Gary R. Graves

Whole-genome analyses resolve early branches in the tree of life of modern birds

To better determine the history of modern birds, we performed a genome-scale phylogenetic analysis of 48 species representing all orders of Neoaves using phylogenomic methods created to handle genome-scale data. We recovered a highly resolved tree that confirms previously controversial sister or close relationships. We identified the first divergence in Neoaves, two groups we named Passerea and Columbea, representing independent lineages of diverse and convergently evolved land and water bird species. Among Passerea, we infer the common ancestor of core landbirds to have been an apex predator and confirm independent gains of vocal learning. Among Columbea, we identify pigeons and flamingoes as belonging to sister clades. Even with whole genomes, some of the earliest branches in Neoaves proved challenging to resolve, which was best explained by massive protein-coding sequence convergence and high levels of incomplete lineage sorting that occurred during a rapid radiation after the Cretaceous-Paleogene mass extinction event about 66 million years ago.

Multiscale assessment of patterns of avian species richness

The search for a common cause of species richness gradients has spawned more than 100 explanatory hypotheses in just the past two decades. Despite recent conceptual advances, further refinement of the most plausible models has been stifled by the difficulty of compiling high-resolution databases at continental scales. We used a database of the geographic ranges of 2,869 species of birds breeding in South America (nearly a third of the worlds living avian species) to explore the influence of climate, quadrat area, ecosystem diversity, and topography on species richness gradients at 10 spatial scales (quadrat area, ≈12,300 to ≈1,225,000 km2). Topography, precipitation, topography × latitude, ecosystem diversity, and cloud cover emerged as the most important predictors of regional variability of species richness in regression models incorporating 16 independent variables, although ranking of variables depended on spatial scale. Direct measures of ambient energy such as mean and maximum temperature were of ancillary importance. Species richness values for 1° × 1° latitude-longitude quadrats in the Andes (peaking at 845 species) were ≈30–250% greater than those recorded at equivalent latitudes in the central Amazon basin. These findings reflect the extraordinary abundance of species associated with humid montane regions at equatorial latitudes and the importance of orography in avian speciation. In a broader context, our data reinforce the hypothesis that terrestrial species richness from the equator to the poles is ultimately governed by a synergism between climate and coarse-scale topographic heterogeneity.

An Update of Wallace’s Zoogeographic Regions of the World

Next-Generation Biogeography In 1876, Alfred Russel Wallace mapped the zoogeographical regions of the world, based on the distributions and taxonomic relationships of broadly defined mammalian families. Wallaces classification of zoogeographical regions became a cornerstone of modern biogeography and a reference for a wide variety of biological disciplines, including global biodiversity and conservation sciences. Holt et al. (p. 74, published online 20 December) present a next-generation map of wallacean zoogeographic regions, incorporating phylogenetic data on >20,000 vertebrate species to discern and characterize their natural biogeographic patterns. Mapping the geographic distribution and phylogenetic relationships of 21,037 vertebrate species yields 11 realms. Modern attempts to produce biogeographic maps focus on the distribution of species, and the maps are typically drawn without phylogenetic considerations. Here, we generate a global map of zoogeographic regions by combining data on the distributions and phylogenetic relationships of 21,037 species of amphibians, birds, and mammals. We identify 20 distinct zoogeographic regions, which are grouped into 11 larger realms. We document the lack of support for several regions previously defined based on distributional data and show that spatial turnover in the phylogenetic composition of vertebrate assemblages is higher in the Southern than in the Northern Hemisphere. We further show that the integration of phylogenetic information provides valuable insight on historical relationships among regions, permitting the identification of evolutionarily unique regions of the world.

The use of isotope tracers for identifying populations of migratory birds

Abstract To determine whether stable isotopes can be used for identifying the geographic origins of migratory bird populations, we examined the isotopic composition of hydrogen (deuterium, δD), carbon (δ13C), and strontium (δ87Sr) in tissues of a migratory passerine, the black-throated blue warbler (Dendroica caerulescens), throughout its breeding range in eastern North America. δD and δ13C values in feathers, which are grown in the breeding area, varied systematically along a latitudinal gradient, being highest in samples from the southern end of the species’ breeding range in Georgia and lowest in southern Canada. In addition, δD decreased from east to west across the northern part of the breeding range, from New Brunswick to Michigan. δ87Sr ratios were highest in the Appalachian Mountains, and decreased towards the west. These patterns are consistent with geographical variation in the isotopic composition of the natural environment, i.e., with that of precipitation, plants, and soils for δD, δ13C, and δ87Sr, respectively. Preliminary analyses of the δD and δ13C composition of feathers collected from warblers in their Caribbean winter grounds indicate that these individuals were mostly from northern breeding populations. Furthermore, variances in isotope ratios in samples from local areas in winter tended to be larger than those in summer, suggesting that individuals from different breeding localities may mix in winter habitats. These isotope markers, therefore, have the potential for locating the breeding origins of migratory species on their winter areas, for quantifying the degree of mixing of breeding populations on migratory and wintering sites, and for documenting other aspects of the population structure migratory animals – information needed for studies of year-round ecology of these species as well as for their conservation. Combining information from several stable isotopes will help to increase the resolution for determining the geographic origins of individuals in such highly vagile populations.

Comparative genomics reveals insights into avian genome evolution and adaptation

Birds are the most species-rich class of tetrapod vertebrates and have wide relevance across many research fields. We explored bird macroevolution using full genomes from 48 avian species representing all major extant clades. The avian genome is principally characterized by its constrained size, which predominantly arose because of lineage-specific erosion of repetitive elements, large segmental deletions, and gene loss. Avian genomes furthermore show a remarkably high degree of evolutionary stasis at the levels of nucleotide sequence, gene synteny, and chromosomal structure. Despite this pattern of conservation, we detected many non-neutral evolutionary changes in protein-coding genes and noncoding regions. These analyses reveal that pan-avian genomic diversity covaries with adaptations to different lifestyles and convergent evolution of traits.

Predicting continental-scale patterns of bird species richness with spatially explicit models

The causes of global variation in species richness have been debated for nearly two centuries with no clear resolution in sight. Competing hypotheses have typically been evaluated with correlative models that do not explicitly incorporate the mechanisms responsible for biotic diversity gradients. Here, we employ a fundamentally different approach that uses spatially explicit Monte Carlo models of the placement of cohesive geographical ranges in an environmentally heterogeneous landscape. These models predict species richness of endemic South American birds (2248 species) measured at a continental scale. We demonstrate that the principal single-factor and composite (species-energy, water-energy and temperature-kinetics) models proposed thus far fail to predict (r2⩽0.05) the richness of species with small to moderately large geographical ranges (first three range-size quartiles). These species constitute the bulk of the avifauna and are primary targets for conservation. Climate-driven models performed reasonably well only for species with the largest geographical ranges (fourth quartile) when range cohesion was enforced. Our analyses suggest that present models inadequately explain the extraordinary diversity of avian species in the montane tropics, the most species-rich region on Earth. Our findings imply that correlative climatic models substantially underestimate the importance of historical factors and small-scale niche-driven assembly processes in shaping contemporary species-richness patterns.

Global phylogeographic limits of Hawaii's avian malaria

The introduction of avian malaria (Plasmodium relictum) to Hawaii has provided a model system for studying the influence of exotic disease on naive host populations. Little is known, however, about the origin or the genetic variation of Hawaiis malaria and traditional classification methods have confounded attempts to place the parasite within a global ecological and evolutionary context. Using fragments of the parasite mitochondrial gene cytochrome b and the nuclear gene dihydrofolate reductase-thymidylate synthase obtained from a global survey of greater than 13 000 avian samples, we show that Hawaiis avian malaria, which can cause high mortality and is a major limiting factor for many species of native passerines, represents just one of the numerous lineages composing the morphological parasite species. The single parasite lineage detected in Hawaii exhibits a broad host distribution worldwide and is dominant on several other remote oceanic islands, including Bermuda and Moorea, French Polynesia. The rarity of this lineage in the continental New World and the restriction of closely related lineages to the Old World suggest limitations to the transmission of reproductively isolated parasite groups within the morphological species.

Macroecological signals of species interactions in the Danish avifauna.

The role of intraspecific and interspecific interactions in structuring biotic communities at fine spatial scales is well documented, but the signature of species interactions at coarser spatial scales is unclear. We present evidence that species interactions may be a significant factor in mediating the regional assembly of the Danish avifauna. Because >95% of breeding species (n = 197) are migratory, we hypothesized that dispersal limitation would not be important and that breeding distributions would largely reflect resource availability and autecological habitat preferences. Instead, we detected a striking pattern of spatial segregation between ecologically similar species at two spatial scales with a suite of null models that factored in the spatial distribution of habitats in Denmark as well as population size and biomass of each species. Habitat utilization analyses indicated that community-wide patterns of spatial segregation could not be attributed to the patchy distribution of habitat or to gross differences in habitat utilization among ecologically similar species. We hypothesize that, when habitat patch size is limited, conspecific attraction in concert with interspecific territoriality may result in spatially segregated distributions of ecologically similar species at larger spatial scales. In the Danish avifauna, the effects of species interactions on community assembly appear pervasive and can be discerned at grain sizes up to four orders of magnitude larger than those of individual territories. These results suggest that species interactions should be incorporated into species distribution modeling algorithms designed to predict species occupancy patterns based on environmental variables.

A Multilocus Molecular Phylogeny of the Parrots (Psittaciformes): Support for a Gondwanan Origin during the Cretaceous

The question of when modern birds (Neornithes) first diversified has generated much debate among avian systematists. Fossil evidence generally supports a Tertiary diversification, whereas estimates based on molecular dating favor an earlier diversification in the Cretaceous period. In this study, we used an alternate approach, the inference of historical biogeographic patterns, to test the hypothesis that the initial radiation of the Order Psittaciformes (the parrots and cockatoos) originated on the Gondwana supercontinent during the Cretaceous. We utilized broad taxonomic sampling (representatives of 69 of the 82 extant genera and 8 outgroup taxa) and multilocus molecular character sampling (3,941 bp from mitochondrial DNA (mtDNA) genes cytochrome oxidase I and NADH dehydrogenase 2 and nuclear introns of rhodopsin intron 1, tropomyosin alpha-subunit intron 5, and transforming growth factor ss-2) to generate phylogenetic hypotheses for the Psittaciformes. Analyses of the combined character partitions using maximum parsimony, maximum likelihood, and Bayesian criteria produced well-resolved and topologically similar trees in which the New Zealand taxa Strigops and Nestor (Psittacidae) were sister to all other psittaciforms and the cockatoo clade (Cacatuidae) was sister to a clade containing all remaining parrots (Psittacidae). Within this large clade of Psittacidae, some traditionally recognized tribes and subfamilies were monophyletic (e.g., Arini, Psittacini, and Loriinae), whereas several others were polyphyletic (e.g., Cyclopsittacini, Platycercini, Psittaculini, and Psittacinae). Ancestral area reconstructions using our Bayesian phylogenetic hypothesis and current distributions of genera supported the hypothesis of an Australasian origin for the Psittaciformes. Separate analyses of the timing of parrot diversification constructed with both Bayesian relaxed-clock and penalized likelihood approaches showed better agreement between geologic and diversification events in the chronograms based on a Cretaceous dating of the basal split within parrots than the chronograms based on a Tertiary dating of this split, although these data are more equivocal. Taken together, our results support a Cretaceous origin of Psittaciformes in Gondwana after the separation of Africa and the India/Madagascar block with subsequent diversification through both vicariance and dispersal. These well-resolved molecular phylogenies will be of value for comparative studies of behavior, ecology, and life history in parrots.

Detection of macro-ecological patterns in South American hummingbirds is affected by spatial scale

Scale is widely recognized as a fundamental conceptual problem in biology, but the question of whether species–richness patterns vary with scale is often ignored in macro–ecological analyses, despite the increasing application of such data in international conservation programmes. We tested for scaling effects in species–richness gradients with spatially scaled data for 241 species of South American hummingbirds (Trochilidae). Analyses revealed that scale matters above and beyond the effect of quadrat area. Species richness was positively correlated with latitude and topographical relief at ten different spatial scales spanning two orders of magnitude (ca. 12300 to ca. 1225000 km2). Surprisingly, when the influence of topography was removed, the conditional variation in species richness explained by latitude fell precipitously to insignificance at coarser spatial scales. The perception of macro–ecological pattern thus depends directly upon the scale of analysis. Although our results suggest there is no single correct scale for macro–ecological analyses, the averaging effect of quadrat sampling at coarser geographical scales obscures the fine structure of species–richness gradients and localized richness peaks, decreasing the power of statistical tests to discriminate the causal agents of regional richness gradients. Ideally, the scale of analysis should be varied systematically to provide the optimal resolution of macro–ecological pattern.