Comparative Transcriptomics of Seasonal Phenotypic Flexibility in Two North American Songbirds.

Phenotypic flexibility allows organisms to reversibly alter their phenotypes to match the changing demands of seasonal environments. Because phenotypic flexibility is mediated, at least in part, by changes in gene regulation, comparative transcriptomic studies can provide insights into the mechanistic underpinnings of seasonal phenotypic flexibility, and the extent to which regulatory responses to changing seasons are conserved across species. To begin to address these questions, we sampled individuals of two resident North American songbird species, American goldfinch (Spinus tristis) and black-capped chickadee (Poecile atricapillus) in summer and winter to measure seasonal variation in pectoralis transcriptomic profiles and to identify conserved and species-specific elements of these seasonal profiles. We found that very few genes exhibited divergent responses to changes in season between species, and instead, a core set of over 1200 genes responded to season concordantly in both species. Moreover, several key metabolic pathways, regulatory networks, and gene functional classes were commonly recruited to induce seasonal phenotypic shifts in these species. The seasonal transcriptomic responses mirror winter increases in pectoralis mass and cellular metabolic intensity documented in previous studies of both species, suggesting that these seasonal phenotypic responses are due in part to changes in gene expression. Despite growing evidence of muscle nonshivering thermogenesis (NST) in young precocial birds, we did not find strong evidence of upregulation of genes putatively involved in NST during winter in either species, suggesting that seasonal modification of muscular NST is not a prominent contributor to winter increases in thermogenic capacity for adult passerine birds. Together, these results provide the first comprehensive overview of potential common regulatory mechanisms underlying seasonally flexible phenotypes in wild, free-ranging birds.

Life-history characteristics influence physiological strategies to cope with hypoxia in Himalayan birds.

Hypobaric hypoxia at high elevation represents an important physiological stressor for montane organisms, but optimal physiological strategies to cope with hypoxia may vary among species with different life histories. Montane birds exhibit a range of migration patterns; elevational migrants breed at high elevations but winter at low elevations or migrate further south, while high-elevation residents inhabit the same elevation throughout the year. Optimal physiological strategies to cope with hypoxia might therefore differ between species that exhibit these two migratory patterns, because they differ in the amount time spent at high elevation. We examined physiological parameters associated with blood-oxygen transport (haemoglobin concentration and haematocrit, i.e. the proportion of red blood cells in blood) in nine species of elevational migrants and six species of high-elevation residents that were sampled along a 2200 m (1000-3200 m) elevational gradient. Haemoglobin concentration increased with elevation within species regardless of migratory strategy, but it was only significantly correlated with haematocrit in elevational migrants. Surprisingly, haemoglobin concentration was not correlated with haematocrit in high-elevation residents, and these species exhibited higher mean cellular haemoglobin concentration than elevational migrants. Thus, alternative physiological strategies to regulate haemoglobin concentration and blood O2 carrying capacity appear to differ among birds with different annual elevational movement patterns.

Spatial patterns of avian malaria prevalence in Zonotrichia capensis on the western slope of the Peruvian Andes.

Environmental heterogeneity largely dictates the spatial distributions of parasites and therefore the susceptibility to infection of host populations. We surveyed avian malaria infections in Rufous-collared sparrows (Zonotrichia capensis) across replicated altitudinal and latitudinal transects along the western slope of the Peruvian Andes to assess geographic patterns of prevalence. We found malaria infection prevalence peaked at midelevations along all 3 altitudinal transects (x ≈ 2,733 m), with highest overall prevalence observed in the northern transect. We observed low levels of malarial parasite diversity, with 94% of infected birds carrying a single Haemoproteus (subgenus Parahaemoproteus) strain. The remaining infected birds harbored either a single alternate Haemoproteus or 1 of 2 Plasmodium strains. Our data suggest that temperature and precipitation are the primary drivers of the spatial patterns in avian malaria prevalence along the western slope of the Andes.

Genomic insights into adaptation to high-altitude environments.

Elucidating the molecular genetic basis of adaptive traits is a central goal of evolutionary genetics. The cold, hypoxic conditions of high-altitude habitats impose severe metabolic demands on endothermic vertebrates, and understanding how high-altitude endotherms cope with the combined effects of hypoxia and cold can provide important insights into the process of adaptive evolution. The physiological responses to high-altitude stress have been the subject of over a century of research, and recent advances in genomic technologies have opened up exciting opportunities to explore the molecular genetic basis of adaptive physiological traits. Here, we review recent literature on the use of genomic approaches to study adaptation to high-altitude hypoxia in terrestrial vertebrates, and explore opportunities provided by newly developed technologies to address unanswered questions in high-altitude adaptation at a genomic scale.

Testing the molecular and evolutionary causes of a 'leapfrog' pattern of geographical variation in coloration.

Understanding the mechanisms accounting for the evolution of phenotypic diversity is central to evolutionary biology. We use molecular and phenotypic data to test hypotheses for 'leapfrog' patterns of geographical variation, in which phenotypically similar, disjunct populations are separated by distinct populations of the same species. Phylogenetic reconstructions revealed independent evolution of melanic plumage characters in different populations in the Neotropical avian genus Arremon. Thus, phenotypic similarities between distant populations cannot be explained by close phylogenetic affinity. Nor can they be attributed to recurring mutations in the MC1R gene, a locus involved in melanic pigmentation. A coalescent analysis indicates that plumage traits have become fixed at a faster rate than expected under genetic drift, suggesting that selection underlies their repeated evolution. In contrast to views that genetic drift drives phenotypic differentiation in Neotropical montane birds, our results imply that geographical variation preceding speciation may reflect the action of deterministic selective processes.

Phylogenetic conservatism and antiquity of a tropical specialization: army-ant-following in the typical antbirds (Thamnophilidae).

One of the most novel foraging strategies in Neotropical birds is army-ant-following, in which birds prey upon arthropods and small vertebrates flushed from the forest floor by swarm raids of the army-ant Eciton burchellii. This specialization is most developed in the typical antbirds (Thamnophilidae) which are divisible into three specialization categories: (1) those that forage at swarms opportunistically as army-ants move through their territories (occasional followers), (2) those that follow swarms beyond their territories but also forage independently of swarms (regular followers), and (3) those that appear incapable of foraging independently of swarms (obligate followers). Although army-ant-following is one of the great spectacles of tropical forests, basic questions about its evolution remain unaddressed. Using a strongly resolved molecular phylogeny of the typical antbirds, we found that army-ant-following is phylogenetically conserved, with regular following having evolved only three times, and that the most likely evolutionary progression was from least (occasional) to more (regular) to most (obligate) specialized, with no reversals from the obligate state. Despite the dependence of the specialists on a single ant species, molecular dating indicates that army-ant-following has persisted in antbirds since the late Miocene. These results provide the first characterization of army-ant-following as an ancient and phylogenetically conserved specialization.

Sequence variation in the coding region of the melanocortin-1 receptor gene (MC1R) is not associated with plumage variation in the blue-crowned manakin (Lepidothrix coronata).

Avian plumage traits are the targets of both natural and sexual selection. Consequently, genetic changes resulting in plumage variation among closely related taxa might represent important evolutionary events. The molecular basis of such differences, however, is unknown in most cases. Sequence variation in the melanocortin-1 receptor gene (MC1R) is associated with melanistic phenotypes in many vertebrate taxa, including several avian species. The blue-crowned manakin (Lepidothrix coronata), a widespread, sexually dichromatic passerine, exhibits striking geographic variation in male plumage colour across its range in southern Central America and western Amazonia. Northern males are black with brilliant blue crowns whereas southern males are green with lighter blue crowns. We sequenced 810 bp of the MC1R coding region in 23 individuals spanning the range of male plumage variation. The only variable sites we detected among L. coronata sequences were four synonymous substitutions, none of which were strictly associated with either plumage type. Similarly, comparative analyses showed that L. coronata sequences were monomorphic at the three amino acid sites hypothesized to be functionally important in other birds. These results demonstrate that genes other than MC1R underlie melanic plumage polymorphism in blue-crowned manakins.

Complex evolutionary history of a Neotropical lowland forest bird (Lepidothrix coronata) and its implications for historical hypotheses of the origin of Neotropical avian diversity.

Here we apply a combination of phylogeographic and historical demographic analyses to the study of mtDNA sequence variation within the Blue-crowned Manakin (Lepidothrix coronata), a widespread Neotropical bird. A high degree of phylogeographic structure allowed us to demonstrate that several vicariant events, including Andean uplift, the formation of riverine barriers, and climatically induced vegetational shifts, as well as a non-vicariant process, range expansion, have all acted, at varying spatial and temporal scales, to influence genetic structure within L. coronata, suggesting that current historical hypotheses of the origin of Neotropical avian diversity that focus on single vicariant mechanisms may be overly simplistic. Our data also support an origin (>2 mybp) that is substantially older than the late Pleistocene for the genetic structure within this species and indicate that phylogeographic patterns within the species are not concordant with plumage-based subspecific taxonomy. These data add to a growing body of evidence suggesting that the origin of several Neotropical avian species may have occurred in the mid-Pliocene, thus, geological arguments surrounding putative Pleistocene vicariant events, while interesting in their own right, may have little relevance to Neotropical avian diversification at the species level.