Species delineation has a long and contentious history, yet most agree that sympatric populations... more Species delineation has a long and contentious history, yet most agree that sympatric populations exhibiting high levels of reproductive isolation and evolving independently are species. In an opinion piece, Hill and Powers (2021; hereafter H&P) claim that several recognized species of crossbills (Loxia spp.) do not represent species because by no measure are they discrete, the vocalizations used to categorize crossbills are learned, modified and can switch to that of a different species, and reproductive isolation is incomplete and weak. We argue that the behavioral and genetic evidence indicate that Cassia crossbills L. sinesciuris, which we focus on because the data relevant to species status are more diverse and extensive, are genetically discrete; call modification rarely leads to crossbill misclassification and overwhelmingly results in call divergence and enhanced discrimination; and are nearly completely reproductively isolated with little evidence of introgression from sympatric red crossbills. The differences in our conclusions result in part from H&P mischaracterizing and misconstruing the ecology of Cassia crossbills, geographic context of their divergence, and evidence for reproductive isolation. H&P seemingly require that crossbills must adhere to the typical model of bird speciation–protracted divergence in allopatry, followed by a gradual increase in sympatry if reproductive isolation and ecological divergence allow–and require evidence such as initial long periods of allopatry, FST values > 0.2, divergent mtDNA and intrinsic postzygotic isolation. Although such evidence commonly distinguishes bird species, an increasing number of studies show that such criteria are not necessary to indicate sympatric, evolutionarily independent lineages.
Spectrograms of contact calls from three individual crossbills that produced Cassia crossbill con... more Spectrograms of contact calls from three individual crossbills that produced Cassia crossbill contact calls when first recorded but switched to producing ponderosa pine crossbill calls in subsequent years (note that we detected no call switching between Cassia and lodgepole pine crossbills, consistent with their greater divergence in call structure). The sex and identification number of each bird is listed at the top of each spectrogram, with the recording dates below. The key feature distinguishing Cassia crossbill contact calls from ponderosa pine crossbill contact calls is the presence of an initially ascending element to the call, which is initially descending in ponderosa pine crossbill calls, though the calls of these crossbills also differ in a variety of frequency characteristics (e.g., fundamental frequency and frequency modulation).
Simulation showing that the predicted quality of foraging (public) information provided by hetero... more Simulation showing that the predicted quality of foraging (public) information provided by heterospecific flockmates relative to conspecific flockmates decreases with increasing differences in mean bill depth. Each point represents the expected difference in feeding rates between two crossbill ecotypes based on simulations using data on feeding performance in relation to bill depth and bill depth distributions. The curve represents a spline fit to the data. The orange dashed lines represent the expected relative quality of foraging information provided by ponderosa pine crossbills to Cassia crossbills, and the purple dashed lines represent the same for lodgepole pine crossbills based on mean differences in bill depth between lineages.
Cultural evolution may accelerate population divergence and speciation, though most support for t... more Cultural evolution may accelerate population divergence and speciation, though most support for this hypothesis is restricted to scenarios of allopatric speciation driven by random cultural drift. By contrast, the role of cultural evolution in non-allopatric speciation (i.e. speciation with gene flow) has received much less attention. One clade in which cultural evolution may have figured prominently in speciation with gene flow includes the conifer-seed-eating finches in the red crossbill (<i>Loxia curvirostra</i>) complex. Here we focus on Cassia crossbills (<i>L</i>. <i>sinesciuris</i>; an ecotype recently split taxonomically from red crossbills) that learn social contact calls from their parents. Previous work found that individuals modify their calls throughout life such that they become increasingly divergent from a closely related, sympatric red crossbill ecotype. This open-ended modification of calls could lead to character displacement if it causes population-level divergence in call structure that, in turn, reduces (maladaptive) heterospecific flocking. Heterospecific flocking is maladaptive because crossbills use public information from flockmates to assess resource quality, and feeding rates are depressed when flockmates differ in their ability to exploit a shared resource (i.e. when flockmates are heterospecifics). We confirm the predictions of character displacement by documenting substantial population-level divergence in Cassia crossbill call structure over just two decades and by using field experiments to demonstrate that Cassia and red crossbills differentially respond to these evolved differences in call structure, reducing heterospecific flock formation. Moreover, because crossbills choose mates from within flocks, a reduction in heterospecific flocking should increase assortative mating and may have been critical for speciation of Cassia crossbills in the face of ongoing gene flow in as few as 5000 years. Our results provide evidence for a largely neglected yet potentially widespread mechani [...]
Summary The direction the lower mandible curves in crossbills (Loxia) is an example of a discrete... more 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.
Tree squirrels (Tamiasciurus) are important selective agents on conifer reproductive strategies (... more Tree squirrels (Tamiasciurus) are important selective agents on conifer reproductive strategies (Smith 1970, 1975). Although this is well established for wind-dispersed pines, the impact of tree squirrels on bird-dispersed pines has been largely ignored. I assessed the impact of tree squirrels on the allocation of reproductive energy in the bird-dispersed limber pine (Pinus flexilis) by comparing its cone and seed traits from three sites in the Rocky Mountains where tree squirrels (Tamiasciurus) are present to those from three mountain ranges in the Great Basin where tree squirrels are absent. As predicted, differences between the two regions in individual cone and seed traits are consistent with the hypothesis that tree squirrels are important selective agents on these traits. In the absence of tree squirrels, limber pine allocates more than twice as much energy to kernel compared with that invested in putative seed defenses (cone, resin, and seed coat) as does limber pine where tree squirrels are present. Such a large difference is particularly striking, because tree squirrels may have become extinct in the Great Basin in only the last 12,000 yr. Although many factors influence the allocation of energy to cones and seeds, no single factor other than the presence of tree squirrels is compatible with the large and consistent differences between limber pine in the Rocky Mountains and Great Basin. These results show that tree squirrels are an important constraint on the evolution of cone and seed traits that promote the dispersal of seeds by birds.
Abstract The structure of forests is a fundamental attribute that impacts biodiversity and ecosys... more Abstract The structure of forests is a fundamental attribute that impacts biodiversity and ecosystem services and in turn is influenced by natural disturbances and management practices. Here, we examine spatial variation in the interaction between a specialized predispersal seed predator, common crossbills (Loxia curvirostra), and Scots pine (Pinus sylvestris) in relation to forest structure and tree features in a managed Mediterranean forest. Crossbills preferred to forage in pine stands that were more open, which correspond to older stands or regeneration stands with scattered old seed trees. More open older stands with larger trees tend to produce more cones that are attractive to crossbills, although their use was also consistent with crossbills reducing their risk of predation. Within these patches, crossbills selectively foraged on trees having many small, thin-scaled cones, which require less effort and time to extract the seeds. Crossbills were apparently limited to only a very small subset of the closed Scots pine cones because they have relatively small and ineffective bills for foraging on Scots pine. Given that crossbills foraged on only a small subset of the cones within more open stands, a management strategy that would aid common crossbills is to thin middle-aged stands. This would accelerate the development of older stand structure, which would benefit crossbills by increasing the occurrence of suitably open woodlands, benefit other species that rely on older more open stand structure, and potentially decrease the vulnerability of the forest to fire and drought.
Abstract The Cassia crossbill (Loxia sinesciuris) feeds exclusively on seeds held in serotinous c... more Abstract The Cassia crossbill (Loxia sinesciuris) feeds exclusively on seeds held in serotinous cones of lodgepole pine (Pinus contorta latifolia). Its population, confined to 67 km2 of pine in southern Idaho, declined by ~ 80% between 2003 and 2011 apparently because an increase in the occurrence of hot summer days (≥32 °C) caused the serotinous cones to open and shed their seeds. We hypothesized that the propensity for serotinous cones to open varies across the landscape depending on the maximum temperatures cones experienced. We tested a suite of abiotic variables for predicting the occurrence of open serotinous cones among 1547 trees at 170 sites. The best-supported model indicated that trees with open cones were less frequent on northeastern aspects and as slope increased. Fewer open cones were expected on northeast aspects because they receive less direct solar radiation. However, the decrease in trees with open cones as slope increased on southwest aspects was unexpected. Increased convection on slopes could reduce maximum cone temperatures and account for the decrease of open cones on steeper slopes, regardless of aspects. Although cones are less likely to open on steeper slopes, slopes with southerly aspects are likely the least favorable for pine recruitment and survival. The most favorable sites for both lodgepole pine and the persistence of closed cones are slopes on northeast aspects. Such locations are often dominated by subalpine fir (Abies bifolia). Reforestation of fir-dominated areas with lodgepole pine, therefore, provides a means to expand microclimatic refugia for Cassia crossbills.
Species delineation has a long and contentious history, yet most agree that sympatric populations... more Species delineation has a long and contentious history, yet most agree that sympatric populations exhibiting high levels of reproductive isolation and evolving independently are species. In an opinion piece, Hill and Powers (2021; hereafter H&amp;P) claim that several recognized species of crossbills (Loxia spp.) do not represent species because by no measure are they discrete, the vocalizations used to categorize crossbills are learned, modified and can switch to that of a different species, and reproductive isolation is incomplete and weak. We argue that the behavioral and genetic evidence indicate that Cassia crossbills L. sinesciuris, which we focus on because the data relevant to species status are more diverse and extensive, are genetically discrete; call modification rarely leads to crossbill misclassification and overwhelmingly results in call divergence and enhanced discrimination; and are nearly completely reproductively isolated with little evidence of introgression from sympatric red crossbills. The differences in our conclusions result in part from H&amp;P mischaracterizing and misconstruing the ecology of Cassia crossbills, geographic context of their divergence, and evidence for reproductive isolation. H&amp;P seemingly require that crossbills must adhere to the typical model of bird speciation–protracted divergence in allopatry, followed by a gradual increase in sympatry if reproductive isolation and ecological divergence allow–and require evidence such as initial long periods of allopatry, FST values &gt; 0.2, divergent mtDNA and intrinsic postzygotic isolation. Although such evidence commonly distinguishes bird species, an increasing number of studies show that such criteria are not necessary to indicate sympatric, evolutionarily independent lineages.
Spectrograms of contact calls from three individual crossbills that produced Cassia crossbill con... more Spectrograms of contact calls from three individual crossbills that produced Cassia crossbill contact calls when first recorded but switched to producing ponderosa pine crossbill calls in subsequent years (note that we detected no call switching between Cassia and lodgepole pine crossbills, consistent with their greater divergence in call structure). The sex and identification number of each bird is listed at the top of each spectrogram, with the recording dates below. The key feature distinguishing Cassia crossbill contact calls from ponderosa pine crossbill contact calls is the presence of an initially ascending element to the call, which is initially descending in ponderosa pine crossbill calls, though the calls of these crossbills also differ in a variety of frequency characteristics (e.g., fundamental frequency and frequency modulation).
Simulation showing that the predicted quality of foraging (public) information provided by hetero... more Simulation showing that the predicted quality of foraging (public) information provided by heterospecific flockmates relative to conspecific flockmates decreases with increasing differences in mean bill depth. Each point represents the expected difference in feeding rates between two crossbill ecotypes based on simulations using data on feeding performance in relation to bill depth and bill depth distributions. The curve represents a spline fit to the data. The orange dashed lines represent the expected relative quality of foraging information provided by ponderosa pine crossbills to Cassia crossbills, and the purple dashed lines represent the same for lodgepole pine crossbills based on mean differences in bill depth between lineages.
Cultural evolution may accelerate population divergence and speciation, though most support for t... more Cultural evolution may accelerate population divergence and speciation, though most support for this hypothesis is restricted to scenarios of allopatric speciation driven by random cultural drift. By contrast, the role of cultural evolution in non-allopatric speciation (i.e. speciation with gene flow) has received much less attention. One clade in which cultural evolution may have figured prominently in speciation with gene flow includes the conifer-seed-eating finches in the red crossbill (<i>Loxia curvirostra</i>) complex. Here we focus on Cassia crossbills (<i>L</i>. <i>sinesciuris</i>; an ecotype recently split taxonomically from red crossbills) that learn social contact calls from their parents. Previous work found that individuals modify their calls throughout life such that they become increasingly divergent from a closely related, sympatric red crossbill ecotype. This open-ended modification of calls could lead to character displacement if it causes population-level divergence in call structure that, in turn, reduces (maladaptive) heterospecific flocking. Heterospecific flocking is maladaptive because crossbills use public information from flockmates to assess resource quality, and feeding rates are depressed when flockmates differ in their ability to exploit a shared resource (i.e. when flockmates are heterospecifics). We confirm the predictions of character displacement by documenting substantial population-level divergence in Cassia crossbill call structure over just two decades and by using field experiments to demonstrate that Cassia and red crossbills differentially respond to these evolved differences in call structure, reducing heterospecific flock formation. Moreover, because crossbills choose mates from within flocks, a reduction in heterospecific flocking should increase assortative mating and may have been critical for speciation of Cassia crossbills in the face of ongoing gene flow in as few as 5000 years. Our results provide evidence for a largely neglected yet potentially widespread mechani [...]
Summary The direction the lower mandible curves in crossbills (Loxia) is an example of a discrete... more 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.
Tree squirrels (Tamiasciurus) are important selective agents on conifer reproductive strategies (... more Tree squirrels (Tamiasciurus) are important selective agents on conifer reproductive strategies (Smith 1970, 1975). Although this is well established for wind-dispersed pines, the impact of tree squirrels on bird-dispersed pines has been largely ignored. I assessed the impact of tree squirrels on the allocation of reproductive energy in the bird-dispersed limber pine (Pinus flexilis) by comparing its cone and seed traits from three sites in the Rocky Mountains where tree squirrels (Tamiasciurus) are present to those from three mountain ranges in the Great Basin where tree squirrels are absent. As predicted, differences between the two regions in individual cone and seed traits are consistent with the hypothesis that tree squirrels are important selective agents on these traits. In the absence of tree squirrels, limber pine allocates more than twice as much energy to kernel compared with that invested in putative seed defenses (cone, resin, and seed coat) as does limber pine where tree squirrels are present. Such a large difference is particularly striking, because tree squirrels may have become extinct in the Great Basin in only the last 12,000 yr. Although many factors influence the allocation of energy to cones and seeds, no single factor other than the presence of tree squirrels is compatible with the large and consistent differences between limber pine in the Rocky Mountains and Great Basin. These results show that tree squirrels are an important constraint on the evolution of cone and seed traits that promote the dispersal of seeds by birds.
Abstract The structure of forests is a fundamental attribute that impacts biodiversity and ecosys... more Abstract The structure of forests is a fundamental attribute that impacts biodiversity and ecosystem services and in turn is influenced by natural disturbances and management practices. Here, we examine spatial variation in the interaction between a specialized predispersal seed predator, common crossbills (Loxia curvirostra), and Scots pine (Pinus sylvestris) in relation to forest structure and tree features in a managed Mediterranean forest. Crossbills preferred to forage in pine stands that were more open, which correspond to older stands or regeneration stands with scattered old seed trees. More open older stands with larger trees tend to produce more cones that are attractive to crossbills, although their use was also consistent with crossbills reducing their risk of predation. Within these patches, crossbills selectively foraged on trees having many small, thin-scaled cones, which require less effort and time to extract the seeds. Crossbills were apparently limited to only a very small subset of the closed Scots pine cones because they have relatively small and ineffective bills for foraging on Scots pine. Given that crossbills foraged on only a small subset of the cones within more open stands, a management strategy that would aid common crossbills is to thin middle-aged stands. This would accelerate the development of older stand structure, which would benefit crossbills by increasing the occurrence of suitably open woodlands, benefit other species that rely on older more open stand structure, and potentially decrease the vulnerability of the forest to fire and drought.
Abstract The Cassia crossbill (Loxia sinesciuris) feeds exclusively on seeds held in serotinous c... more Abstract The Cassia crossbill (Loxia sinesciuris) feeds exclusively on seeds held in serotinous cones of lodgepole pine (Pinus contorta latifolia). Its population, confined to 67 km2 of pine in southern Idaho, declined by ~ 80% between 2003 and 2011 apparently because an increase in the occurrence of hot summer days (≥32 °C) caused the serotinous cones to open and shed their seeds. We hypothesized that the propensity for serotinous cones to open varies across the landscape depending on the maximum temperatures cones experienced. We tested a suite of abiotic variables for predicting the occurrence of open serotinous cones among 1547 trees at 170 sites. The best-supported model indicated that trees with open cones were less frequent on northeastern aspects and as slope increased. Fewer open cones were expected on northeast aspects because they receive less direct solar radiation. However, the decrease in trees with open cones as slope increased on southwest aspects was unexpected. Increased convection on slopes could reduce maximum cone temperatures and account for the decrease of open cones on steeper slopes, regardless of aspects. Although cones are less likely to open on steeper slopes, slopes with southerly aspects are likely the least favorable for pine recruitment and survival. The most favorable sites for both lodgepole pine and the persistence of closed cones are slopes on northeast aspects. Such locations are often dominated by subalpine fir (Abies bifolia). Reforestation of fir-dominated areas with lodgepole pine, therefore, provides a means to expand microclimatic refugia for Cassia crossbills.
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