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.

A taxonomic review of the Golden-green Woodpecker, Piculus chrysochloros (Aves: Picidae) reveals the existence of six valid taxa.

Piculus chrysochloros (Vieillot 1818) is a species of woodpecker that ranges from Argentina to Panama, occurring in lowland forests as well as Cerrado, Caatinga and Chaco vegetation. Currently, nine subspecies are accepted, but no study has evaluated individual variation within populations, so the status of these taxa remains uncertain. Here we review the taxonomy and distribution of this species, based on morphological and morphometric data from 267 specimens deposited in ornithological collections. Our results suggest the existence of six unambiguous taxonomic units that can be treated as phylogenetic species: Piculus xanthochloros (Sclater & Salvin 1875), from northwestern South America; Piculus capistratus (Malherbe 1862), from northern Amazonia west to the Branco River; Piculus laemostictus Todd 1937, from southern Amazonia; Piculus chrysochloros (Vieillot 1818), from the Cerrado, Caatinga and Chaco; Piculus paraensis (Snethlage 1907) from the Belém Center of Endemism; and Piculus polyzonus (Valenciennes 1826) from the Atlantic Forest. Both Brazilian endemics (P. polyzonus and P. paraensis) are threatened due to habitat loss. In addition, we found one undescribed form from the Tapajós-Tocantins interfluve, now under study, that may prove to be a valid species once more specimens and other data become available.

Displaced clines in an avian hybrid zone (Thamnophilidae: Rhegmatorhina) within an Amazonian interfluve.

Secondary contact between species often results in the formation of a hybrid zone, with the eventual fates of the hybridizing species dependent on evolutionary and ecological forces. We examine this process in the Amazon Basin by conducting the first genomic and phenotypic characterization of the hybrid zone formed after secondary contact between two obligate army-ant-followers: the White-breasted Antbird (Rhegmatorhina hoffmannsi) and the Harlequin Antbird (Rhegmatorhina berlepschi). We found a major geographic displacement (∼120 km) between the mitochondrial and nuclear clines, and we explore potential hypotheses for the displacement, including sampling error, genetic drift, and asymmetric cytonuclear incompatibilities. We cannot exclude roles for sampling error and genetic drift in contributing to the discordance; however, the data suggest expansion and unidirectional introgression of hoffmannsi into the distribution of berlepschi.

River network rearrangements promote speciation in lowland Amazonian birds.

Large Amazonian rivers impede dispersal for many species, but lowland river networks frequently rearrange, thereby altering the location and effectiveness of river barriers through time. These rearrangements may promote biotic diversification by facilitating episodic allopatry and secondary contact among populations. We sequenced genome-wide markers to evaluate the histories of divergence and introgression in six Amazonian avian species complexes. We first tested the assumption that rivers are barriers for these taxa and found that even relatively small rivers facilitate divergence. We then tested whether species diverged with gene flow and recovered reticulate histories for all species, including one potential case of hybrid speciation. Our results support the hypothesis that river rearrangements promote speciation and reveal that many rainforest taxa are micro-endemic, unrecognized, and thus threatened with imminent extinction. We propose that Amazonian hyper-diversity originates partly from fine-scale barrier displacement processes-including river dynamics-which allow small populations to differentiate and disperse into secondary contact.

Plant invasion: Another threat to the São Paulo Marsh Antwren (Formicivora paludicola), a species on the verge of extinction.

During the past 100 years in densely populated south-eastern Brazil, wetlands have been severely transformed due to urbanization, agriculture and mining. The recently discovered São Paulo Marsh Antwren (Formicivora paludicola) is endemic to these wetlands, and is listed as "Critically Endangered" by the IUCN. The species is only found in an area of 1.42 km2, it has a sparse and fragmented distribution, low dispersal capacity, and has probably lost around 300 km2 of habitat in the past 100 years. Furthermore, very little is known about F. paludicola natural history, and so it is difficult to construct a robust conservation plan. Using Kernel home range estimations and the Adjusted-SD/Torus Shift test (a novel tool for animal-habitat association studies), we showed that the species avoids patches of the alien invasive ginger lily (Hedychium coronarium). Given the high density of their population (3.6 mature individuals/ha), F. paludicola could thrive in relatively small areas of suitable wetlands protected from human occupation and water contamination, however special attention should be paid to biological invasions, which may represent a serious threat to the remaining populations. Protecting a few small wetlands used by F. paludicola would be an important step towards general conservation and restoration of Atlantic Forest wetlands and its endemic endangered species.

A multiscale approach indicates a severe reduction in Atlantic Forest wetlands and highlights that São Paulo Marsh Antwren is on the brink of extinction.

Over the last 200 years the wetlands of the Upper Tietê and Upper Paraíba do Sul basins, in the southeastern Atlantic Forest, Brazil, have been almost-completely transformed by urbanization, agriculture and mining. Endemic to these river basins, the São Paulo Marsh Antwren (Formicivora paludicola) survived these impacts, but remained unknown to science until its discovery in 2005. Its population status was cause for immediate concern. In order to understand the factors imperiling the species, and provide guidelines for its conservation, we investigated both the species' distribution and the distribution of areas of suitable habitat using a multiscale approach encompassing species distribution modeling, fieldwork surveys and occupancy models. Of six species distribution models methods used (Generalized Linear Models, Generalized Additive Models, Multivariate Adaptive Regression Splines, Classification Tree Analysis, Artificial Neural Networks and Random Forest), Random Forest showed the best fit and was utilized to guide field validation. After surveying 59 sites, our results indicated that Formicivora paludicola occurred in only 13 sites, having narrow habitat specificity, and restricted habitat availability. Additionally, historic maps, distribution models and satellite imagery showed that human occupation has resulted in a loss of more than 346 km2 of suitable habitat for this species since the early twentieth century, so that it now only occupies a severely fragmented area (area of occupancy) of 1.42 km2, and it should be considered Critically Endangered according to IUCN criteria. Furthermore, averaged occupancy models showed that marshes with lower cattail (Typha dominguensis) densities have higher probabilities of being occupied. Thus, these areas should be prioritized in future conservation efforts to protect the species, and to restore a portion of Atlantic Forest wetlands, in times of unprecedented regional water supply problems.

Marshes as "Mountain Tops": Genetic Analyses of the Critically Endangered São Paulo Marsh Antwren (Aves: Thamnophilidae).

Small populations of endangered species can be impacted by genetic processes such as drift and inbreeding that reduce population viability. As such, conservation genetic analyses that assess population levels of genetic variation and levels of gene flow can provide important information for managing threatened species. The São Paulo Marsh Antwren (Formicivora paludicola) is a recently-described and critically endangered bird from São Paulo State (Brazil) whose total estimated population is around 250-300 individuals, distributed in only 15 isolated marshes around São Paulo metropolitan region. We used microsatellite DNA markers to estimate the population genetic characteristics of the three largest remaining populations of this species all within 60 km of each other. We detected a high and significant genetic structure between all populations (overall FST = 0.103) which is comparable to the highest levels of differentiation ever documented for birds, (e.g., endangered birds found in isolated populations on the tops of African mountains), but also evidence for first-generation immigrants, likely from small local unsampled populations. Effective population sizes were small (between 28.8-99.9 individuals) yet there are high levels of genetic variability within populations and no evidence for inbreeding. Conservation implications of this work are that the high levels of genetic structure suggests that translocations between populations need to be carefully considered in light of possible local adaptation and that remaining populations of these birds should be managed as conservation units that contain both main populations studied here but also small outlying populations which may be a source of immigrants.