Elizabeth P. Derryberry

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.

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.

The drivers of tropical speciation

Since the recognition that allopatric speciation can be induced by large-scale reconfigurations of the landscape that isolate formerly continuous populations, such as the separation of continents by plate tectonics, the uplift of mountains or the formation of large rivers, landscape change has been viewed as a primary driver of biological diversification. This process is referred to in biogeography as vicariance. In the most species-rich region of the world, the Neotropics, the sundering of populations associated with the Andean uplift is ascribed this principal role in speciation. An alternative model posits that rather than being directly linked to landscape change, allopatric speciation is initiated to a greater extent by dispersal events, with the principal drivers of speciation being organism-specific abilities to persist and disperse in the landscape. Landscape change is not a necessity for speciation in this model. Here we show that spatial and temporal patterns of genetic differentiation in Neotropical birds are highly discordant across lineages and are not reconcilable with a model linking speciation solely to landscape change. Instead, the strongest predictors of speciation are the amount of time a lineage has persisted in the landscape and the ability of birds to move through the landscape matrix. These results, augmented by the observation that most species-level diversity originated after episodes of major Andean uplift in the Neogene period, suggest that dispersal and differentiation on a matrix previously shaped by large-scale landscape events was a major driver of avian speciation in lowland Neotropical rainforests.

LINEAGE DIVERSIFICATION AND MORPHOLOGICAL EVOLUTION IN A LARGE-SCALE CONTINENTAL RADIATION: THE NEOTROPICAL OVENBIRDS AND WOODCREEPERS (AVES: FURNARIIDAE)

Patterns of diversification in species‐rich clades provide insight into the processes that generate biological diversity. We tested different models of lineage and phenotypic diversification in an exceptional continental radiation, the ovenbird family Furnariidae, using the most complete species‐level phylogenetic hypothesis produced to date for a major avian clade (97% of 293 species). We found that the Furnariidae exhibit nearly constant rates of lineage accumulation but show evidence of constrained morphological evolution. This pattern of sustained high rates of speciation despite limitations on phenotypic evolution contrasts with the results of most previous studies of evolutionary radiations, which have found a pattern of decelerating diversity‐dependent lineage accumulation coupled with decelerating or constrained phenotypic evolution. Our results suggest that lineage accumulation in tropical continental radiations may not be as limited by ecological opportunities as in temperate or island radiations. More studies examining patterns of both lineage and phenotypic diversification are needed to understand the often complex tempo and mode of evolutionary radiations on continents.

High dispersal ability inhibits speciation in a continental radiation of passerine birds

Dispersal can stimulate speciation by facilitating geographical expansion across barriers or inhibit speciation by maintaining gene flow among populations. Therefore, the relationship between dispersal ability and speciation rates can be positive or negative. Furthermore, an ‘intermediate dispersal’ model that combines positive and negative effects predicts a unimodal relationship between dispersal and diversification. Because both dispersal ability and speciation rates are difficult to quantify, empirical evidence for the relationship between dispersal and diversification remains scarce. Using a surrogate for flight performance and a species-level DNA-based phylogeny of a large South American bird radiation (the Furnariidae), we found that lineages with higher dispersal ability experienced lower speciation rates. We propose that the degree of fragmentation or permeability of the geographical setting together with the intermediate dispersal model are crucial in reconciling previous, often contradictory findings regarding the relationship between dispersal and diversification.

SONG DIVERGENCE BY SENSORY DRIVE IN AMAZONIAN BIRDS

Visual signals are shaped by variation in the signaling environment through a process termed sensory drive, sometimes leading to speciation. However, the evidence for sensory drive in acoustic signals is restricted to comparisons between highly dissimilar habitats, or single‐species studies in which it is difficult to rule out the influence of undetected ecological variables, pleiotropic effects, or chance. Here we assess whether this form of sensory drive—often termed “acoustic adaptation”—can generate signal divergence across ecological gradients. By studying avian communities in two Amazonian forest types, we show that songs of 17 “bamboo‐specialist” bird species differ in predictable ways from their nearest relatives in adjacent terra firme forest. We also demonstrate that the direction of song divergence is correlated with the sound transmission properties of habitats, rather than with genetic divergence, ambient noise, or pleiotropic effects of mass and bill size. Our findings indicate that acoustic adaptation adds significantly to stochastic processes underlying song divergence, even when comparing between habitats with relatively similar structure. Furthermore, given that song differences potentially contribute to reproductive isolation, these findings are consistent with a wider role for sensory drive in the diversification of lineages with acoustic mating signals.

Ecology Shapes Birdsong Evolution: Variation in Morphology and Habitat Explains Variation in White‐Crowned Sparrow Song

Ecological variation appears to underlie the evolution of mating signals in many taxa, yet understanding of how this process occurs over time is limited. Here, I investigate whether changes over time in a well‐studied mating signal—birdsong—are attributable to ecological factors that affect signal production and transmission. Variation in the acoustic properties of songs is thought to be affected by the mechanics of sound production as well as by features of the habitat that affect sound transmission. To determine whether these mechanisms contribute to song variation, I compare patterns of morphological and habitat variation with variation in song structure among populations of white‐crowned sparrows (Zonotrichia leucophrys) at two time points separated by 35 years. Among contemporary (2005) populations, vegetation density and bill size explain significant variation in song structure. The direction of change in song structure between 1970 and 2005 is also consistent with the direction of change in vegetation density. These findings suggest that variation in factors that affect signal production and transmission explains significant variation in white‐crowned sparrow song.

Species coexistence and the dynamics of phenotypic evolution in adaptive radiation

Interactions between species can promote evolutionary divergence of ecological traits and social signals, a process widely assumed to generate species differences in adaptive radiation. However, an alternative view is that lineages typically interact when relatively old, by which time selection for divergence is weak and potentially exceeded by convergent selection acting on traits mediating interspecific competition. Few studies have tested these contrasting predictions across large radiations, or by controlling for evolutionary time. Thus the role of species interactions in driving broad-scale patterns of trait divergence is unclear. Here we use phylogenetic estimates of divergence times to show that increased trait differences among coexisting lineages of ovenbirds (Furnariidae) are explained by their greater evolutionary age in relation to non-interacting lineages, and that—when these temporal biases are accounted for—the only significant effect of coexistence is convergence in a social signal (song). Our results conflict with the conventional view that coexistence promotes trait divergence among co-occurring organisms at macroevolutionary scales, and instead provide evidence that species interactions can drive phenotypic convergence across entire radiations, a pattern generally concealed by biases in age.

HZAR: hybrid zone analysis using an R software package

We present a new software package (hzar) that provides functions for fitting molecular genetic and morphological data from hybrid zones to classic equilibrium cline models using the Metropolis–Hastings Markov chain Monte Carlo (MCMC) algorithm. The software applies likelihood functions appropriate for different types of data, including diploid and haploid genetic markers and quantitative morphological traits. The modular design allows flexibility in fitting cline models of varying complexity. To facilitate hypothesis testing, an autofit function is included that allows automated model selection from a set of nested cline models. Cline parameter values, such as cline centre and cline width, are estimated and may be compared statistically across clines. The package is written in the R language and is available through the Comprehensive R Archive Network (CRAN; http://cran.r-project.org/). Here, we describe hzar and demonstrate its use with a sample data set from a well‐studied hybrid zone in western Panama between white‐collared (Manacus candei) and golden‐collared manakins (M. vitellinus). Comparisons of our results with previously published results for this hybrid zone validate the hzar software. We extend analysis of this hybrid zone by fitting additional models to molecular data where appropriate.

Next-generation sequencing reveals phylogeographic structure and a species tree for recent bird divergences

Next generation sequencing (NGS) technologies are revolutionizing many biological disciplines but have been slow to take root in phylogeography. This is partly due to the difficulty of using NGS to sequence orthologous DNA fragments for many individuals at low cost. We explore cases of recent divergence in four phylogenetically diverse avian systems using a method for quick and cost-effective generation of primary DNA sequence data using pyrosequencing. NGS data were processed using an analytical pipeline that reduces many reads into two called alleles per locus per individual. Using single nucleotide polymorphisms (SNPs) mined from the loci, we detected population differentiation in each of the four bird systems, including: a case of ecological speciation in rails (Rallus); a rapid postglacial radiation in the genus Junco; recent in situ speciation among hummingbirds (Trochilus) in Jamaica; and subspecies of white-crowned sparrows (Zonotrichia leucophrys) along the Pacific coast. The number of recovered loci aligning closely to chromosomal locations on the zebra finch (Taeniopygia guttata) genome was highly correlated to the size of the chromosome, suggesting that loci are randomly distributed throughout the genome. Using eight loci found in Zonotrichia and Junco lineages, we were also able to generate a species tree of these sparrow sister genera, demonstrating the potential of this method for generating data amenable to coalescent-based analysis. We discuss improvements that should enhance the methods utility for primary data generation.