Contrasting drivers of diversity in hosts and parasites across the tropical Andes.

Geographic turnover in community composition is created and maintained by eco-evolutionary forces that limit the ranges of species. One such force may be antagonistic interactions among hosts and parasites, but its general importance is unknown. Understanding the processes that underpin turnover requires distinguishing the contributions of key abiotic and biotic drivers over a range of spatial and temporal scales. Here, we address these challenges using flexible, nonlinear models to identify the factors that underlie richness (alpha diversity) and turnover (beta diversity) patterns of interacting host and parasite communities in a global biodiversity hot spot. We sampled 18 communities in the Peruvian Andes, encompassing ∼1,350 bird species and ∼400 hemosporidian parasite lineages, and spanning broad ranges of elevation, climate, primary productivity, and species richness. Turnover in both parasite and host communities was most strongly predicted by variation in precipitation, but secondary predictors differed between parasites and hosts, and between contemporary and phylogenetic timescales. Host communities shaped parasite diversity patterns, but there was little evidence for reciprocal effects. The results for parasite communities contradicted the prevailing view that biotic interactions filter communities at local scales while environmental filtering and dispersal barriers shape regional communities. Rather, subtle differences in precipitation had strong, fine-scale effects on parasite turnover while host-community effects only manifested at broad scales. We used these models to map bird and parasite turnover onto the ecological gradients of the Andean landscape, illustrating beta-diversity hot spots and their mechanistic underpinnings.

Blood Variation Implicates Respiratory Limits on Elevational Ranges of Andean Birds.

AbstractThe extent to which species ranges reflect intrinsic physiological tolerances is a major question in evolutionary ecology. To date, consensus has been hindered by the limited tractability of experimental approaches across most of the tree of life. Here, we apply a macrophysiological approach to understand how hematological traits related to oxygen transport shape elevational ranges in a tropical biodiversity hot spot. Along Andean elevational gradients, we measured traits that affect blood oxygen-carrying capacity-total and cellular hemoglobin concentration and hematocrit, the volume percentage of red blood cells-for 2,355 individuals of 136 bird species. We used these data to evaluate the influence of hematological traits on elevational ranges. First, we asked whether the sensitivity of hematological traits to changes in elevation is predictive of elevational range breadth. Second, we asked whether variance in hematological traits changed as a function of distance to the nearest elevational range limit. We found that birds showing greater hematological sensitivity had broader elevational ranges, consistent with the idea that a greater acclimatization capacity facilitates elevational range expansion. We further found reduced variation in hematological traits in birds sampled near their elevational range limits and at high absolute elevations, patterns consistent with intensified natural selection, reduced effective population size, or compensatory changes in other cardiorespiratory traits. Our findings suggest that constraints on hematological sensitivity and local genetic adaptation to oxygen availability promote the evolution of the narrow elevational ranges that underpin tropical montane biodiversity.

Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau.

When different species experience similar selection pressures, the probability of evolving similar adaptive solutions may be influenced by legacies of evolutionary history, such as lineage-specific changes in genetic background. Here we test for adaptive convergence in hemoglobin (Hb) function among high-altitude passerine birds that are native to the Qinghai-Tibet Plateau, and we examine whether convergent increases in Hb-O2 affinity have a similar molecular basis in different species. We documented that high-altitude parid and aegithalid species from the Qinghai-Tibet Plateau have evolved derived increases in Hb-O2 affinity in comparison with their closest lowland relatives in East Asia. However, convergent increases in Hb-O2 affinity and convergence in underlying functional mechanisms were seldom attributable to the same amino acid substitutions in different species. Using ancestral protein resurrection and site-directed mutagenesis, we experimentally confirmed two cases in which parallel substitutions contributed to convergent increases in Hb-O2 affinity in codistributed high-altitude species. In one case involving the ground tit (Parus humilis) and gray-crested tit (Lophophanes dichrous), parallel amino acid replacements with affinity-enhancing effects were attributable to nonsynonymous substitutions at a CpG dinucleotide, suggesting a possible role for mutation bias in promoting recurrent changes at the same site. Overall, most altitude-related changes in Hb function were caused by divergent amino acid substitutions, and a select few were caused by parallel substitutions that produced similar phenotypic effects on the divergent genetic backgrounds of different species.

Life history predicts flight muscle phenotype and function in birds.

Functional traits are the essential phenotypes that underlie an organism's life history and ecology. Although biologists have long recognized that intraspecific variation is consequential to an animals' ecology, studies of functional variation are often restricted to species-level comparisons, ignoring critical variation within species. In birds, interspecific comparisons have been foundational in connecting flight muscle phenotypes to species-level ecology, but intraspecific variation has remained largely unexplored. We asked how age- and sex-dependent demands on flight muscle function are reconciled in birds. The flight muscle is an essential multifunctional organ, mediating a large range of functions associated with powered flight and thermoregulation. These functions must be balanced over an individual's lifetime. We leveraged within- and between-species comparisons in a clade of small passerines (Tarsiger bush-robins) from the eastern edge of the Qinghai-Tibet Plateau. We integrated measurements of flight muscle physiology, morphology, behaviour, phenology and environmental data, analysing trait data within a context of three widespread, adaptive life-history strategies-sexual dichromatism, age and sex-structured migration, and delayed plumage maturation. This approach provides a framework of the selective forces that shape functional variation within and between species. We found more variation in flight muscle traits within species than has been previously described between species of birds under 20 g. This variation was associated with the discovery of mixed muscle fibre types (i.e. both fast glycolytic and fast oxidative fibres), which differ markedly in their physiological and functional attributes. This result is surprising given that the flight muscles of small birds are generally thought to contain only fast oxidative fibres, suggesting a novel ecological context for glycolytic muscle fibres in small birds. Within each species, flight muscle phenotypes varied by age and sex, reflecting the functional demands at different life-history stages and the pressures that individuals face as a result of their multi-class identity (i.e. species, age and sex). Our findings reveal new links between avian physiology, ecology, behaviour and life history, while demonstrating the importance of demographic-dependent selection in shaping functional phenotypic variation.

Bird specimens track 135 years of atmospheric black carbon and environmental policy.

Atmospheric black carbon has long been recognized as a public health and environmental concern. More recently, black carbon has been identified as a major, ongoing contributor to anthropogenic climate change, thus making historical emission inventories of black carbon an essential tool for assessing past climate sensitivity and modeling future climate scenarios. Current estimates of black carbon emissions for the early industrial era have high uncertainty, however, because direct environmental sampling is sparse before the mid-1950s. Using photometric reflectance data of >1,300 bird specimens drawn from natural history collections, we track relative ambient concentrations of atmospheric black carbon between 1880 and 2015 within the US Manufacturing Belt, a region historically reliant on coal and dense with industry. Our data show that black carbon levels within the region peaked during the first decade of the 20th century. Following this peak, black carbon levels were positively correlated with coal consumption through midcentury, after which they decoupled, with black carbon concentrations declining as consumption continued to rise. The precipitous drop in atmospheric black carbon at midcentury reflects policies promoting burning efficiency and fuel transitions rather than regulating emissions alone. Our findings suggest that current emission inventories based on predictive modeling underestimate levels of atmospheric black carbon for the early industrial era, suggesting that the contribution of black carbon to past climate forcing may also be underestimated. These findings build toward a spatially dynamic emission inventory of black carbon based on direct environmental sampling.

Differential high-altitude adaptation and restricted gene flow across a mid-elevation hybrid zone in Andean tit-tyrant flycatchers.

The tropical Andes are a global hotspot of avian diversity that is characterized by dramatic elevational shifts in community composition and a preponderance of recently evolved species. Bird habitats in the Andes span a nearly twofold range of atmospheric pressure that poses challenges for respiration, thermoregulation, water balance and powered flight, but the extent to which physiological constraints limit species' elevational distributions is poorly understood. We report a previously unknown hybrid zone between recently diverged flycatchers (Aves, Tyrannidae) with partially overlapping elevational ranges. The southern Anairetes reguloides has a broad elevational range (0-4200 m), while the northern Anairetes nigrocristatus is restricted to high elevations (>2200 m). We found hybrids in central Peru at elevations between ~3100 and 3800 m, with A. nigrocristatus above this elevation and A. reguloides below. We analysed variation in haematology, heart mass, morphometrics, plumage and one mitochondrial and three nuclear loci across an elevational transect that encompasses the hybrid zone. Phenotypic traits and genetic markers all showed steep clines across the hybrid zone. Haemoglobin concentration, haematocrit, mean cellular haemoglobin concentration and relative heart mass each increased at altitude more strongly in A. reguloides than in A. nigrocristatus. These findings suggest that A. nigrocristatus is more resistant than A. reguloides to high-altitude hypoxic respiratory stress. Considering that the ancestor of the genus is suggested to have been restricted to high elevations, A. reguloides may be secondarily adapted to low altitude. We conclude that differential respiratory specialization on atmospheric pressure combined with competitive exclusion maintains replacement along an elevational contour, despite interbreeding.

An improved phylogeny of the Andean tit-tyrants (Aves, Tyrannidae): more characters trump sophisticated analyses.

The phylogeny of the flycatcher genus Anairetes was previously inferred using short fragments of mitochondrial DNA and parsimony and distance-based methods. The resulting topology spurred taxonomic revision and influenced understanding of Andean biogeography. More than a decade later, we revisit the phylogeny of Anairetes tit-tyrants using more mtDNA characters, seven unlinked loci (three mitochondrial genes, six nuclear loci), more closely related outgroup taxa, partitioned Bayesian analyses, and two coalescent species-tree approaches (Bayesian estimation of species trees, BEST; Bayesian evolutionary analysis by sampling trees, (*)BEAST). Of these improvements in data and analyses, the fourfold increase in mtDNA characters was both necessary and sufficient to incur a major shift in the topology and near-complete resolution. The species-tree analyses, while theoretically preferable to concatenation or single gene approaches, yielded topologies that were compatible with mtDNA but with weaker statistical resolution at nodes. The previous results that had led to taxonomic and biogeographic reappraisal were refuted, and the current results support the resurrection of the genus Uromyias as the sister clade to Anairetes. The sister relationship between these two genera corresponds to an ecological dichotomy between a depauperate humid cloud forest clade and a diverse dry-tolerant clade that has diversified along the latitudinal axis of the Andes. The species-tree results and the concatenation results each reaffirm the primacy of mtDNA to provide phylogenetic signal for avian phylogenies at the species and subspecies level. This is due in part to the abundance of informative characters in mtDNA, and in part to its lower effective population size that causes it to more faithfully track the species tree.

Dung-associated arthropods influence foraging ecology and habitat selection in Black-necked Cranes (Grus nigricollis) on the Qinghai-Tibet Plateau.

Variation in grassland vegetation structure influences the habitat selection of insectivorous birds. This variation presents a trade-off for insectivorous predators: Arthropod abundance increases with vegetation height and heterogeneity, but access to arthropod prey items decreases. In contrast, grazing by large herbivores reduces and homogenizes vegetation, decreasing total arthropod abundance and diversity. However, the presence of livestock dung may help counteract the overall reduction in invertebrates by increasing arthropods associated with dung. It is unclear, however, how the presence of arthropod prey in dung contributes to overall habitat selection for insectivorous birds or how dung-associated arthropods affect trade-offs between vegetation structure, arthropod abundance, and access to prey. To explore these relationships, we studied habitat selection of the Black-necked Crane (Grus nigricollis), a large omnivorous bird that breeds on the Qinghai-Tibet Plateau. We assessed the relationships between habitat selection of cranes and vegetation structure, arthropod abundance, and the presence of yak dung. We found that Black-necked Cranes disproportionately foraged in grassland patches with short sward height, low sward height heterogeneity, and high numbers of dry yak dung, despite these habitats having lower total arthropod abundance. Although total arthropod abundance is lower, these habitats are supplemented with dry yak dung, which are associated with coleopteran larvae, making dung pats an indicator of food resources for breeding Black-necked Cranes. Coleopteran adults and larvae in yak dung appear to be an important factor influencing the habitat selection of Black-necked Cranes and should be considered when assessing grassland foraging trade-offs of insectivorous birds. This research provides new insights into the role of livestock dung in defining foraging habitats and resources for insectivorous predators.