Amazonian birds in more dynamic habitats have less population genetic structure and higher gene flow.

Understanding the factors that govern variation in genetic structure across species is key to the study of speciation and population genetics. Genetic structure has been linked to several aspects of life history, such as foraging strategy, habitat association, migration distance, and dispersal ability, all of which might influence dispersal and gene flow. Comparative studies of population genetic data from species with differing life histories provide opportunities to tease apart the role of dispersal in shaping gene flow and population genetic structure. Here, we examine population genetic data from sets of bird species specialized on a series of Amazonian habitat types hypothesized to filter for species with dramatically different dispersal abilities: stable upland forest, dynamic floodplain forest, and highly dynamic riverine islands. Using genome-wide markers, we show that habitat type has a significant effect on population genetic structure, with species in upland forest, floodplain forest, and riverine islands exhibiting progressively lower levels of structure. Although morphological traits used as proxies for individual-level dispersal ability did not explain this pattern, population genetic measures of gene flow are elevated in species from more dynamic riverine habitats. Our results suggest that the habitat in which a species occurs drives the degree of population genetic structuring via its impact on long-term fluctuations in levels of gene flow, with species in highly dynamic habitats having particularly elevated gene flow. These differences in genetic variation across taxa specialized in distinct habitats may lead to disparate responses to environmental change or habitat-specific diversification dynamics over evolutionary time scales.

A compreensão dos fatores que governam a variação da estrutura genética entre as espécies é fundamental para o estudo da especiação e da genética das populações. A estrutura genética tem sido ligada a vários aspectos da história da vida, tais como estratégia de forrageio, associação ao habitat, distância de migração e capacidade de dispersão, os quais poderiam influenciar a dispersão e o fluxo gênico. Estudos comparativos usando espécies que diferem nas suas histórias de vida oferecem uma oportunidade para desvendar o papel da dispersão no estabelecimento do fluxo gênico e da estrutura genética da população. Aqui examinamos dados genéticos populacionais de diversas espécies de aves com diferentes capacidades de dispersão especializadas em três habitats amazônicos, incluindo florestas de terra-firme, florestas de várzea e ilhas fluviais, cujos ambientes ripários são altamente dinâmicos. Utilizando dados genômicos que incluem milhares de loci, mostramos que o tipo de habitat tem um efeito significativo na estruturação genética das populações; espécies de florestas de terra-firme, florestas de várzea e ilhas fluviais exibem níveis de estruturação progressivamente menores. Embora os traços morfológicos frequentemente usados como indicadores da capacidade de dispersão a nível individual não expliquem este padrão, as medidas genéticas populacionais de fluxo gênico são altas em espécies associadas a habitats ribeirinhos mais dinâmicos. Nossos resultados sugerem que o habitat no qual uma espécie é encontrada determina o grau de estruturação genética da população através de seu impacto nas flutuações de longo prazo do fluxo gênico, com espécies em habitats altamente dinâmicos tendo um fluxo gênico particularmente alto. As diferenças na variação genética dos táxons especializados em diferentes habitats podem resultar em respostas díspares às mesmas mudanças ambientais, ou dinâmicas de diversificação específicas a um determinado habitat ao longo de escalas de tempo evolutivas.

Comprender los factores que rigen la variación de la estructura genética entre especies es clave para el estudio de la especiación y la genética de poblaciones. La estructura genética se ha relacionado con varios aspectos de la historia vital, como la estrategia de búsqueda de alimento, la asociación de hábitats, la distancia de migración y la capacidad de dispersión, factores todos ellos que podrían influir en la dispersión y el flujo genético. Los estudios comparativos de datos genéticos poblacionales de especies con historias vitales diferentes ofrecen la oportunidad de desentrañar el papel de la dispersión en la conformación del flujo genético y la estructura genética poblacional. En este trabajo examinamos los datos genéticos de poblaciones de especies de aves especializadas en una serie de hábitats amazónicos que, según la hipótesis, filtran especies con capacidades de dispersión radicalmente diferentes: bosques estables de tierras altas, bosques dinámicos de llanuras aluviales e islas fluviales altamente dinámicas. Utilizando marcadores genómicos, demostramos que el tipo de hábitat tiene un efecto significativo en la estructura genética de la población, y que las especies de los bosques de tierras altas, los bosques inundables y las islas fluviales presentan niveles de estructura progresivamente más bajos. Aunque los rasgos morfológicos utilizados como indicadores de la capacidad de dispersión individual no explican este patrón, las medidas genéticas poblacionales del flujo genético son más elevadas en las especies de hábitats fluviales más dinámicos. Nuestros resultados sugieren que el hábitat en el que se encuentra una especie determina el grado de estructuración genética de la población a través de su impacto en las fluctuaciones a largo plazo de los niveles de flujo genético, siendo las especies de hábitats muy dinámicos las que presentan un flujo genético particularmente elevado. Estas diferencias en la variación genética entre taxones especializados en hábitats distintos pueden dar lugar a respuestas dispares al cambio ambiental o a dinámicas de diversificación específicas del hbitat a lo largo de escalas temporales evolutivas.

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.

Moving beyond the riverine barrier vicariant paradigm.

One of the main goals of evolutionary biology is to understand the processes behind current patterns of biodiversity. Shared geographic distributions among unrelated species may result from a common history, providing a unique opportunity to assess the evolution of the landscape and the origins of biodiversity. Until recently, vicariance prevailed as the main evolutionary model to be tested, and the riverine barrier hypothesis the null model for taxa with river-bounded distributions. In recent years, however, multispecies comparative approaches have unveiled idiosyncratic scenarios among codistributed species, suggesting that rivers may or may not play a role in the speciation process. In a From the Cover article in this issue of Molecular Ecology, Kopuchian et al. (2020) explore predictions of the riverine barrier hypothesis in a major subtropical river system, evaluating the degree of mitochondrial and nuclear genomic differentiation in seven bird species with allegedly morphological differentiation across the Paraná-Paraguay river system. The authors show that in only one case, the genetic differentiation was concordant with the river. Interestingly, pairs presented disparate divergence times and/or distinct demographic histories. In most cases, putative contact zones broadly coincided with the transition of different ecoregions, such as the Espinal/Chaco ecological ecotone. These findings argue against the role of the Paraná-Paraguay river system as a major biogeographic barrier and highlight the need to explore the role of ecology in species diversification. Here, we feature different perspectives for studying the processes governing species divergence and suggest a basic protocol to advance the study of riverine barriers.

The pitfalls of biodiversity proxies: Differences in richness patterns of birds, trees and understudied diversity across Amazonia.

Most knowledge on biodiversity derives from the study of charismatic macro-organisms, such as birds and trees. However, the diversity of micro-organisms constitutes the majority of all life forms on Earth. Here, we ask if the patterns of richness inferred for macro-organisms are similar for micro-organisms. For this, we barcoded samples of soil, litter and insects from four localities on a west-to-east transect across Amazonia. We quantified richness as Operational Taxonomic Units (OTUs) in those samples using three molecular markers. We then compared OTU richness with species richness of two relatively well-studied organism groups in Amazonia: trees and birds. We find that OTU richness shows a declining west-to-east diversity gradient that is in agreement with the species richness patterns documented here and previously for birds and trees. These results suggest that most taxonomic groups respond to the same overall diversity gradients at large spatial scales. However, our results show a different pattern of richness in relation to habitat types, suggesting that the idiosyncrasies of each taxonomic group and peculiarities of the local environment frequently override large-scale diversity gradients. Our findings caution against using the diversity distribution of one taxonomic group as an indication of patterns of richness across all groups.

ATLANTIC BIRD TRAITS: a data set of bird morphological traits from the Atlantic forests of South America.

Scientists have long been trying to understand why the Neotropical region holds the highest diversity of birds on Earth. Recently, there has been increased interest in morphological variation between and within species, and in how climate, topography, and anthropogenic pressures may explain and affect phenotypic variation. Because morphological data are not always available for many species at the local or regional scale, we are limited in our understanding of intra- and interspecies spatial morphological variation. Here, we present the ATLANTIC BIRD TRAITS, a data set that includes measurements of up to 44 morphological traits in 67,197 bird records from 2,790 populations distributed throughout the Atlantic forests of South America. This data set comprises information, compiled over two centuries (1820-2018), for 711 bird species, which represent 80% of all known bird diversity in the Atlantic Forest. Among the most commonly reported traits are sex (n = 65,717), age (n = 63,852), body mass (n = 58,768), flight molt presence (n = 44,941), molt presence (n = 44,847), body molt presence (n = 44,606), tail length (n = 43,005), reproductive stage (n = 42,588), bill length (n = 37,409), body length (n = 28,394), right wing length (n = 21,950), tarsus length (n = 20,342), and wing length (n = 18,071). The most frequently recorded species are Chiroxiphia caudata (n = 1,837), Turdus albicollis (n = 1,658), Trichothraupis melanops (n = 1,468), Turdus leucomelas (n = 1,436), and Basileuterus culicivorus (n = 1,384). The species recorded in the greatest number of sampling localities are Basileuterus culicivorus (n = 243), Trichothraupis melanops (n = 242), Chiroxiphia caudata (n = 210), Platyrinchus mystaceus (n = 208), and Turdus rufiventris (n = 191). ATLANTIC BIRD TRAITS (ABT) is the most comprehensive data set on measurements of bird morphological traits found in a biodiversity hotspot; it provides data for basic and applied research at multiple scales, from individual to community, and from the local to the macroecological perspectives. No copyright or proprietary restrictions are associated with the use of this data set. Please cite this data paper when the data are used in publications or teaching and educational activities.

The dual role of Amazonian rivers in the generation and maintenance of avian diversity.

The Amazon River and its major tributaries delimit the distributions of hundreds of terrestrial taxa. It remains unclear whether river-bounded distributions and taxon replacements reflect the historical role of rivers in generating species diversity as vicariant forces, or are the result of their role as secondary barriers, maintaining current levels of species diversity by inhibiting gene flow and population introgression. We use a community-wide comparative phylogeographic and phylogenetic approach to address the roles that the Rio Negro and the Rio Branco play in the avian speciation process in the Guiana Shield. Examining 74 pairs of ecologically similar geographic replacements that turn over across the lower Negro, we found substantial variation in the levels of genetic divergence and the inferred timing of diversification among pairs, ranging from ~0.24 to over 8 million years (Ma ago). The breadth of this variation is inconsistent with a single, shared speciation event. Coalescent simulations also rejected a simultaneous divergence scenario for pairs divided by the Rio Branco but could not reject a single diversification pulse for a subset of 12 pairs of taxa divided by the upper Negro. These results are consistent with recent geomorphological hypotheses regarding the origins of these rivers. Phylogenetically, taxon pairs represent a blend of sister (~40%) and nonsister taxa (~60%), consistent with river-associated allopatric or peripatric speciation and secondary contact, respectively. Our data provide compelling evidence that species turnover across the Rio Negro basin encompasses a mixture of histories, supporting a dual role for Amazonian rivers in the generation and maintenance of biological diversity.

Ecological and phylogenetic predictors of mobbing behavior in a tropical dry forest.

Mobbing represents a well-known anti-predatory behavior, where potential prey display aggressively against a predator. Despite considerable experimental and descriptive work, no models predict species participation in mobbing assemblages. Here, we aimed to understand why some bird species engage in this behavior, while others do not, and what factors can be used to predict mobbing engagement within an avian community. We investigated whether certain functional traits, such as body size, foraging guild, foraging mode, and strata, as well species abundance and evolutionary relatedness, are important mobbing predictors. To address these goals, we simulated the presence of the Ferruginous Pygmy-Owl (Glaucidium brasilianum) by broadcasting its voice in 230 experiments conducted in 115 points, systematically distributed in a dry forest of northeastern Brazil. We compared these results to 162 avian surveys (point counts) conducted in the same area. Our avian surveys detected 108 bird species (local avian community), whereas our playback experiments attracted 72 species (mobbing assemblage). In general, small, canopy insectivorous or frugivorous birds dominated the mobs. The best mobbing predictors were body mass and guild, whereas species abundance, foraging mode, and strata were not retained in the best models. We found a strong phylogenetic component in body mass and mobbing propensity (almost 90% of the species and individuals participating in the mobs were passerines). At the community level, we found significant differences in the functional and phylogenetic structure of the mobbing assemblage in relation to the avian community. Our results suggest that mobbing behavior is tightly associated with predation risk and the capacity of individual species to find and detect predators, and that functional and phylogenetic features can predict species participation in this complex animal behavior.

ATLANTIC BIRDS: a data set of bird species from the Brazilian Atlantic Forest.

South America holds 30% of the world's avifauna, with the Atlantic Forest representing one of the richest regions of the Neotropics. Here we have compiled a data set on Brazilian Atlantic Forest bird occurrence (150,423) and abundance samples (N = 832 bird species; 33,119 bird individuals) using multiple methods, including qualitative surveys, mist nets, point counts, and line transects). We used four main sources of data: museum collections, on-line databases, literature sources, and unpublished reports. The data set comprises 4,122 localities and data from 1815 to 2017. Most studies were conducted in the Florestas de Interior (1,510 localities) and Serra do Mar (1,280 localities) biogeographic sub-regions. Considering the three main quantitative methods (mist net, point count, and line transect), we compiled abundance data for 745 species in 576 communities. In the data set, the most frequent species were Basileuterus culicivorus, Cyclaris gujanensis, and Conophaga lineata. There were 71 singletons, such as Lipaugus conditus and Calyptura cristata. We suggest that this small number of records reinforces the critical situation of these taxa in the Atlantic Forest. The information provided in this data set can be used for macroecological studies and to foster conservation strategies in this biodiversity hotspot. No copyright restrictions are associated with the data set. Please cite this Data Paper if data are used in publications and teaching events.