Bigger or long-winged male common crossbills exhibit redder carotenoid-based plumage coloration.

Carotenoid-based ornaments are often considered reliable (honest) individual condition signals because their expression implies physiological costs unaffordable for low-quality animals (handicap signals). Recently, it has been suggested that efficient cell respiration is mandatory for producing red ketocarotenoids from dietary yellow carotenoids. This implies that red colorations should be entirely unfalsifiable and independent of expression costs (index signals). In a precedent study, male common crossbills, Loxia curvirostra, showing a red plumage reported higher apparent survival than those showing yellowish-orange colors. The plumage redness in this species is due to ketocarotenoid accumulation in feathers. Here, we correlated the male plumage redness (a 4-level visual score: yellow, patchy, orange, and red) and the body morphology in more than 1,000 adult crossbills captured in 3 Iberian localities to infer the mechanisms responsible for color evolution. A principal component analysis summarized morphometry of 10 variables (beak, wing, tarsus length, etc.). The overall body size (PC1) and the length of flight feathers regarding body size (PC3) showed significant positive relationships with plumage redness. Plumage redness was barely correlated with bill shape measures, suggesting no constraint in acquiring carotenoids from pine cones. However, large body sizes or proportionally long flying feathers could help carotenoid acquisition via social competition or increased foraging ranges. Proportionally longer flight feathers might also be associated with a specific cell respiration profile that would simultaneously favor flying capacities and enzymatic transformations needed for ketocarotenoid synthesis. Such a phenotypic profile would agree with the hypothesis of ketocarotenoid-based colors acting as individual quality index signals.

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.

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.

Innate immunity and environmental correlates of Haemoproteus prevalence and intensity in an opportunistic breeder.

While parasite infection can have substantial fitness consequences in organisms, the predictors of parasite prevalence and intensity are often complex and vary depending on the host species. Here, we examined correlates of Haemoproteus (a common malaria parasite) prevalence and intensity in an opportunistically breeding songbird, the red crossbill (Loxia curvirostra). Specifically, we quantified Haemoproteus prevalence and intensity in crossbills caught in the Grand Teton National Park from 2010 to 2013. We found that parasite prevalence varies seasonally and across years, with the highest number of infected individuals occurring in the summer, although there was variation across summers sampled, and that prevalence was positively related to annual mean cone crop sizes (a measure of crossbill food abundance) and daily ambient temperature (a correlate of vector abundance). Parasite intensity was significantly and positively related to one measure of innate immunity, leucocyte counts per blood volume. Finally, neither crossbill age, ecomorph, nor sex had significant effects on parasite infection intensity; however, parasite prevalence did significantly vary among ecomorph and age classes. These results support the interpretation that a combination of physiological (specifically immune activity) and environmental factors affects parasite prevalence and infection intensity in this opportunistically breeding avian species.

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.

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.

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.