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.     

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.     

Assortative mating and patterns of inheritance indicate that the three crossbill taxa in Scotland are species

There are three breeding taxa of crossbills in highland Scotland, the common crossbill Loxia curvirostra , parrot crossbill L. pytyopsittacus and endemic Scottish crossbill L. scotica . These taxa show no genetic differentiation in neutral DNA (microsatellites and mitochondrial DNA), but do show some differentiation in morphology and have distinct calls. Mating patterns and bill size inheritance were examined to test four different hypotheses for their genetic similarity: (1) the three taxa belong to the same species and differences in bill sizes are caused by phenotypic plasticity, (2) the taxa are a result of genetic polymorphism at a single locus, (3) the taxa largely act as species but occasionally cross-breed, such that gene flow results in genetic homogenisation of part of the genome, and (4) the taxa are fully reproductively isolated species but diverged only recently, such that insufficient time has passed for neutral DNA to differentiate by genetic drift. Hypotheses 1 and 2 could be excluded because wild crossbills mated assortatively with respect to bill depth (a measure of bill size) and bill depth was highly heritable; narrow-sense heritabilities of 0.58 for female and 0.71 for male Scottish crossbills. Only two of 46 pairs (4.3%) were not assortative by bill size. Pairing was strongly assortative by flight calls (50 out of 52 pairs, 96.2%) and excitement calls (88 out of 93 pairs, 94.6%). Therefore, the three crossbill taxa do not cross-mate freely, nor do they seem totally reproductively isolated (excluding hypothesis 4). Thus, the results mostly favour hypothesis 3. The small amount of gene flow among crossbill taxa may contribute to the lack of genetic differentiation in neutral DNA. However, this appears to be insufficient not to classify them as species, as long as the calls can be regarded as diagnostic.     

Is the nominate subspecies of the common crossbill Loxia c. curvirostra polytypic? II. Differentiation among vocal types in functional traits

Vocally differentiated common crossbill Loxia curvirostra populations ('vocal types') in North America show a high degree of morphological and ecological specialization coupled with significant genetic differentiation and appreciable levels of assortative mating in sympatry. Similar vocally differentiated common crossbill vocal types have recently also been uncovered in Europe. These vocal types frequently overlap in space and time, and preliminary data indicate strong assortatively mating in sympatry. These observations suggest that the European nominate subspecies also consists of several independent evolutionary lineages, but so far morphological and ecological support for this view has been lacking. Bill morphology of crossbills is tightly linked to resource use, and we earlier showed that average morphology (of birds of unknown vocal type) indeed differed among years, consistent with the possibility that vocal types are morphologically differentiated if the proportion of each type caught varies among years. Here we test specifically for morphological differences between birds assigned to vocal type, at two sites and during two independent influxes. Differentiation between the two vocal types studied is highly significant, with the same pattern uncovered at each site and for each influx. Of eight traits investigated, in both univariate and multivariate analyses, the trait that differs most between the two types is the ecologically important bill depth. The difference in average bill depth between these two European vocal types (0.26 mm) is equivalent to the difference between some ecologically specialised North American vocal types. These results provide further evidence that the nominate subspecies of the common crossbill consists of several ecologically distinct populations, if not cryptic species.     

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.     

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.     

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.     

AUTOMATIC FEATURE EXTRACTION AND CLASSIFICATION OF CROSSBILL (LOXIA SPP.) FLIGHT CALLS

ABSTRACT

In this paper a new method for the automatic classification of bird sounds is presented. Our method is based on acoustic parameters (features) taken from the first harmonic component computed from the sound spectrogram. The features are based on a line segment approximation of the first harmonic component. The final feature vectors, consisting of 16 real numbers, are then classified using a self-organizing map (SOM) neural network. Flight calls of four crossbill species (Loxia spp.) are used as a test example. In the first phase, an unsupervised network was trained and tested using common crossbill L. curvirostra flight calls recorded mainly in the Netherlands. The network was tested using two-barred L. leucoptera, Scottish L. scotica and parrot L. pytyopsittacus crossbill flight calls in the second phase. Finally, the results were validated applying the same network to flight calls of common crossbills and parrot crossbills recorded in Finland. The method automatically separated common crossbill flight calls from those of parrot crossbills. The classification accuracy of the Dutch recordings was 58% in the first phase and 54% in the second phase. The Finnish recordings were classified with 54% accuracy.     

On the relative importance of ecology and geographic isolation as drivers for differentiation of call types of red crossbill Loxia curvirostra in the Palearctic

Efforts to understand the process of speciation have been central to the research of biologists since the origin of evolutionary biology as a discipline. While it is well established that geographic isolation has played a key role in many speciation events, particularly in birds, there is ongoing debate about how frequent speciation is in the partial or complete absence of geographical isolation. In the red crossbill Loxia curvirostra, good arguments do exist for sympatric speciation processes. In this species, several classes of calls are clustered in distinct groups, so-called ‘call types', which mate assortatively. Often, several call types can be found at a single site, breeding and feeding next to each other. It has been hypothesized that red crossbill call types evolved by specialising in extracting seeds from cones of different conifer species. Alternatively, call types might have evolved in temporal geographic isolation. Within Europe, little is known about the distribution of the various call types and preferences for distinct food resources. In this study, we analysed the temporal and spatial occurrence of red crossbill call types in the Palearctic, investigated potential reasons for call-type composition at a site, and compared the occurrence of call types with the fructification of conifers. Call-type composition changed with site and season but hardly with conifer species. With our data, we could localise range areas of twelve different call types, which cannot be explained by conifer species occurrence. Therefore, we suggest that call types evolved in parapatry in most of the northern Palearctic region, and, although contradictory results exist from Iberia, we argue that differentiation might be driven by the same drivers there as well. Additionally, we discuss the potential influence of anthropogenic changes of forest composition and distribution on call types, which offers a unique possibility for future studies.     

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.     

A coevolutionary arms race causes ecological speciation in crossbills

We examined three ecological factors potentially causing premating reproductive isolation to determine whether divergent selection as a result of coevolution between South Hills crossbills (Loxia curvirostra complex) and Rocky Mountain lodgepole pine (Pinus contorta latifolia) promotes ecological speciation. One factor was habitat isolation arising because of enhanced seed defenses of lodgepole pine in the South Hills. This caused the crossbill call types (morphologically and vocally differentiated forms) adapted to alternative resources to be rare. Another occurred when crossbills of other call types moved into the South Hills late in the breeding season and feeding conditions were deteriorating so that relatively few non-South Hills crossbills bred ("immigrant infecundity"). Finally, among those crossbills that bred, pairing was strongly assortative by call type (behavioral isolation). Total reproductive isolation between South Hills crossbills and the two other crossbills most common in the South Hills (call types 2 and 5) summed to .9975 and .9998, respectively, on a scale of 0 (no reproductive isolation) to 1 (complete reproductive isolation). These extremely high levels of reproductive isolation indicate that the divergent selection resulting from the coevolutionary arms race between crossbills and lodgepole pine is causing the South Hills crossbill to speciate.     

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.     

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.     

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.     

Microsatellite and mitochondrial DNA homogeneity among phenotypically diverse crossbill taxa in the UK.

Genetic differentiation within and between the three morphologically divergent crossbill species extant in the UK was assessed by comparison of allele frequencies at five unlinked microsatellite loci and DNA sequence variation across the mitochondrial control region. No significant differences in microsatellite allele frequency were found either between different populations of the same species or between the crossbill species themselves. A similar lack of genetic divergence was apparent from the mitochondrial sequence data. We resolved 33 different haplotypes, separated by low levels of sequence divergence (0-0.15%). Levels of divergence within and between species were not significantly different. Haplotypes formed a polyphyletic phylogeny, indicating that the crossbill species do not form genetically separate clades. Discordance between neutral DNA polymorphisms and adaptive morphological variation is discussed in relation to defining the systematic relationship between crossbill forms. If adaptive differences have arisen without a concomitant divergence in neutral DNA then attempting to define crossbill types from microsatellite and mitochondrial DNA without recourse to ecology and behaviour may be misleading.     

Are the ratios of bill crossing morphs in crossbills the result of frequency-dependent selection?

Summary The direction the lower mandible curves in crossbills (Loxia) is an example of a discrete polymorphism. The lower mandible crosses with equal frequency to the left and to the right in several crossbill populations. I hypothesize that the 1:1 ratio results from negative frequency-dependent selection favouring the rarer morph. A crossbill always orients toward closed conifer cones so that its lower mandible is directed towards the cone axis. Thus, only part of the cone can be reached easily when crossbills have few perch sites and the cone cannot be removed from the branch or otherwise turned round. Since crossbills may visit cones which have previously been foraged on by other individuals, an equal frequency of left-to-right mandible crossings may minimize overlap in the use of cones and enhance foraging efficiency. Experimental data support this hypothesis. Moreover, the variation in the ratio of mandible crossing directions among crossbill populations is consistent with this hypothesis.     

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.     

Mate choice based on a key ecological performance trait

Mate preference for well‐adapted individuals may strengthen divergent selection and thereby facilitate adaptive divergence. We performed mate choice experiments in which we manipulated male red crossbill (Loxia curvirostra complex) feeding rates. Using association time as a proxy for preference, we found that females preferred faster foragers, which reinforces natural selection because poorly adapted males would be less likely to obtain a mate as well as less likely to survive. Although theoretical models predict direct preference for adaptation and performance, to the best of our knowledge this experiment provides the first evidence of individuals directly assessing feeding performance in mate choice. In species where assessing the ecological adaptation of potential mates is possible, females may gain fitness benefits from choosing a well‐adapted mate directly or indirectly, promoting the use of information about ecological adaptation in mate choice.