirrels, and lodgepole pine in a geographic selection mosaic

Repeated patterns among biological communities suggest similar evolutionary and ecological forces are acting on the communities. Conversely, the lack of such patterns suggests that similar forces are absent or additional ones are present. Coevolution between a seed predator, the red crossbill (Loxia curvirostra complex), and lodgepole pine (Pinus contorta var. latifolia) exemplifies the ecological and evolutionary predictions for coevolving systems. In the absence of another seed predator and preemptive competitor (pine squirrels Tamiasciurus hudsonicus), natural selection by crossbills results in the evolution of larger cones with thicker distal scales, while relaxation of selection by squirrels results in the evolution of cones with more seeds and a greater ratio of seed mass to cone mass. However, in one range, the Little Rocky Mountains, distal scale thickness has diverged as expected but cone size has not. In these mountains seed predation by lodgepole pine cone borer moths (Eucosma recissoriana) was about 10 times greater than in other ranges lacking squirrels. We quantified moth predation and cone traits and found that moths select for smaller cones with fewer seeds. Thus, selection by moths in the Little Rocky Mountains counters both selection by crossbills for large cone size and relaxation of selection by squirrels favoring more seeds per cone and accounts for the relatively small and few-seeded cones in these mountains. It is also apparent that selection by crossbills changes seed defenses in a manner that favors seed predation by moths, whereas selection by squirrels likely reduces such predation. These results demonstrate the importance of considering the evolutionary consequences of community context in locally evolved (coevolved) traits and interactions.     

The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine

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 cold-spots).     

The geographic selection mosaic for squirrels, crossbills and Aleppo pine

The interactions between many species are structured in a geographic mosaic of populations among which selection is divergent. Here we tested the hypothesis that such a geographic selection mosaic arises for common crossbills (Loxia curvirostra) feeding on seeds in the cones of Aleppo pine (Pinus halepensis) because of geographic variation in the occurrence of European red squirrels (Sciurus vulgaris). On the Iberian Peninsula, Sciurus exerted directional selection favouring larger cones with larger scales, which has caused cones there to be larger than in the Balearic Islands where Sciurus are absent. Moreover, cones on the Iberian Peninsula are so large that they are apparently little used by the relatively small-billed crossbills on the Peninsula; selection by Sciurus seems to have made the cones so difficult to feed on that crossbills rely mostly on the seeds of other conifers. Where crossbills are present but Sciurus are absent (Mallorca Island), cones were smaller as a result of relaxation of selection by Sciurus. However, cones on Mallorca had proportionally thicker scales in comparison to where both Sciurus and crossbills are absent (Ibiza Island), presumably as an adaptation against crossbill predation. Here crossbills specialize on Aleppo pine, have relatively large bills and have apparently coevolved in an arms race with Aleppo pine. These results suggest that Sciurus has influenced both the geographic selection mosaics for crossbills and conifers and the adaptive radiation of crossbills in Eurasia much like Tamiasciurus has done in the North America.     

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.     

The geographic selection mosaic for ponderosa pine and crossbills: a tale of two squirrels

Recent research demonstrates how the occurrence of a preemptive competitor (Tamiasciurus) gives rise to a geographic mosaic of coevolution for crossbills (Loxia) and conifers. We extend these studies by examining ponderosa pine (Pinus ponderosa), which produces more variable annual seed crops than the conifers in previous studies and often cooccurs with tree squirrels in the genus Sciurus that are less specialized than Tamiasciurus on conifer seed. We found no evidence of seed defenses evolving in response to selection exerted by S. aberti, which was apparently overwhelmed by selection resulting from inner bark feeding that caused many developing cones to be destroyed. In the absence of S. aberti, defenses directed at crossbills increased, favoring larger-billed crossbills and causing stronger reciprocal selection between crossbills and ponderosa pine. However, crossbill nomadism in response to cone crop fluctuations prevents localized reciprocal adaptation by crossbills. In contrast, evolution in response to S. griseus has incidentally defended cones against crossbills, limiting the geographic range of the interaction between crossbills and ponderosa pine. Our results suggest that annual resource variation does not prevent competitors from shaping selection mosaics, although such fluctuations likely prevent fine-scale geographic differentiation in predators that are nomadic in response to resource variability.     

Temporal variation in breeding and cone size selection by three species of crossbills Loxia spp. in a native Scots pinewood

The breeding biology and cone size selection of crossbills was studied mainly during 1995 to 2002 at Abernethy Forest, Scotland, an ancient native Scots pine Pinus sylvestris wood, where only a single crossbill species, the Scottish crossbill Loxia scotica, was assumed to occur and to be adapted to feed on seeds in Scots pine cones. However, three crossbill species (common Loxia curvirostra, Scottish and parrot crossbills Loxia pytyopsittacus) nested in some years, with the parrot crossbill being the most abundant. Most nests were in old large pines, with the three crossbill species not differing in their use of tree size or stand density for nesting. The mean clutch and brood sizes were 3.8 and 2.9, and their mean survivals were 86 and 74%, respectively, with no significant differences among species. The timing of breeding differed between species, with parrot crossbills breeding earliest (median date 21 March, including second attempts) and common crossbills breeding last (median date 21 April), probably in response to the differing accessibility of Scots pine seeds to these species. The difference in the time of breeding may reduce mixed mating. Crossbills foraged preferentially on trees with small cones when the cones were closed. Small cones had thinner scales than large cones, suggesting that the preference for small cones was related to higher feeding rates on these cones when cones are closed. Such a preference was also found for captive crossbills with the Scottish crossbill showing a more pronounced preference for smaller cones than the larger‐billed parrot crossbill. However, crossbills selected larger cones within trees and trees with larger cones once the cones opened in April. Such a shift occurred presumably because variation in scale thickness has little impact on seed accessibility once cones open, and larger cones have larger and more seeds. The greater ability of parrot crossbills to exploit seeds in closed Scots pine cones allowed parrot crossbills to start breeding earlier and to have young when seeds were most accessible. Only after the cones opened were the smaller‐billed common crossbills able to easily access seeds and to start breeding. The time of breeding of Scottish crossbills was intermediate between common and parrot crossbills, and they probably had an intermediate ability to exploit Scots pine cones. The reason why there were few Scottish crossbills nesting in Abernethy Forest remains a puzzle, considering that native pine wood is assumed to be the ancestral habitat to which the Scottish crossbill is adapted. The breeding season for all crossbills ended in June, when most of the seed from a given cone cohort was shed. This is when starved broods were found, not associated with bad weather.     

Ecological differentiation in relation to bill size amongst sympatric, genetically undifferentiated crossbills Loxia spp.

Recent evidence of genetic homogeneity across morphologically diverse crossbill taxa Loxia spp. suggests that strong directional natural selection sustains morphological differences. If so, we would expect that, in sympatry, persistent crossbill morphs will be associated with the ecological circumstances that select for particular features. Here we report on a field study of niche differentiation in sympatric crossbills, showing correlation between bill size and habitat use, foraging and movements. In Deeside, north-east Scotland, crossbills occupied three ecological niches. Small-billed birds L. curvirostra were itinerant and migratory. They switched between conifer species in relation to the phenology of cone ripeness, feeding on spruce or larch from summer through winter and Scots Pine Pinus sylvestris in spring and early summer. Large-billed birds L. pytyopsittacus were more sedentary, feeding on pine seed year round in semi-natural pine forest. Birds with intermediate bills L. scotica were also sedentary but switched seasonally between conifer species. Deeside crossbills thus occupied three niches in line with the current designation of three species, but in the study years (1990–1997) there was no shortage of conifer seed and no evidence of strong selection for optimal bill size. Bill sizes did not fall precisely into three distinct modes so other factors were involved. These could have included the immigration of two sizes of L. curvirostra , and introgression (and possibly phenotypic plasticity) amongst the more sedentary larger-billed birds. The origin of L. scotica is discussed within the context of novel habitat, introgression, niche shift and competition for pine seed.     

COEVOLUTION BETWEEN HISPANIOLAN CROSSBILLS AND PINE: DOES MORE TIME ALLOW FOR GREATER PHENOTYPIC ESCALATION AT LOWER LATITUDE?

Crossbills (Aves: Loxia) and several conifers have coevolved in predator-prey arms races over the last 10,000 years. However, the extent to which coevolutionary arms races have contributed to the adaptive radiation of crossbills or to any other adaptive radiation is largely unknown. Here we extend our previous studies of geographically structured coevolution by considering a crossbill-conifer interaction that has persisted for a much longer time period and involves a conifer with more variable annual seed production. We examined geographic variation in the cone and seed traits of two sister species of pines, Pinus occidentalis and P. cubensis, on the islands of Hispaniola and Cuba, respectively. We also compared the Hispaniolan crossbill (Loxia megaplaga) to its sister taxa the North American white-winged crossbill (Loxia leucoptera leucoptera). The Hispaniolan crossbill is endemic to Hispaniola whereas Cuba lacks crossbills. In addition and in contrast to previous studies, the variation in selection experienced by these pines due to crossbills is not confounded by the occurrence of selection by tree squirrels (Tamiasciurus and Sciurus). As predicted if P. occidentalis has evolved defenses in response to selection exerted by crossbills, cones of P. occidentalis have scales that are 53% thicker than those of P. cubensis. Cones of P. occidentalis, but not P. cubensis, also have well-developed spines, a known defense against vertebrate seed predators. Consistent with patterns of divergence seen in crossbills coevolving locally with other conifers, the Hispaniolan crossbill has evolved a bill that is 25% deeper than the white-winged crossbill. Together with phylogenetic analyses, our results suggest that predator-prey coevolution between Hispaniolan crossbills and P. occidentalis over approximately 600,000 years has caused substantial morphological evolution in both the crossbill and pine. This also indicates that cone crop fluctuations do not prevent crossbills and conifers from coevolving. Furthermore, because the traits at the phenotypic interface of the interaction apparently remain the same over at least several hundred thousand years, divergence as a result of coevolution is greater at lower latitude where crossbill-conifer interactions have been less interrupted by Pleistocene events.