Camila C. Ribas

A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years

Many hypotheses have been proposed to explain high species diversity in Amazonia, but few generalizations have emerged. In part, this has arisen from the scarcity of rigorous tests for mechanisms promoting speciation, and from major uncertainties about palaeogeographic events and their spatial and temporal associations with diversification. Here, we investigate the environmental history of Amazonia using a phylogenetic and biogeographic analysis of trumpeters (Aves: Psophia), which are represented by species in each of the vertebrate areas of endemism. Their relationships reveal an unforeseen ‘complete’ time-slice of Amazonian diversification over the past 3.0 Myr. We employ this temporally calibrated phylogeny to test competing palaeogeographic hypotheses. Our results are consistent with the establishment of the current Amazonian drainage system at approximately 3.0–2.0 Ma and predict the temporal pattern of major river formation over Plio-Pleistocene times. We propose a palaeobiogeographic model for the last 3.0 Myr of Amazonian history that has implications for understanding patterns of endemism, the temporal history of Amazonian diversification and mechanisms promoting speciation. The history of Psophia, in combination with new geological evidence, provides the strongest direct evidence supporting a role for river dynamics in Amazonian diversification, and the absence of such a role for glacial climate cycles and refugia.

The assembly of montane biotas: linking Andean tectonics and climatic oscillations to independent regimes of diversification in Pionus parrots

The mechanisms underlying the taxonomic assembly of montane biotas are still poorly understood. Most hypotheses have assumed that the diversification of montane biotas is loosely coupled to Earth history and have emphasized instead the importance of multiple long-distance dispersal events and biotic interactions, particularly competition, for structuring the taxonomic composition and distribution of montane biotic elements. Here we use phylogenetic and biogeographic analyses of species in the parrot genus Pionus to demonstrate that standing diversity within montane lineages is directly attributable to events of Earth history. Phylogenetic relationships confirm three independent biogeographic disjunctions between montane lineages, on one hand, and lowland dry-forest/wet-forest lineages on the other. Temporal estimates of lineage diversification are consistent with the interpretation that the three lineages were transported passively to high elevations by mountain building, and that subsequent diversification within the Andes was driven primarily by Pleistocene climatic oscillations and their large-scale effects on habitat change. These results support a mechanistic link between diversification and Earth history and have general implications for explaining high altitudinal disjuncts and the origin of montane biotas.

Molecular systematics in Aratinga parakeets: species limits and historical biogeography in the 'solstitialis' group, and the systematic position of Nandayus nenday.

The parrot genus Aratinga comprises 20 species that can be separated, based on morphological characters, in at least three distinct groups. We performed a phylogenetic analysis based on mtDNA sequences of individuals belonging to the solstitialis group with the objectives of: (1) assessing the genetic differences among individuals in order to clarify their specific status; (2) testing the monophyly of the group and establishing its phylogenetic position relative to other Aratinga species, (3) making inferences about temporal and geographical patterns of diversification in the Neotropics. As a result of the analysis, the three taxa belonging to the Aratinga solstitialis complex were found to be diagnosable phylogenetic species, the monotypic genus Nandayus was found to be included in the solstitialis group and the non-monophyly of the genus Aratinga was confirmed. Most of the speciation events occurred during the Pliocene and Pleistocene and may be related to habitat shifts associated to climate oscillation during these periods.

Spatial and temporal patterns of diversification on the Amazon: A test of the riverine hypothesis for all diurnal primates of Rio Negro and Rio Branco in Brazil.

The role of Amazonian rivers as drivers of speciation through vicariance remains controversial. Here we explore the riverine hypothesis by comparing spatial and temporal concordances in pattern of diversification for all diurnal primates of Rio Negro and its largest tributary, Rio Branco. We built a comprehensive comparative phylogenetic timetree to identify sister lineages of primates based on mitochondrial cytochrome b DNA sequences from 94 samples, including 19 of the 20 species of diurnal primates from our study region and 17 related taxa from elsewhere. Of the ten primate genera found in this region, three had populations on opposite banks of Rio Negro that formed reciprocally monophyletic clades, with roughly similar divergence times (Cebus: 1.85 Ma, HPD 95% 1.19-2.62; Callicebus: 0.83 Ma HPD 95% 0.36-1.32, Cacajao: 1.09 Ma, 95% HPD 0.58-1.77). This also coincided with time of divergence of several allopatric species of Amazonian birds separated by this river as reported by other authors. Our data offer support for the riverine hypothesis and for a Plio-Pleistocene time of origin for Amazonian drainage system. We showed that Rio Branco was an important geographical barrier, limiting the distribution of six primate genera: Cacajao, Callicebus, Cebus to the west and Pithecia, Saguinus, Sapajus to the east. The role of this river as a vicariant agent however, was less clear. For example, Chiropotes sagulata on the left bank of the Rio Branco formed a clade with C. chiropotes from the Amazonas Department of Venezuela, north of Rio Branco headwaters, with C. israelita on the right bank of the Rio Branco as the sister taxon to C. chiropotes+C. sagulata. Although we showed that the formation of the Rio Negro was important in driving diversification in some of our studied taxa, future studies including more extensive sampling of markers across the genome would help determine what processes contributed to the evolutionary history of the remaining primate genera.

MOLECULAR SYSTEMATICS AND PATTERNS OF DIVERSIFICATION IN PYRRHURA (PSITTACIDAE), WITH SPECIAL REFERENCE TO THE PICTA-LEUCOTIS COMPLEX

Abstract Parakeets in the genus Pyrrhura occur in Amazonia and in almost all other major Neotropical forests. Their uneven distribution (with some widespread and several geographically restricted endemic taxa) and complex patterns of plum- age variation have long generated a confused taxonomy. Several taxonomically difficult polytypic species are usually recognized. Here, we present a mitochondrial DNA (mtDNA) phylogenetic analysis of Pyrrhura, with emphasis on the especially problematic picta-leucotis complex, to provide a more robust basis for interpreting the systematics and historical biogeography of the group. Our main findings are that (1) Pyrrhura can be divided into three main evolutionary lineages, one comprising P. cruentata, an Atlantic Forest endemic, the second comprising the picta-leucotis complex, and the third comprising the remaining species; (2) the traditionally recognized species P. picta and P. leucotis are not monophyletic; and (3) most of the species recognized by Joseph (2000, 2002) are diagnosable as independent evolutionary units, with the exception of the following species pairs: P. snethlageae and P. amazonum, P. leucotis and P. griseipectus, and P. roseifrons and P. peruviana. Other than P. cruentata, the two clades that constitute Pyrrhura appear to have radiated and evolved their present mtDNA diversity over short periods during the Plio-Pleistocene. Sistemática Molecular y Patrones de Diversificación en Pyrrhura (Psittacidae), con Énfasis en el Complejo Picta-Leucotis

The Andean Hapalopsittaca parrots (Psittacidae, Aves): an example of montane-tropical lowland vicariance

Quintero, E., Ribas, C. C. & Cracraft, J. (2012). The Andean Hapalopsittaca parrots (Psittacidae, Aves): an example of montane‐tropical lowland vicariance. —Zoologica Scripta, 42, 28–43.

What is the avifauna of Amazonian white-sand vegetation?

White-sand vegetation (WSV) is a rare vegetation type in the Amazon basin that grows in nutrient impoverished sandy soils that occur as patches of variable size. Associated with this vegetation is bird assemblage that has not yet been fully characterized. Based on published species inventories and our own field data we compile a checklist of bird species recorded in WSV. In addition, we compared the avifauna of WSV with that found in savanna patches, another type of Amazonian open vegetation. WSV hosted a distinctive avifauna including endemic and threatened species. The number of bird species was lower in WSV compared to nearby terra firme forests, seasonally flooded forests and Amazonian savannas. Despite its low diversity, the avifauna of WSV has a distinctive species composition and makes a significant contribution to Amazonian beta diversity. At least 35 bird species can be considered as indicator species for this environment. Previously identified areas of endemism within the Amazon basin house at least one WSV indicator bird including cases of congeneric species with allopatric distributions. Seven of the WSV indicator species (20% of this avifauna) are in an IUCN threatened category, with one species Polioptila clementsi considered Critically Endangered. Their isolated distribution, small area occupied, and fragility to human-driven disturbances makes WSV one of the most threatened vegetation types in the Amazon basin. The study of WSV avifauna contributes to a better understanding of mechanisms that generate and maintain species diversity as well as of the environmental history of the most biologically diverse biome of the planet.

Habitat Association Predicts Genetic Diversity and Population Divergence in Amazonian Birds

The ecological traits of organisms may predict their genetic diversity and population genetic structure and mediate the action of evolutionary processes important for speciation and adaptation. Making these ecological-evolutionary links is difficult because it requires comparable genetic estimates from many species with differing ecologies. In Amazonian birds, habitat association is an important component of ecological diversity. Here, we examine the link between habitat association and genetic parameters using 20 pairs of closely related Amazonian bird species in which one member of the pair occurs primarily in forest edge and floodplains and the other occurs in upland forest interior. We use standardized geographic sampling and data from 2,416 genomic markers to estimate genetic diversity, population genetic structure, and statistics reflecting demographic and evolutionary processes. We find that species of upland forest have greater genetic diversity and divergence across the landscape as well as signatures of older histories and less gene flow than floodplain species. Our results reveal that species ecology in the form of habitat association is an important predictor of genetic diversity and population divergence and suggest that differences in diversity between floodplain and upland avifaunas in the Amazon may be driven by differences in the demographic and evolutionary processes at work in the two habitats.

Phenotypic and Genetic Structure Support Gene Flow Generating Gene Tree Discordances in an Amazonian Floodplain Endemic Species

Abstract Before populations become independent evolutionary lineages, the effects of micro evolutionary processes tend to generate complex scenarios of diversification that may affect phylogenetic reconstruction. Not accounting for gene flow in species tree estimates can directly impact topology, effective population sizes and branch lengths, and the resulting estimation errors are still poorly understood in wild populations. In this study, we used an integrative approach, including sequence capture of ultra‐conserved elements (UCEs), mtDNA Sanger sequencing and morphological data to investigate species limits and phylogenetic relationships in face of gene flow in an Amazonian endemic species (Myrmoborus lugubris: Aves). We used commonly implemented species tree and model‐based approaches to understand the potential effects of gene flow in phylogenetic reconstructions. The genetic structure observed was congruent with the four recognized subspecies of M. lugubris. Morphological and UCEs data supported the presence of a wide hybrid zone between M. l. femininus from the Madeira river and M. l. lugubris from the Middle and lower Amazon river, which were recovered as sister taxa by species tree methods. When fitting gene flow into simulated demographic models with different topologies, the best‐fit model indicated these two taxa as non‐sister lineages, a finding that is in agreement with the results of mitochondrial and morphological analyses. Our results demonstrated that failing to account for gene flow when estimating phylogenies at shallow divergence levels can generate topological uncertainty, which can nevertheless be statistically well supported, and that model testing approaches using simulated data can be useful tools to test alternative phylogenetic hypotheses.

Systematics and biogeography of the Automolus infuscatus complex (Aves; Furnariidae): Cryptic diversity reveals western Amazonia as the origin of a transcontinental radiation

A revision of the avian Neotropical genus Automolus and the Furnariidae family points to the paraphyly of A. infuscatus and reveals a species complex comprising A. infuscatus, A. ochrolaemus, A. paraensis, A. leucophthalmus, A. lammi and A. subulatus, the latter historically classified in the genus Hyloctistes. Detailed knowledge of the taxonomy, geographic distribution, phylogenetic relationship and divergence times of a taxon allows exploration of its evolutionary history and the testing of different scenarios of diversification. In this context, we studied the A. infuscatus complex using molecular data in order to unveil its cryptic diversity and reveal its evolutionary history. For that we sequenced two mitochondrial (ND2 and cytb) and three nuclear markers (G3PDH, ACO, Fib7) for 302 individuals belonging to all species in the complex and most described subspecies. Our analysis supports the paraphyly of A. infuscatus, indicating the existence of at least two distinct clades not closely related. The remaining species were all recovered as monophyletic. Notwithstanding, a well-structured intraspecific diversity was found with 19 lineages suggesting substantial cryptic diversity within the described species. A. subulatus was recovered within the complex, corroborating its position inside the genus. In spite of the high congruence between distributions of different lineages, with several sister lineages currently separated by the same barriers, the temporal incongruence between divergences over the same barriers reveals a complex evolutionary history. While older events might be related to the emergence of barriers such as the Andes and major Amazonian rivers, younger events suggest dispersal after the consolidation of those barriers. Our analysis suggests that the complex had its origin around 6million years (Ma) and inhabited Western Amazonia in Late Miocene-Early Pliocene. Considering the riparian habit of species in its sister clade, the rise and early diversifications of the complex may be related to the establishment of terra firme forests as it changed from a floodplain to a fluvial system. The late Amazonian colonization by A. subulatus and A. ochrolaemus lineages may have been hampered by the previous existence of well established A. infuscatus lineages in the region.