Geogenomic predictors of genetree heterogeneity explain phylogeographic and introgression history: a case study in an Amazonian bird (Thamnophilus aethiops).

Can knowledge about genome architecture inform biogeographic and phylogenetic inference? Selection, drift, recombination, and gene flow interact to produce a genomic landscape of divergence wherein patterns of differentiation and genealogy vary nonrandomly across the genomes of diverging populations. For instance, genealogical patterns that arise due to gene flow should be more likely to occur on smaller chromosomes, which experience high recombination, whereas those tracking histories of geographic isolation (reduced gene flow caused by a barrier) and divergence should be more likely to occur on larger and sex chromosomes. In Amazonia, populations of many bird species diverge and introgress across rivers, resulting in reticulated genomic signals. Herein, we used reduced representation genomic data to disentangle the evolutionary history of four populations of an Amazonian antbird, Thamnophilus aethiops, whose biogeographic history was associated with the dynamic evolution of the Madeira River Basin. Specifically, we evaluate whether a large river capture event ca. 200 Ka, gave rise to reticulated genealogies in the genome by making spatially explicit predictions about isolation and gene flow based on knowledge about genomic processes. We first estimated chromosome-level phylogenies and recovered two primary topologies across the genome. The first topology (T1) was most consistent with predictions about population divergence and was recovered for the Z chromosome. The second (T2), was consistent with predictions about gene flow upon secondary contact. To evaluate support for these topologies, we trained a convolutional neural network to classify our data into alternative diversification models and estimate demographic parameters. The best-fit model was concordant with T1 and included gene flow between non-sister taxa. Finally, we modeled levels of divergence and introgression as functions of chromosome length and found that smaller chromosomes experienced higher gene flow. Given that (1) gene-trees supporting T2 were more likely to occur on smaller chromosomes and (2) we found lower levels of introgression on larger chromosomes (and especially the Z-chromosome), we argue that T1 represents the history of population divergence across rivers and T2 the history of secondary contact due to barrier loss. Our results suggest that a significant portion of genomic heterogeneity arises due to extrinsic biogeographic processes such as river capture interacting with intrinsic processes associated with genome architecture. Future phylogeographic studies would benefit from accounting for genomic processes, as different parts of the genome reveal contrasting, albeit complementary histories, all of which are relevant for disentangling the intricate geogenomic mechanisms of biotic diversification.

Amazonian colonization from the Atlantic Forest: New perspectives on the connections of South American tropical forests.

An open and dry vegetation belt separates Amazonia (AM) and the Atlantic Forest (AF). Evidence from palaeoclimatic and phylogenetic studies suggests past connections between these forests during cycles of increased humidity through the formation of forest corridors. The distinctive northern AF avifauna is known to have affinities both with AM and the southern AF. Still, the extent of how these two regions contributed to the assemblage of this avifauna remains poorly understood. Using historical demographic analyses and comparative phylogeography based on sub-genomic genetic sampling, we assessed how past connections between AM and AF led to shared vicariance and colonization events in four avian AF endemic taxa. Our results supported the occurrence of humid forest corridors promoting the contact between AF and AM populations and suggested two vicariant events and two colonization events from AF to AM. Population divergences were mostly non-synchronous and occurred multiple times during the Pleistocene. Historical gene flow was prevalent across study groups, supporting migration flows after the initial separation between AM and AF - a pattern previously unknown in birds between these regions. Idiosyncratic histories and divergent demographic syndromes suggest that organisms' responses to climate-driven habitat shifts broadly depend on their ecological attributes. This study strengthened our knowledge of past connections between AM and AF and provided demographic scenarios amenable for testing in other groups of co-distributed organisms.

AVONET: morphological, ecological and geographical data for all birds.

Functional traits offer a rich quantitative framework for developing and testing theories in evolutionary biology, ecology and ecosystem science. However, the potential of functional traits to drive theoretical advances and refine models of global change can only be fully realised when species-level information is complete. Here we present the AVONET dataset containing comprehensive functional trait data for all birds, including six ecological variables, 11 continuous morphological traits, and information on range size and location. Raw morphological measurements are presented from 90,020 individuals of 11,009 extant bird species sampled from 181 countries. These data are also summarised as species averages in three taxonomic formats, allowing integration with a global phylogeny, geographical range maps, IUCN Red List data and the eBird citizen science database. The AVONET dataset provides the most detailed picture of continuous trait variation for any major radiation of organisms, offering a global template for testing hypotheses and exploring the evolutionary origins, structure and functioning of biodiversity.

Earth history and the passerine superradiation.

Avian diversification has been influenced by global climate change, plate tectonic movements, and mass extinction events. However, the impact of these factors on the diversification of the hyperdiverse perching birds (passerines) is unclear because family level relationships are unresolved and the timing of splitting events among lineages is uncertain. We analyzed DNA data from 4,060 nuclear loci and 137 passerine families using concatenation and coalescent approaches to infer a comprehensive phylogenetic hypothesis that clarifies relationships among all passerine families. Then, we calibrated this phylogeny using 13 fossils to examine the effects of different events in Earth history on the timing and rate of passerine diversification. Our analyses reconcile passerine diversification with the fossil and geological records; suggest that passerines originated on the Australian landmass ∼47 Ma; and show that subsequent dispersal and diversification of passerines was affected by a number of climatological and geological events, such as Oligocene glaciation and inundation of the New Zealand landmass. Although passerine diversification rates fluctuated throughout the Cenozoic, we find no link between the rate of passerine diversification and Cenozoic global temperature, and our analyses show that the increases in passerine diversification rate we observe are disconnected from the colonization of new continents. Taken together, these results suggest more complex mechanisms than temperature change or ecological opportunity have controlled macroscale patterns of passerine speciation.

Comparative phylogeographic and demographic analyses reveal a congruent pattern of sister relationships between bird populations of the northern and south-central Atlantic Forest.

The Pernambuco Center of Endemism (PCE) is the northernmost strip of the Atlantic Forest (AF). Biogeographic affinities among avifaunas in the PCE, the southern-central Atlantic Forest (SCAF), and Amazonia (AM) have not been studied comprehensively, and current patterns of genetic diversity in the PCE remain unclear. The interplay between species' ecological attributes and historical processes, such as Pleistocene climate fluctuations or the appearance of rivers, may have affected population genetic structures in the PCE. Moreover, the role of past connections between the PCE and AM and the elevational distribution of species in assembling the PCE avifauna remain untested. Here, we investigated the biogeographic history of seven taxa endemic to the PCE within a comparative phylogeographic framework based on a mean of 3,618 independent single nucleotide polymorphisms (SNPs) extracted from flanking regions of ultraconserved elements (UCEs) and one mitochondrial gene. We found that PCE populations were more closely related to SCAF populations than they were to those in AM, regardless of their elevational range, with divergence times placed during the Mid-Pleistocene. These splits were consistent with a pattern of allopatric divergence with gene flow until the upper Pleistocene and no signal of rapid changes in population sizes. Our results support the existence of a Pleistocene refugium driving current genetic diversity in the PCE, thereby rejecting the role of the São Francisco River as a primary barrier for population divergence. Additionally, we found that connections with Amazonia also played a significant role in assembling the PCE avifauna through subsequent migration events.

Evidence for the Pleistocene Arc Hypothesis from genome-wide SNPs in a Neotropical dry forest specialist, the Rufous-fronted Thornbird (Furnariidae: Phacellodomus rufifrons).

South American dry forests have a complex and poorly understood biogeographic history. Based on the fragmented distribution of many Neotropical dry forest species, it has been suggested that this biome was more widely distributed and contiguous under drier climate conditions in the Pleistocene. To test this scenario, known as the Pleistocene Arc Hypothesis, we studied the phylogeography of the Rufous-fronted Thornbird (Phacellodomus rufifrons), a widespread dry forest bird with a disjunct distribution closely matching that of the biome itself. We sequenced mtDNA and used ddRADseq to sample 7,167 genome-wide single-nucleotide polymorphisms from 74 P. rufifrons individuals across its range. We found low genetic differentiation over two prominent geographic breaks - particularly across a 1,000 km gap between populations in Bolivia and Northern Peru. Using demographic analyses of the joint site frequency spectrum, we found evidence of recent divergence without subsequent gene flow across those breaks. By contrast, parapatric morphologically distinct populations in northeastern Brazil show high genetic divergence with evidence of recent gene flow. These results, in combination with our paleoclimate species distribution modelling, support the idea that currently disjunct patches of dry forest were more connected in the recent past, probably during the Middle and Late Pleistocene. This notion fits the major predictions of the Pleistocene Arc Hypothesis and illustrates the importance of comprehensive genomic and geographic sampling for examining biogeographic and evolutionary questions in complex ecosystems like Neotropical dry forests.

Phylogeography of the Variable Antshrike (Thamnophilus caerulescens), a South American passerine distributed along multiple environmental gradients.

The Neotropics show a wealth of distributional patterns shared by many co-distributed species. A distinctive pattern is the so-called "circum-Amazonian distribution," which is observed in species that do not occur in Amazonia but rather along a belt of forested habitats spanning south and east of Amazonia, the Andean foothills, and often into the Venezuelan Coastal Range and the Tepuis. Although this pattern is widespread across animals and plants, its underlying biogeographic mechanisms remain poorly understood. The Variable Antshrike (Thamnophilus caerulescens) is a sexually dimorphic suboscine passerine that exhibits extreme plumage variation and occurs along the southern portion of the circum-Amazonian belt. We describe broad-scale phylogeographic patterns of T. caerulescens and assess its demographic history using DNA sequences from the mitochondrion and ultraconserved elements (UCEs). We identified three genomic clusters: a) northern Atlantic Forest; b) southeastern Cerrado and central-southern Atlantic Forest, and c) Chaco and Andes. Our results were consistent with Pleistocene divergence followed by gene flow, mainly between the latter two clusters. There were no genetic signatures of rapid population expansions or bottlenecks. The population from the northern Atlantic Forest was the most genetically divergent group within the species. The demographic history of T. caerulescens was probably affected by series of humid and dry periods throughout the Quaternary that generated subtle population expansions and contractions allowing the intermittent connection of habitats along the circum-Amazonian belt. Recognizing the dynamic history of climate-mediated forest expansions, contractions, and connections during the South American Pleistocene is central toward a mechanistic understanding of circum-Amazonian distributions.

Molecular systematics and biogeography of lowland antpittas (Aves, Grallariidae): The role of vicariance and dispersal in the diversification of a widespread Neotropical lineage.

We infer phylogenetic relationships, divergence times, and the diversification history of the avian Neotropical antpitta genera Hylopezus and Myrmothera (Grallariidae), based on sequence data (3,139 base pairs) from two mitochondrial (ND2 and ND3) and three nuclear nuclear introns (TGFB2, MUSK and FGB-I5) from 142 individuals of the 12 currently recognized species in Hylopezus and Myrmothera and 5 outgroup species. Phylogenetic analyses recovered 19 lineages clustered into two major clades, both distributed in Central and South America. Hylopezus nattereri, previously considered a subspecies of H. ochroleucus, was consistently recovered as the most divergent lineage within the Grallaricula/Hylopezus/Myrmothera clade. Ancestral range estimation suggested that modern lowland antpittas probably originated in the Amazonian Sedimentary basin during the middle Miocene, and that most lineages within the Hylopezus/Myrmothera clade appeared in the Plio-Pleistocene. However, the rate of diversification in the Hylopezus/Myrmothera clade appeared to have remained constant through time, with no major shifts over the 20 million years. Although the timing when most modern lineages of the Hylopezus/Myrmothera clade coincides with a period of intense landscape changes in the Neotropics (Plio-Pleistocene), the absence of any significant shifts in diversification rates over the last 20 million years challenges the view that there is a strict causal relationship between intensification of landscape changes and cladogenesis. The relative old age of the Hylopezus/Myrmothera clade coupled with an important role ascribed to dispersal for its diversification, favor an alternative scenario whereby long-term persistence and dispersal across an ever-changing landscape might explain constant rates of cladogenesis through time.

Inferring speciation history in the Andes with reduced-representation sequence data: an example in the bay-backed antpittas (Aves; Grallariidae; Grallaria hypoleuca s. l.).

In the Andes, humid-forest organisms frequently exhibit pronounced genetic structure and geographic variation in phenotype, often coincident with physical barriers to dispersal. However, phylogenetic relationships of clades have often been difficult to resolve due to short internodes. Consequently, even in taxa with well-defined genetic structure, the temporal and geographic sequences of dispersal and vicariance events that led to this differentiation have remained opaque, hindering efforts to test the association between diversification and earth history and to understand the assembly of species-rich communities on Andean slopes. Here, we use mitochondrial DNA and thousands of short-read sequences generated with genotyping by sequencing (GBS) to examine the geographic history of speciation in a lineage of passerine birds found in the humid forest of the Andes, the 'bay-backed' antpitta complex (Grallaria hypoleuca s. l). Mitochondrial DNA genealogies documented genetic structure among clade but were poorly resolved at nodes relevant for biogeographic inference. By contrast, relationships inferred from GBS loci were highly resolved and suggested a biogeographic history in which the ancestor originated in the northern Andes and dispersed south. Our results are consistent with a scenario of vicariant speciation wherein the range of a widespread ancestor was fragmented as a result of geologic or climatic change, rather than a stepping-stone series of dispersal events across pre-existing barriers. However, our study also highlights challenges of distinguishing dispersal-mediated speciation from static vicariance. Our results further demonstrate the substantial evolutionary timescale over which the diverse biota of the Andes was assembled.

The role of biogeographical barriers on the historical dynamics of passerine birds with a circum-Amazonian distribution.

Common distributional patterns have provided the foundations of our knowledge of Neotropical biogeography. A distinctive pattern is the "circum-Amazonian distribution", which surrounds Amazonia across the forested lowlands south and east of the basin, the Andean foothills, the Venezuelan Coastal Range, and the Tepuis. The underlying evolutionary and biogeographical mechanisms responsible for this widespread pattern of avian distribution have yet to be elucidated. Here, we test the effects of biogeographical barriers in four species in the passerine family Thamnophilidae by performing comparative demographic analyses of genome-scale data. Specifically, we used flanking regions of ultraconserved regions to estimate population historical parameters and genealogical trees and tested demographic models reflecting contrasting biogeographical scenarios explaining the circum-Amazonian distribution. We found that taxa with circum-Amazonian distribution have at least two main phylogeographical clusters: (1) Andes, often extending into Central America and the Tepuis; and (2) the remaining of their distribution. These clusters are connected through corridors along the Chaco-Cerrado and southeastern Amazonia, allowing gene flow between Andean and eastern South American populations. Demographic histories are consistent with Pleistocene climatic fluctuations having a strong influence on the diversification history of circum-Amazonian taxa, Refugia played a crucial role, enabling both phenotypic and genetic differentiation, yet maintaining substantial interconnectedness to keep considerable levels of gene flow during different dry/cool and warm/humid periods. Additionally, steep environmental gradients appear to play a critical role in maintaining both genetic and phenotypic structure.

Taxonomic revision of Myrmeciza (Aves: Passeriformes: Thamnophilidae) into 12 genera based on phylogenetic, morphological, behavioral, and ecological data.

A comprehensive molecular phylogeny of the family Thamnophilidae indicated that the genus Myrmeciza (Gray) is not monophyletic. Species currently assigned to the genus are found in three of the five tribes comprising the subfamily Thamnophilinae. Morphological, behavioral, and ecological character states of species within these tribes and their closest relatives were compared to establish generic limits. As a result of this analysis, species currently placed in Myrmeciza are assigned to Myrmeciza and eleven other genera, four of which (Myrmelastes Sclater, Myrmoderus Ridgway, Myrmophylax Todd, and Sipia Hellmayr) are resurrected, and seven of which (Ammonastes, A mpelornis, Aprositornis, Hafferia, Inundicola, Poliocrania, and Sciaphylax) are newly described.

DNA sequence data reveal a subfamily-level divergence within Thamnophilidae (Aves: Passeriformes).

The Thamnophilidae is a diverse radiation of insectivorous passerine birds that comprises nearly 220 species and is mostly restricted to the lowlands and lower montane forests of the Neotropics. Current classification within Thamnophilidae relies primarily on morphological variation, but recent incorporation of molecular and vocal data has promoted changes at various taxonomic levels. Here we demonstrate that the genus Terenura is polyphyletic because Terenura callinota, T. humeralis, T. spodioptila, and T. sharpei are phylogenetically distant from the type species of the genus, Terenura maculata. More importantly, the former four species are not particularly closely related to any other thamnophilids and represent a clade that is sister to all other members of the family. Because no genus name is available for this previously undetected lineage in the Thamnophilidae, we describe the genus Euchrepomis for callinota, humeralis, spodioptila, and sharpei, and erect the subfamily Euchrepomidinae. We discuss the taxonomic and evolutionary significance of this divergent lineage. This study highlights the importance of taxonomic coverage and the inclusion of type taxa to redefine classifications to reflect accurately evolutionary relationships.

Systematics of Thraupis (Aves, Passeriformes) reveals an extensive hybrid zone between T. episcopus (Blue-gray Tanager) and T. sayaca (Sayaca Tanager).

The Neotropical avian genus Thraupis (Passeriformes, Thraupidae) currently comprises seven species that are widespread and abundant throughout their ranges. However, no phylogenetic hypothesis with comprehensive intraspecific sampling is available for the group and, therefore, currently accepted species limits remain untested. We obtained sequence data for two mitochondrial (ND2, cyt-b) and three non-coding nuclear (TGFB2, MUSK, and ßF5) markers from 118 vouchered museum specimens. We conducted population structure and coalescent-based species-tree analyses using a molecular clock calibration. We integrated these results with morphometric and coloration analyses of 1,003 museum specimens to assess species limits within Thraupis. Our results confirm that Thraupis is a monophyletic group and support its origin in the late Miocene and subsequent diversification during the Pleistocene. However, we found conflicts with previous phylogenies. We recovered Thraupis glaucocolpa to be sister to all other species in the genus, and T. cyanoptera to the remaining five species. Our phylogenetic trees and population structure analyses uncovered phylogeographic structure within Thraupis episcopus that is congruent with geographic patterns of phenotypic variation and distributions of some named taxa. The first genetic and phenotypic cluster in T. episcopus occurs east of the Andes and is diagnosed by the white patch on the lesser and median wing coverts, whereas the second group has a blue patch on the wing and distributes to the west of Colombia's eastern Andes. Finally, we present evidence of hybridization and ongoing gene flow between several taxa at different taxonomic levels and discuss its taxonomic implications.

The evolution of sex similarities in social signals: Climatic seasonality is associated with lower sexual dimorphism and greater elaboration of female and male signals in antbirds (Thamnophilidae).

Selection on signals that mediate social competition varies with resource availability. Climate regulates resource availability, which may affect the strength of competition and selection on signals. Traditionally, this meant that more seasonal, colder, or dryer-overall harsher-environments should favor the elaboration of male signals under stronger male-male competition, increasing sexual dimorphism. However, females also use signals to compete; thus, harsher environments could strengthen competition and favor elaboration of signals in both sexes, decreasing sexual dimorphism. Alternatively, harsher environments could decrease sexual dimorphism due to scarcer resources to invest in signal elaboration in both sexes. We evaluated these contrasting hypotheses in antbirds, a family of Neotropical passerines that varies in female and male signals and occurs across diverse climatic regimes. We tested the association of sexual dimorphism of plumage coloration and songs with temperature, precipitation, and their seasonality. We found that greater seasonality is associated with lower sexual dimorphism in plumage coloration and greater elaboration of visual signals in both sexes, but not acoustic signals. Our results suggest that greater seasonality may be associated with convergent elaboration of female and male visual signals, highlighting the role of signals of both sexes in the evolution of sexual dimorphism.

Ecology and behavior predict an evolutionary trade-off between song complexity and elaborate plumages in antwrens (Aves, Thamnophilidae).

The environment can impose constraints on signal transmission properties such that signals should evolve in predictable directions (Sensory Drive Hypothesis). However, behavioral and ecological factors can limit investment in more than one sensory modality leading to a trade-off in use of different signals (Transfer Hypothesis). In birds, there is mixed evidence for both sensory drive and transfer hypothesis. Few studies have tested sensory drive while also evaluating the transfer hypothesis, limiting understanding of the relative roles of these processes in signal evolution. Here, we assessed both hypotheses using acoustic and visual signals in male and female antwrens (Thamnophilidae), a species-rich group that inhabits diverse environments and exhibits behaviors, such as mixed-species flocking, that could limit investment in different signal modalities. We uncovered significant effects of habitat (sensory drive) and mixed-species flocking behavior on both sensory modalities, and we revealed evolutionary trade-offs between song and plumage complexity, consistent with the transfer hypothesis. We also showed sex- and trait-specific responses in visual signals that suggest both natural and social selection play an important role in the evolution of sexual dimorphism. Altogether, these results support the idea that environmental (sensory drive) and behavioral pressures (social selection) shape signal evolution in antwrens.

The dynamics of introgression across an avian radiation.

Hybridization and resulting introgression can play both a destructive and a creative role in the evolution of diversity. Thus, characterizing when and where introgression is most likely to occur can help us understand the causes of diversification dynamics. Here, we examine the prevalence of and variation in introgression using phylogenomic data from a large (1300+ species), geographically widespread avian group, the suboscine birds. We first examine patterns of gene tree discordance across the geographic distribution of the entire clade. We then evaluate the signal of introgression in a subset of 206 species triads using Patterson's D-statistic and test for associations between introgression signal and evolutionary, geographic, and environmental variables. We find that gene tree discordance varies across lineages and geographic regions. The signal of introgression is highest in cases where species occur in close geographic proximity and in regions with more dynamic climates since the Pleistocene. Our results highlight the potential of phylogenomic datasets for examining broad patterns of hybridization and suggest that the degree of introgression between diverging lineages might be predictable based on the setting in which they occur.

A phylogenetic approach to disentangling the role of competition and habitat filtering in community assembly of Neotropical forest birds.

1. Methods that assess patterns of phylogenetic relatedness, as well as character distribution and evolution, allow one to infer the ecological processes involved in community assembly. Assuming niche conservatism, assemblages should shift from phylogenetic clustering to evenness with decreasing geographic scale because the relative importance of mechanisms that shape assemblages is hypothesized to be scale-dependent. Whereas habitat filtering is more likely to act at regional scales because of increased habitat heterogeneity that allows sorting of ecologically similar species in contrasting environments, competition is more likely to act at local scales because low habitat heterogeneity provides few opportunities for niche partitioning. 2. We used species lists to assess assemblage composition, data on ecologically-relevant traits, and a molecular phylogeny, to examine the phylogenetic structure of antbird (Thamnophilidae) assemblages at three different geographical scales: regional (ecoregions), intermediate (100-ha plots) and local (mixed-flocks). In addition, we used patterns of phylogenetic beta diversity and beta diversity to separate the factors that structure antbird assemblages at regional scales. 3. Contrary to previous findings, we found a shift from phylogenetic evenness to clustering with decreasing geographical scale. We argue that this does not reject the hypothesis that habitat filtering is the predominant force in regional community assembly, because analyses of trait evolution and structure indicated a lack of niche conservatism in antbirds. 4. In some cases, phylogenetic evenness at regional scales can be an effect of historical biogeographic processes instead of niche-based processes. However, regional patterns of beta diversity and phylogenetic beta diversity suggested that phylogenetic structure in our study cannot be explained by the history of speciation and dispersal of antbirds, further supporting the habitat-filtering hypothesis. 5. Our analyses suggested that competitive interactions might not play an important role locally, which would provide a plausible explanation for the high alpha diversity of antbirds in Amazonia. 6. Finally, we emphasize the importance of including trait information in studies of phylogenetic community structure to adequately assess the mechanisms that determine species co-existence.

The evolution of a tropical biodiversity hotspot.

The tropics are the source of most biodiversity yet inadequate sampling obscures answers to fundamental questions about how this diversity evolves. We leveraged samples assembled over decades of fieldwork to study diversification of the largest tropical bird radiation, the suboscine passerines. Our phylogeny, estimated using data from 2389 genomic regions in 1940 individuals of 1283 species, reveals that peak suboscine species diversity in the Neotropics is not associated with high recent speciation rates but rather with the gradual accumulation of species over time. Paradoxically, the highest speciation rates are in lineages from regions with low species diversity, which are generally cold, dry, unstable environments. Our results reveal a model in which species are forming faster in environmental extremes but have accumulated in moderate environments to form tropical biodiversity hotspots.