Taxonomic revision of the Scaled Antbird Drymophila squamata (Aves: Thamnophilidae) reveals a new and critically endangered taxon from northeastern Brazil.

The Scaled Antbird Drymophila squamata is a suboscine passerine endemic to the Atlantic Forest of eastern Brazil. Two subspecies, putatively diagnosed by the presence/absence of white spots on the crown, have traditionally been recognized: the nominate, ranging from Pernambuco to Bahia in northeastern Brazil, and D. squamata stictocorypha, from Minas Gerais to Santa Catarina in southeastern and southern Brazil. Here we combine morphological, acoustic, and genetic data to examine geographic variation in and revise the taxonomy of D. squamata. We show that there are two separately evolving population lineages in D. squamata, one south and the other north of the So Francisco River. The latter is unnamed and is thus described herein. We found that crown variation is not as geographically structured as previously thought, and thus we suggest that D. squamata stictocorypha is not a valid taxon. Finally, we also provide evidence of clinal variation in the species vocalizations and underscore the importance of broad geographic sampling when assessing species limits using vocalizations.

Evolutionary and Ecological Processes Underlying Geographic Variation in Innate Bird Songs.

AbstractEcological and evolutionary processes underlying spatial variation in signals involved in mate recognition and reproductive isolation are crucial to understanding the causes of population divergence and speciation. Here, to test hypotheses concerning the causes of song divergence, we examine how songs of two sister species of Atlantic Forest suboscine birds with innate songs, the Pyriglena fire-eye antbirds, vary across their ranges. Specifically, we evaluated the influence of isolation by distance and introgressive hybridization, as well as morphological and environmental variation, on geographic variation in male songs. Analyses based on 496 male vocalizations from 63 locations across a 2,200-km latitudinal transect revealed clinal changes in the structure of songs and showed that introgressive hybridization increases both the variability and the homogenization of songs in the contact zone between the two species. We also found that isolation by distance, morphological constraints, the environment, and genetic introgression independently predicted song variation across geographic space. Our study shows the importance of an integrative approach that investigates the roles of distinct ecological and evolutionary processes that influence acoustic signal evolution.

Rugged relief and climate promote isolation and divergence between two neotropical cold-associated birds.

The role of historical factors in establishing patterns of diversity in tropical mountains is of interest to understand the buildup of megadiverse biotas. In these regions, the historical processes of range fragmentation and contraction followed by dispersal are thought to be mediated by the interplay between rugged relief (complex topography) and climate fluctuations and likely explain most of the dynamics of diversification in plants and animals. Although empirical studies addressing the interaction between climate and topography have provided invaluable insights into population divergence and speciation patterns in tropical montane organisms, a more detailed and robust test of such processes in an explicit spatio-temporal framework is still lacking. Consequently, our ability to gain insights into historical range shifts over time and the genomic footprint left by them is limited. Here, we used niche modeling and subgenomic population-level datasets to explore the evolution of two species of warbling finches (genus Microspingus) disjunctly distributed across the Montane Atlantic Forest, a Neotropical region with complex geological and environmental histories. Population structure inferences suggest a scenario of three genetically differentiated populations, which are congruent with both geography and phenotypic variation. Demographic simulations support asynchronous isolation of these populations as recently as ∼40,000 years ago, relatively stable population sizes over recent time, and past gene flow subsequent to divergence. Throughout the last 800,000 years, niche models predicted extensive expansion into lowland areas with increasing overlap of species distributions during glacial periods, with prominent retractions and isolation into higher altitudes during interglacials, which are in line with signs of introgression of currently isolated populations. These results support a dual role of cyclical climatic changes: population divergence and persistence in mountain tops during warm periods followed by periods of expansion and admixture in lower elevations during cold periods. Our results underscore the role of the interplay between landscape and climate as an important mechanism in the evolution of the Neotropical montane biota.

Life history and ecology might explain incongruent population structure in two co-distributed montane bird species of the Atlantic Forest.

Comparative phylogeography is a powerful approach to investigate the role of historical and environmental processes in the evolution of biodiversity within a region. In this regard, comparative studies of species with similar habitat preferences are valuable to reduce the confounding influence of habitat association when interpreting phylogeographic patterns. In the Atlantic Forest of South America, phylogeographic studies of highland and lowland species have shown distinct population structure patterns so far, suggesting that such species have responded differently to Pleistocene glacial cycles. Herein, we performed a comparative analysis using molecular data and paleodistribution models of two Montane Atlantic Forest (MAF) co-distributed passerine birds with similar habitat requirements but with distinct life-history traits and ecologies: the frugivore lek-breeding Blue Manakin (Chiroxiphia caudata) and the insectivore and socially monogamous Drab-Breasted Bamboo Tyrant (Hemitriccus diops). We aimed to shed light on the role of contrasting life histories and ecologies onto the demography and population structure of MAF species. We sampled both species throughout most of their distribution range, sequenced a mitochondrial and a nuclear molecular marker, and used standard phylogeographic methods to investigate population structure and ecological niche modeling (ENM) to infer the species' paleodistributions. Our analyses recovered a phylogeographic break in H. diops in the region of the Doce River, but no genetic structure in C. caudata. We also found higher differentiation among subpopulations within each lineage of H. diops than among subpopulations of C. caudata. We suggest that these discrepancies in population structure might be due to distinct life-history traits and their impact on gene flow and generation time. For example, while H. diops is an insectivore species, C. caudata is a frugivore and the latter ecological aspect likely selects for a higher dispersion distance. Additionally, because C. caudata is a lek-breeding species, it has a longer generation time than H. diops. These traits could hinder genetic differentiation when populations become geographically isolated. Nonetheless, both species showed some common biological features, such as signatures of synchronous population expansion and larger distribution ranges during the Last Glacial Maximum, possibly due to similar cold tolerance.

Vicariance, dispersal, extinction and hybridization underlie the evolutionary history of Atlantic forest fire-eye antbirds (Aves: Thamnophilidae).

In order to gain insights into the biogeographic processes underlying biotic diversification in the Atlantic Forest (AF), we used a multi-locus approach to examine the evolutionary history of the White-shouldered Fire-eye (Pyriglena leucoptera) and the Fringe-backed Fire-eye (Pyriglena atra), two parapatric sister species endemic to the AF. We sequenced one mitochondrial, three Z chromosome-linked and three anonymous markers of 556 individuals from 66 localities. We recovered four lineages throughout the AF: P. atra and three populations within P. leucoptera. All populations diverged during the late Pleistocene and presented varying levels of admixture. One Z-linked locus showed the highest level of differentiation between the two species. On the other hand, a mitochondrial haplotype was shared extensively between them. Our data supported vicariance driving speciation along with extinction and dispersal as processes underlying intraspecific diversification. Furthermore, signatures of demographic expansion in most populations and areas of genetic admixture were recovered throughout the AF, suggesting that forest fragmentation was also important in differentiation. Genetic admixture areas are located between large rivers suggesting that AF rivers may diminish gene flow. Our results indicated a complex and dynamic biogeographic history of Pyriglena in the AF, with vicariance, extinction, dispersal and secondary contact followed by introgression likely influencing the current patterns of genetic distribution.

Historical climate changes and hybridization shaped the evolution of Atlantic Forest spinetails (Aves: Furnariidae).

Combining phylogeographic approaches and hybrid zone inference in a single framework is a robust way to depict respectively the biogeographic history of lineages and the evolutionary processes responsible for speciation. Here, we studied the spatiotemporal patterns of diversification and characterize the hybrid zone between two Atlantic Forest spinetails (Synallaxis ruficapilla and Synallaxis cinerea) using mitochondrial DNA and nuclear (autosomal and Z-linked) genes. We consistently recovered divergence between and within the two species during the late Pliocene and Pleistocene using an isolation with migration model. Also, our results indicate distinct levels of introgression among lineages. Ecological niche models and demographic inferences, used to infer range distributions throughout the late Quaternary, were not consistent with the hypothesis of a large river as a primary barrier responsible for the divergence of the two species. Instead, a scenario of isolation and divergence followed by geographic expansion and admixture as a consequence of Quaternary climatic oscillations was supported. Paleomodels also were not consistent with the idea that the hybrid zone originated in primary differentiation and favor a secondary contact scenario. Model fitting indicated that clines of different loci spanning the hybrid zone are coincident and concordant. The narrow cline for one Z-linked locus could be indicative of some form of post-zygotic selection hindering genetic homogenization between the two species.

Recent chapters of Neotropical history overlooked in phylogeography: Shallow divergence explains phenotype and genotype uncoupling in Antilophia manakins.

Establishing links between phenotypic and genotypic variation is a central goal of evolutionary biology, as they might provide important insights into evolutionary processes shaping genetic and species diversity in nature. One of the more intriguing possibilities is when no genetic divergence is found to be associated with conspicuous phenotypic divergence. In that case, speciation theory predicts that phenotypic divergence may still occur in the presence of significant gene flow-thereby resulting in little genomic divergence-when genetic loci underpinning phenotypes are under strong divergent selection. However, a finding of phenotypic distinctiveness with weak or no population genetic structure may simply result from low statistical power to detect shallow genetic divergences when small data sets are used. Here, we used a subgenomic data set of 2,386 ultraconserved elements to explore genomewide divergence between two species of Antilophia manakins, which are phenotypically distinct yet evidently lack strong genetic differentiation according to previous studies based on a limited number of loci. Our results revealed clear population structure that matches the two phenotypes, supporting the idea that smaller data sets lacked the power to detect this recent divergence event (likely <100 k ya). Indeed, we found little or no introgression between the species, as well as evidence of genomewide divergence. One implication of our study is that the Araripe plateau may be a hot spot of cryptic-diverging forest Cerrado populations. Besides their use in biogeography, subgenomic data sets may help redefine local conservation programmes by revealing cryptic population structure that may be key to population management.