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.     

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.     

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.     

On the advantages of crossed mandibles: an experimental approach

The importance of the crossed mandibles to crossbills for foraging on conifer cones was studied by removing most of the crossed portion of the mandibles of two Red Crossbills L. curvirostra. The foraging rate of these two bill-altered crossbills on the cones of three species of conifers was compared to their rates prior to bill alteration and to two controls. The mandible crossing proved essential for extracting seeds from closed cones. However, as cones open the bill crossing becomes less critical. The mandible crossing appears to be one of several adaptations of crossbills that have extended the period during which conifer seeds can be exploited effectively.     

Matching habitat choice in nomadic crossbills appears most pronounced when food is most limiting

Of the various forms of nonrandom dispersal, matching habitat choice, whereby individuals preferentially reside in habitats where they are best adapted, has relatively little empirical support. Here, I use mark‐recapture data to test for matching habitat choice in two nomadic ecotypes of North American Red Crossbills (Loxia curvirostra complex) that exist in the lodgepole pine (Pinus contorta) forests in the South Hills, Idaho, every summer. Crossbills are adapted for foraging on seeds in conifer cones, and in the South Hills the cones are distinctive, favoring a relatively large bill. During a period when seed was most limiting, only the largest individuals approximating the average size of the locally adapted ecotype remained for a year or more. During a period when seed was less limiting, proportionately more individuals remained and the trend for larger individuals to remain was weaker. Although matching habitat choice is difficult to demonstrate, it likely contributed to the observed patterns. Otherwise, nearly unprecedented intensities of natural selection would be needed. Given the nomadic behavior of most crossbill ecotypes and the heterogeneous nature of conifer seed crops, matching habitat choice should be favored and likely contributes to their adaptation to alternative conifers and rapid diversification.     

Vocal types in crossbill populations (Loxia spp.) of Southwest Europe

The evolution of crossbills is one of the most fascinating topics in evolutionary ecology. Recent studies have shown an astonishing divergence in terms of vocalisation between morphologically quite similar crossbill populations in the Red/Common Crossbill complex (Loxia curvirostra) of North America and Europe. Some evidence even indicates the existence of “cryptic” species with different vocal types and bill sizes, which are adapted to different conifer species. However, there is so far no strong genetic evidence for the existence of separate species, although assortative mating occurs with respect to bill size. To understand the role of vocalisation in the speciation process of crossbill taxa, basic studies that assess the distribution of vocal types of crossbills and the use of different habitats and resources are needed. In our study, we investigated the occurrence of crossbill vocal types in Southwest Europe. In addition to the well-known vocal types described first by Robb (Dutch Birding 22:61–107, 2000) for the Benelux and Great Britain, we discovered at least six more vocal types in the Mediterranean area. Some vocal types were found exclusively in rather small areas, e.g. in the Pyrenees, the Sierra de Cazorla, Sierra de Javalambre and on Corsica, and appeared to be tightly linked to certain habitat types and pine species. Overall, vocal types in the Mediterranean had a more local occurrence than vocal types from northern populations, which were more widely distributed. This might reflect the nomadic behaviour of northern European crossbills, which feed, in contrast to Mediterranean crossbills, mostly on rather unstable food sources, especially spruce seeds. Furthermore, the vocal types of Mediterranean crossbills show at least some similarities to the vocal types of the rather sedentary crossbills of North Europe (L. pytyopsittacus, L. scotica), which are as well adapted to pine seeds. This might reflect a common ancestry of crossbills adapted for pines. We therefore suggest the existence of two main groups of crossbills in Europe: one group that is rather sedentary and feeds mainly on pine seeds (L. pytyopsittacus, L. scotica and the Mediterranean forms), and another group in Central, Northern and Eastern Europe that is highly nomadic and mostly feeds on spruce seeds (L. curvirostra). Further studies are needed to unravel the consistency of vocal types and the genetic relationship between the different forms, and to provide more evidence for the degree of assortative mating of crossbills with distinct vocalisation breeding in sympatry.     

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.     

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.     

The role of marker traits in the assortative mating within red crossbills, Loxia curvirostra complex

We conducted mate choice experiments to determine whether differences in calls or bill morphology might influence assortative mating between call types of red crossbills (Loxia curvirostra complex) that have diverged in bill structure to specialize on different species of conifers. Females preferred males that gave calls that matched their own type, but did not prefer males that more closely approximated the average or optimal bill size of the female's call type. These results were consistent with our breeding simulations, which showed that females gained an indirect fitness benefit by choosing a male of her own call type because this reduced the production of offspring with morphologies that fell between adaptive peaks. However, choice based on bill morphology within a call type provided no further benefit. Calls, which crossbills learn from their parents, likely act as a marker trait indicative of the morphological adaptations of the group, allow for easy assessment of potential mates and facilitate rapid divergence under ecological selection.     

The distribution and habitats of crossbills Loxia spp. in Britain, with special reference to the Scottish Crossbill Loxia scotica

A study was carried out, primarily in northern Scotland, to relate bill and wing measurements to diagnostic calls of crossbill species, and thereby use the calls to describe the distributions and habitats of the different species. Bill depth and wing length measurements from museum specimens and live‐trapped birds were used to describe the size categories. Almost all measurements of crossbills from England were similar to measurements of Common Crossbills from Fennoscandia. Museum specimens showed that crossbills in northern Scotland between 1822 and 1990 were a combination of Common Crossbills, birds which were intermediate between Common and Parrot Crossbills (Scottish Crossbills), and perhaps a few Parrot Crossbills. However, catches of crossbills between 1995 and 2000 showed that Parrot Crossbills (based on bill and wing measurements) were present at some sites in the Highlands. Recordings of flight calls and excitement calls of birds of known bill sizes allowed a classification of crossbills according to call types. Four different flight calls (referred to here as types 1–4) and five excitement calls (types A–E) were recognized. A sample of small‐billed birds, thereby identified as Common Crossbills, indicated that there were three groups of Common Crossbills: those giving type 1 flight calls and type A excitement calls (1A), type 2 flight calls and type B excitement calls (2B), and type 4 flight calls and type E excitement calls (4E). Large‐billed birds identified as Parrot Crossbills gave mainly type 2 flight calls and type D excitement calls. Birds with intermediate bill depths (Scottish Crossbills) gave type 3 flight calls and type C excitement calls. Distributions based on calls showed that 1A Common Crossbills were widespread in Scotland but the other types of Common Crossbill were rare. Parrot Crossbills were found in a few localities in the Highlands, and Scottish Crossbills (defined as those giving type 3 flight calls and type C excitement calls) were restricted to the northern and eastern Highlands. Scottish Crossbills and 1A Common Crossbills had overlapping distributions, and overlapped greatly in the types of forests they used between January and March when the Scots Pine cones were still closed. However, Scottish Crossbills were more frequently associated with stands containing Scots Pine compared with Common Crossbills.     

The genetic structure of crossbills suggests rapid diversification with little niche conservatism

Conservatism of ecological niches can cause geographical ranges or the formation of new species to be constrained, and might be expected in situations where strong trade‐offs result in ecological specialization. Here we address the flexibility of resource use in European crossbills by comparing the ecological and genetic similarities between four Mediterranean and three northern European crossbill populations, all specialized in feeding on a different resource. We used sequence data of one mitochondrial and two nuclear genes from between 211 and 256 individuals. The northern crossbills were genetically too similar to infer which population was more related to the southern ones. Crossbills from the island of Mallorca showed genetic signatures of a stable and isolated population, supporting their past treatment as a locally (co)evolving taxon, and seem to have evolved from an ecologically distinct ancestor. Previous studies in other populations also suggest that genetic similarity does not predict morphological and resource similarity. We estimate that the divergence of all western European crossbills has occurred within the last 11 000 years. Overall, it appears that crossbills can diversify rapidly and with little niche conservatism, but that such potentially reproductively isolated specialists are evolutionarily short‐lived. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 908–922.     

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.     

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).     

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.     

When directional selection reduces geographic variation in traits mediating species interactions

Although we often focus on the causes of geographic variation, understanding processes that act to reduce geographic variation is also important. Here, we consider a process whereby adaptive foraging across the landscape and directional selection exerted by a conifer seed predator, the common crossbill (Loxia curvirostra), potentially act to homogenize geographic variation in the defensive traits of its prey. We measured seed predation and phenotypic selection exerted by crossbills on black pine (Pinus nigra) at two sites in the Pindos Mountains, Greece. Seed predation by crossbills was over an order of magnitude higher at the site where cone scale thickness was significantly thinner, which was also the cone trait that was the target of selection at the high predation site. Additional comparisons of selection differentials demonstrate that crossbills exert selection on black pine that is consistent in form across space and time, and increases in strength with increasing seed predation. If predators distribute themselves in relation to the defensive traits of their prey and the strength of selection predators exert is proportional to the amount of predation, then predators may act to homogenize trait variation among populations of their prey in a process analogous to coevolutionary alternation with escalation.     

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.     

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.     

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.     

Population differentiation and restricted gene flow in Spanish crossbills: not isolation-by-distance but isolation-by-ecology

Divergent selection stemming from environmental variation may induce local adaptation and ecological speciation whereas gene flow might have a homogenizing effect. Gene flow among populations using different environments can be reduced by geographical distance (isolation-by-distance) or by divergent selection stemming from resource use (isolation-by-ecology). We tested for and encountered phenotypic and genetic divergence among Spanish crossbills utilizing different species of co-occurring pine trees as their food resource. Morphological, vocal and mtDNA divergence were not correlated with geographical distance, but they were correlated with differences in resource use. Resource diversity has now been found to repeatedly predict crossbill diversity. However, when resource use is not 100% differentiated, additional characters (morphological, vocal, genetic) must be used to uncover and validate hidden population structure. In general, this confirms that ecology drives adaptive divergence and limits neutral gene flow as the first steps towards ecological speciation, unprevented by a high potential for gene flow.     

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.