Seasonal patterns of dietary partitioning in vertebrates.

Dietary partitioning plays a central role in biological communities, yet the extent of partitioning often varies dramatically over time. Food availability may drive temporal variation in dietary partitioning, but alternative paradigms offer contrasting predictions about its effect. We compiled estimates of dietary overlap between co-occurring vertebrates to test whether partitioning is greater during periods of high or low food abundance. We found that dietary partitioning was generally greatest when food abundance was low, suggesting that competition for limited food drives partitioning. The extent of dietary partitioning in birds and mammals was also related to seasonality in primary productivity. As seasonality increased, partitioning increased during the nonbreeding season for birds and the breeding season for mammals. Although some hypotheses invoke changes in dietary breadth to explain temporal variation in dietary partitioning, we found no association between dietary breadth and partitioning. These results have important implications for the evolution of dietary divergence.

Performance Trade-Offs and Resource Availability Drive Variation in Reproductive Isolation between Sympatrically Diverging Crossbills.

AbstractTheoretical models indicate that speciation, especially when the scope for gene flow is great (e.g., sympatric speciation), is most likely when strong performance trade-offs coincide with reproduction. We tested this classic hypothesis using measures of the strength of three prezygotic reproductive isolating barriers (habitat isolation, reduced immigrant fecundity, and behavioral isolation) between two young (~2,000 years) and sympatric red crossbill (Loxia curvirostra) ecotypes. All three isolating barriers increased with increases in performance trade-offs, with total reproductive isolation varying between 0.72 and 1 (0 represents random mating, and 1 represents complete reproductive isolation). Strong trade-offs led to strong habitat isolation, an inability to breed in the "wrong" habitat, and more assortative flocks, with the latter leading to stronger behavioral isolation. Reproductive isolation decreased as resource availability increased relative to the demands of breeding, with higher resource availabilities eliminating the positive relationship between reproductive isolation and performance trade-offs. This latter result is consistent with previous work suggesting that increasing resource abundance dampens the effect of strong performance trade-offs on evolutionary divergence. Because many organisms, with the notable exception of host-specific phytophagous insects, rely on abundant food resources with weak performance trade-offs while breeding, our results may explain why sympatric speciation is uncommon.

Enhanced seed defenses potentially relax selection by seed predators against serotiny in lodgepole pine.

Serotiny, the retention of seeds in a canopy seed bank until high temperatures cause seeds to be released, is an important life history trait for many woody plants in fire-prone habitats. Serotiny provides a competitive advantage after fire but increases vulnerability to predispersal seed predation, due to the seeds being retained in clusters in predictable locations for extended periods. This creates opposing selection pressures. Serotiny is favored in areas of high fire frequency, but is selected against by predispersal seed predators. However, predation also selects for cone traits associated with seed defense that could reduce predation on serotinous cones and thereby relax selection against serotiny. This helps explain the elevated defenses in highly serotinous species. However, whether such interactions drive variation in seed defenses within variably serotinous populations has been studied rarely. We investigated the effects of phenotypic selection exerted by red squirrel (Tamiasciurus hudsonicus) predation on Rocky Mountain lodgepole pine (Pinus contorta latifolia) seeds. Squirrels preferentially harvested cones with more and larger seeds, indicating a preference for a higher food reward. We found evidence for stronger selection on trees with serotinous cones, which presumably accounts for the elevated defenses of and lower predation on serotinous compared to non-serotinous cones. Lower levels of predation on serotinous cones in turn lessen selection against serotiny by squirrels. This has important implications because the frequency of serotiny in lodgepole pine has profound consequences for post-fire communities and ecosystems widespread in the Rocky Mountains.

Character displacement of a learned behaviour and its implications for ecological speciation.

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 (Loxia curvirostra) complex. Here we focus on Cassia crossbills (Loxia sinesciuris; 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 mechanism by which reproductive isolation can evolve between sympatric lineages as a byproduct of adaptive cultural evolution.

Resource stability and geographic isolation are associated with genome divergence in western Palearctic crossbills.

While many conifers produce annually variable seed crops, serotinous species (which hold seeds in cones for multiple years) represent unusually stable food resources for seed predators. Such stability is conducive to residency and potentially population divergence of consumers as exemplified by the Cassia crossbill (Loxia sinesciuris) in North America. We used genotyping by sequencing (GBS) to test whether three Mediterranean subspecies of common crossbills (L. curvirostra) associated with the serotinous Aleppo pine (Pinus halepensis) were more genetically distinct than European crossbills associated with nonserotinous conifers. We assembled a Cassia crossbill draft genome as a reference for mapping GBS reads and as a first step towards a more contiguous genome assembly. We found clear patterns of genetic divergence for each of the P. halepensis-associated subspecies. Geographic isolation, as promoted by resource stability and residency, is associated with genetic divergence of two of these subspecies. However, geographic isolation cannot account for divergence of L. c. hispana. Instead, resource stability likely contributed to divergence by reducing dispersal and increasing resource competition that may limit breeding by immigrants. In contrast, we found no differentiation among common crossbills associated with less stable resources, and only slight differentiation between common crossbills and parrot crossbills (L. pytyopsittacus). The substantial morphological divergence between common and parrot crossbills has likely originated or been maintained by selection despite gene flow generated by spatiotemporal resource fluctuation. Our results indicate that phenological as well as morphological characteristics of conifers have influenced crossbill diversification, and suggest a possible link between resource stability and population divergence.

Assessing the Potential Contributions of Reduced Immigrant Viability and Fecundity to Reproductive Isolation.

Reduced fitness of immigrants from alternative environments is thought to be an important reproductive isolating barrier. Most studies evaluating the importance of the relative fitness of immigrants to speciation have focused on reduced survival of immigrants (i.e., immigrant inviability). However, variation in fecundity appears to have a greater impact on variation in fitness than does variation in viability, suggesting that reduced fecundity of immigrants could act as an important yet largely overlooked reproductive isolating barrier. Using a model and a survey of studies of local adaptation, we evaluate the relative strength of reduced immigrant viability and fecundity as potential causes of reproductive isolation. We found that reduced fecundity as compared to reduced viability as a reproductive isolating barrier should increase in importance as the relative costs of reproduction increase. Consistent with the elevated demands of reproduction reported in the literature, we found that reproductive isolation from reduced immigrant fecundity was of similar magnitude or greater than that from reduced immigrant viability, particularly in the early stages of speciation. These results suggest that the important role of differential fecundity in local adaptation extends to speciation.

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.

The Natural History of the South Hills Crossbill in Relation to Its Impending Extinction.

Increasingly, the species that we discover will be uncommon, area restricted, and vulnerable to extinction. I describe the natural history of a newly discovered seed-eating finch from the Rocky Mountain region, the South Hills crossbill (Loxia curvirostra complex). It relies on seeds in the closed cones of the fire-adapted Rocky Mountain lodgepole pine (Pinus contorta latifolia) and is found only in the higher elevations of two small mountain ranges in southern Idaho. Here crossbills and pine are engaged in a coevolutionary arms race. Although most of the seeds remain secured within the cones for decades until the heat of a stand-replacing fire causes the cone scales to separate, seeds become accessible to crossbills slowly as cones weather and gaps form between some of the scales. However, hot days (≥32°C), especially four or more hot days, seem to mimic the effect of fire, apparently causing the immediate release of a fraction of the seeds. Such events caused a 20% annual decline in crossbills that lasted up to 4 years and an 80% decline in the population between 2003 and 2011. This is an example of a novel trophic mismatch between a consumer and its resource caused by a shift in the phenology of the resource arising from climate change. Not only do these phenological shifts have the potential to cause seed consumers to decline, these shifts are also likely to cause reduced recruitment of the plants. The South Hills crossbill is especially vulnerable and will likely go extinct this century before lodgepole pine is extirpated from the South Hills.

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 (FST  = 0.011-0.035), we found evidence of relative genetic differentiation (as measured by FST ) 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.

From the ground up: biotic and abiotic features that set the course from genes to ecosystems.

Spatial variation in cone serotiny in Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia) across Yellowstone National Park influences initial pine recruitment after stand-replacing fire with tremendous population, community, and ecosystem consequences. A previous study showed that much of the spatial variation in serotiny results from the balance of selection arising from high frequencies of fire favoring serotiny countered by opposing selection exerted by American red squirrels (Tamiasciurus hudsonicus) as seed predators. This earlier study, however, assumed stable local red squirrel densities over multiple generations of pines. Here, we examine environmental properties that might contribute to long-term stability in the densities of red squirrels among sites. We found that the amount of clay in the soil, an indicator of plant and fungal growth-the latter an important food resource for red squirrels-and the coefficient of variation (CV) in diameter at breast height (DBH) of forest trees together account for a substantial amount of variation in red squirrel density. Soil development occurs over very long time scales, and thus, intersite variation in the amount of clay is unlikely to shift across pine generations. However, CV of DBH and squirrel density increase with stand age, which acts to amplify selection against serotiny with increasing interfire interval. Regardless, much of the variation in the CV of DBH is accounted for by soil bulk density, mean annual temperature, and surface curvature, which are unlikely to vary in their relative differences among sites over time. Consequently, these soil and abiotic attributes could contribute to consistent spatial patterns of red squirrel densities from one pine generation to the next, resulting in consistent local and spatial variation in selection exerted by red squirrels against serotiny.

Phenotypic Selection Exerted by a Seed Predator Is Replicated in Space and Time and among Prey Species.

Although consistent phenotypic selection arising from biotic interactions is thought to be the primary cause of adaptive diversification, studies documenting such selection are relatively few. Here we analyze 12 episodes of phenotypic selection exerted by a predispersal seed predator, the red crossbill (Loxia curvirostra complex), on five species of pines (Pinus). We find that even though the intensity of selection for some traits increased with the strength of the interaction (i.e., proportion of seeds eaten), the relative strength of selection exerted by crossbills on cone and seed traits is replicated across space and time and among species. Such selection (1) can account for repeated patterns of conifer cone evolution and escalation in seed defenses with time and (2) suggests that variation in selection is less the result of variation intrinsic to pairwise biotic interactions than, for example, variation in relative densities of the interacting species, community context, and abiotic factors.

Conflicting selection from fire and seed predation drives fine-scaled phenotypic variation in a widespread North American conifer.

Recent work has demonstrated that evolutionary processes shape ecological dynamics on relatively short timescales (eco-evolutionary dynamics), but demonstrating these effects at large spatial scales in natural landscapes has proven difficult. We used empirical studies and modeling to investigate how selective pressures from fire and predispersal seed predation affect the evolution of serotiny, an ecologically important trait. Serotiny is a highly heritable key reproductive trait in Rocky Mountain lodgepole pine (Pinus contorta subsp. latifolia), a conifer that dominates millions of hectares in western North America. In these forests, the frequency of serotiny determines postfire seedling density with corresponding community- and ecosystem-level effects. We found that serotinous individuals have a selective advantage at high fire frequencies and low predation pressure; however, very high seed predation shifted the selective advantage to nonserotinous individuals even at high fire frequencies. Simulation modeling suggests that spatial variation in the frequency of serotiny results from heterogeneity in these two selective agents. These results, combined with previous findings showing a negative association between the density of seed predators and the frequency of serotiny at both landscape and continental scales, demonstrate that contemporary patterns in serotiny reflect an evolutionary response to conflicting selection pressures from fire and seed predation. Thus, we show that variation in the frequency of a heritable polygenic trait depends on spatial variation in two dominant selective agents, and, importantly, the effects of the local trait variation propagate with profound consequences to the structure and function of communities and ecosystems across a large landscape.

Causes of variation in biotic interaction strength and phenotypic selection along an altitudinal gradient.

Understanding the causes of variation in biotic interaction strength and phenotypic selection remains one of the outstanding goals of evolutionary ecology. Here we examine the variation in strength of interactions between two seed predators, common crossbills (Loxia curvirostra) and European red squirrels (Sciurus vulgaris), and mountain pine (Pinus uncinata) at and below tree limit in the Pyrenees, and how this translates into phenotypic selection. Seed predation by crossbills increased whereas seed predation by squirrels decreased with increasing elevation and as the canopy became more open. Overall, seed predation by crossbills averaged about twice that by squirrels, and the intensity of selection exerted by crossbills averaged between 2.6 and 7.5 times greater than by squirrels. The higher levels of seed predation by crossbills than squirrels were related to the relatively open nature of most of the forests, and the higher intensity of selection exerted by crossbills resulted from their higher levels of seed predation. However, most of the differences in selection intensity between crossbills and squirrels were the result of habitat features having a greater effect on the foraging behavior of squirrels than of crossbills, causing selection to be much lower for squirrels than for crossbills.

Landscape-scale eco-evolutionary dynamics: selection by seed predators and fire determine a major reproductive strategy.

Recent work in model systems has demonstrated significant effects of rapid evolutionary change on ecological processes (eco-evolutionary dynamics). Fewer studies have addressed whether eco-evolutionary dynamics structure natural ecosystems. We investigated variation in the frequency of serotiny in lodgepole pine (Pinus contorta), a widespread species in which postfire seedling density and ecosystem structure are largely determined by serotiny. Serotiny, the retention of mature seeds in cones in a canopy seed bank, is thought to be an adaptation for stand-replacing fire, but less attention has been paid to the potential selective effects of seed predation on serotiny. We hypothesized that spatial variation in percentage serotiny in lodgepole pine forests results from an eco-evolutionary dynamic where the local level of serotiny depends on the relative strengths of conflicting directional selection from fire (favoring serotiny) and seed predation (favoring cones that open at maturity). We measured percentage serotiny, the abundance of American red squirrels (Tamiasciurus hudsonicus; the primary pre-dispersal seed predator of lodgepole pine), and several measures of forest structure in Yellowstone National Park, USA. Fire frequency strongly predicted the frequency of serotiny, a pattern that is well-supported in the literature. At sites with high fire frequency (return intervals of -135-185 years) where fire favors increased serotiny, squirrel abundance was negatively associated with serotiny, suggesting that selection from predation can overwhelm selection from fire when squirrels are abundant. At sites with low fire frequency (return intervals of -280-310 years), serotiny was nearly universally uncommon (< 10%). Finally, forest structure strongly predicted squirrel density independently of serotiny, and serotiny provided no additional explanatory power, suggesting that the correlation is caused by selection against serotiny exerted by squirrels, rather than squirrels responding to variation in percentage serotiny.

Biotic interaction strength and the intensity of selection.

Although the ecological and evolutionary impacts of species interactions have been the foci of much research, the relationship between the strength of species interactions and the intensity of selection has been investigated only rarely. I develop a simple model demonstrating how the opportunity for selection varies with interaction strength, and then use the relationship between the maximum value of the selection differential and the opportunity for selection (Arnold & Wade 1984) to evaluate how selection differentials vary in relation to species interaction strength. This model predicts an initial deceleration and then an accelerating increase in the intensity of selection with increasing strength of antagonistic interactions and with decreasing strength of mutualistic interactions. Empirical data from several studies provide support for this model. These results further support an evolutionary mechanism for some striking patterns of evolutionary diversification including the latitudinal species gradient, and should be relevant to studies of eco-evolutionary dynamics.

Consistency and variation in phenotypic selection exerted by a community of seed predators.

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

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.

Genome-wide association genetics of an adaptive trait in lodgepole pine.

Pine cones that remain closed and retain seeds until fire causes the cones to open (cone serotiny) represent a key adaptive trait in a variety of pine species. In lodgepole pine, there is substantial geographical variation in serotiny across the Rocky Mountain region. This variation in serotiny has evolved as a result of geographically divergent selection, with consequences that extend to forest communities and ecosystems. An understanding of the genetic architecture of this trait is of interest owing to the wide-reaching ecological consequences of serotiny and also because of the repeated evolution of the trait across the genus. Here, we present and utilize an inexpensive and time-effective method for generating population genomic data. The method uses restriction enzymes and PCR amplification to generate a library of fragments that can be sequenced with a high level of multiplexing. We obtained data for more than 95,000 single nucleotide polymorphisms across 98 serotinous and nonserotinous lodgepole pines from three populations. We used a Bayesian generalized linear model (GLM) to test for an association between genotypic variation at these loci and serotiny. The probability of serotiny varied by genotype at 11 loci, and the association between genotype and serotiny at these loci was consistent in each of the three populations of pines. Genetic variation across these 11 loci explained 50% of the phenotypic variation in serotiny. Our results provide a first genome-wide association map of serotiny in pines and demonstrate an inexpensive and efficient method for generating population genomic data.

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.