Alexandre Aleixo

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 drivers of tropical speciation

Since the recognition that allopatric speciation can be induced by large-scale reconfigurations of the landscape that isolate formerly continuous populations, such as the separation of continents by plate tectonics, the uplift of mountains or the formation of large rivers, landscape change has been viewed as a primary driver of biological diversification. This process is referred to in biogeography as vicariance. In the most species-rich region of the world, the Neotropics, the sundering of populations associated with the Andean uplift is ascribed this principal role in speciation. An alternative model posits that rather than being directly linked to landscape change, allopatric speciation is initiated to a greater extent by dispersal events, with the principal drivers of speciation being organism-specific abilities to persist and disperse in the landscape. Landscape change is not a necessity for speciation in this model. Here we show that spatial and temporal patterns of genetic differentiation in Neotropical birds are highly discordant across lineages and are not reconcilable with a model linking speciation solely to landscape change. Instead, the strongest predictors of speciation are the amount of time a lineage has persisted in the landscape and the ability of birds to move through the landscape matrix. These results, augmented by the observation that most species-level diversity originated after episodes of major Andean uplift in the Neogene period, suggest that dispersal and differentiation on a matrix previously shaped by large-scale landscape events was a major driver of avian speciation in lowland Neotropical rainforests.

LINEAGE DIVERSIFICATION AND MORPHOLOGICAL EVOLUTION IN A LARGE-SCALE CONTINENTAL RADIATION: THE NEOTROPICAL OVENBIRDS AND WOODCREEPERS (AVES: FURNARIIDAE)

Patterns of diversification in species‐rich clades provide insight into the processes that generate biological diversity. We tested different models of lineage and phenotypic diversification in an exceptional continental radiation, the ovenbird family Furnariidae, using the most complete species‐level phylogenetic hypothesis produced to date for a major avian clade (97% of 293 species). We found that the Furnariidae exhibit nearly constant rates of lineage accumulation but show evidence of constrained morphological evolution. This pattern of sustained high rates of speciation despite limitations on phenotypic evolution contrasts with the results of most previous studies of evolutionary radiations, which have found a pattern of decelerating diversity‐dependent lineage accumulation coupled with decelerating or constrained phenotypic evolution. Our results suggest that lineage accumulation in tropical continental radiations may not be as limited by ecological opportunities as in temperate or island radiations. More studies examining patterns of both lineage and phenotypic diversification are needed to understand the often complex tempo and mode of evolutionary radiations on continents.

HISTORICAL DIVERSIFICATION OF A TERRA-FIRME FOREST BIRD SUPERSPECIES: A PHYLOGEOGRAPHIC PERSPECTIVE ON THE ROLE OF DIFFERENT HYPOTHESES OF AMAZONIAN DIVERSIFICATION

Abstract Among those few hypotheses of Amazonian diversification amenable to falsification by phylogenetic and population genetics methods, three can be singled out because of their general application to vertebrates: the riverine barrier, the refuge, and the Miocene marine incursion hypotheses. I used phylogenetic and population genetics methods to reconstruct the diversification history of the upland (terra‐firme) forest superspecies Xiphorhynchus spixii/elegans (Aves: Dendrocolaptidae) in Amazonia, and to evaluate predictions of the riverine barrier, refuge, and Miocene marine incursion hypotheses. Phylogeographic and population genetics analyses of the X. spixiilelegans superspecies indicated that the main prediction of the riverine barrier hypothesis (that sister lineages occur across major rivers) hold only for populations separated by “clear‐water” rivers located on the Brazilian shield, in central and eastern Amazonia; in contrast, “white‐water” rivers located in western Amazonia did not represent areas of primary divergence for populations of this superspecies. The main prediction derived from the refuge hypothesis (that populations of the X. spixiilelegans superspecies would show signs of past population bottlenecks and recent demographic expansions) was supported only for populations found in western Amazonia, where paleoecological data have failed to support past rainforest fragmentation and expansion of open vegetation types; conversely, populations from the eastern and central parts of Amazonia, where paleoecological data are consistent with an historical interplay between rainforest and open vegetation types, did not show population genetics attributes expected under the refuge hypothesis. Phylogeographic and population genetics data were consistent with the prediction made by the Miocene marine incursion hypothesis that populations of the X. spixii/elegans superspecies found on the Brazilian shield were older than populations from other parts of Amazonia. In contrast, the phylogeny obtained for lineages of this superspecies falsified the predicted monophyly of Brazilian shield populations, as postulated by the Miocene marine incursion hypothesis. In general, important predictions of both riverine barrier and Miocene marine incursion hypotheses were supported, indicating that they are not mutually exclusive; in fact, the data presented herein suggest that an interaction among geology, sea level changes, and hydrography created opportunities for cladogenesis in the X. spixii/elegans superspecies at different temporal and geographical scales.

Composition and dynamics of the bird community of mata de Santa Genebra, Campinas, São Paulo, Brazil

A quali-quantitative survey of avifauna was earried out at the Santa Genebra forest reserve (MSG) in order to evaluate the current state of conservation of this important conservation area in the interior of Sao Paulo Stale. The qualilative survey recorded 134 species and the quantitativo survey through unlimited distance point counts recorded the abundance of 97 species. The low number of species recorded in both surveys was due to the small size (251 ha) and the high degree of isolation of the MSG. These factors plus the extensivo degradation of the forest cover prevent recolonization of extinct species and allow the expansion of some species tolerant to disturbance. The quantitative survey showed some species with an unusually high abundance index. The abundance of most species at MSG is higher whon compared with other areas of similar vegetation which are not fragmented and isolated, There was no striking seasonal variation in the number of birds recorded. These caracteristics could be interpreted as resulting from the density compensation phenomenon. The structure of the bird community of MSG resembles that from an island with low number of species but overall density similar to that of the mainland, leading to a higher density per species. The process responsible for these patterns seems to be related to the habitat appropriateness, mainly because the MSG is completely isolated from other forest arcas.

A social and ecological assessment of tropical land uses at multiple scales: the Sustainable Amazon Network

Science has a critical role to play in guiding more sustainable development trajectories. Here, we present the Sustainable Amazon Network (Rede Amazônia Sustentável, RAS): a multidisciplinary research initiative involving more than 30 partner organizations working to assess both social and ecological dimensions of land-use sustainability in eastern Brazilian Amazonia. The research approach adopted by RAS offers three advantages for addressing land-use sustainability problems: (i) the collection of synchronized and co-located ecological and socioeconomic data across broad gradients of past and present human use; (ii) a nested sampling design to aid comparison of ecological and socioeconomic conditions associated with different land uses across local, landscape and regional scales; and (iii) a strong engagement with a wide variety of actors and non-research institutions. Here, we elaborate on these key features, and identify the ways in which RAS can help in highlighting those problems in most urgent need of attention, and in guiding improvements in land-use sustainability in Amazonia and elsewhere in the tropics. We also discuss some of the practical lessons, limitations and realities faced during the development of the RAS initiative so far.

Avian gene trees, landscape evolution, and geology: towards a modern synthesis of Amazonian historical biogeography?

Recent studies have improved our understanding of Amazonian geological history during the late Tertiary and Quaternary, two periods regarded as critical for the recent diversification of the Amazonian avifauna. The notion that geologically older and more stable areas of Amazonia (such as the Brazilian and Guianan shields) functioned as “species-pumps”, whereas geologically more dynamic areas (such as the western Amazonian lowlands) mostly “captured” part of the diversity generated nearby, was supported by a recent phylogeographic study focusing on a species complex of the genus Xiphorhynchus (Dendrocolaptidae). Here, we review several additional molecular datasets to assess whether this historical scenario can be extended to other lineages of Amazonian birds as well. The datasets reviewed indicated that most lineages of upland forest species found nowadays in western Amazonia are associated with more basal lineages from the Brazilian shield, Guianan shield, and the Andes, indicating a more recent history in this geologically dynamic region. Conversely, lineages associated with seasonally flooded forests seem to have an ancient history in western Amazonia, apparently expanding over the geologically more stable areas only recently. Most sister taxa of the lineages reviewed exhibited levels of pairwise sequence divergence consistent with splitting events dating back to a time frame stretching from the late Miocene to the early Pleistocene, a period when significant physiographic and landscape changes took place in Amazonia. When interpreted together, all the studies reviewed provide evidence that geology and landscape evolution are tightly linked with the timing and mode of differentiation of Amazonian birds.

Temporal and spatial diversification of Pteroglossus araçaris (AVES: Ramphastidae) in the neotropics: Constant rate of diversification does not support an increase in radiation during the Pleistocene

We use the small-bodied toucan genus Pteroglossus to test hypotheses about diversification in the lowland Neotropics. We sequenced three mitochondrial genes and one nuclear intron from all Pteroglossus species and used these data to reconstruct phylogenetic trees based on maximum parsimony, maximum likelihood, and Bayesian analyses. These phylogenetic trees were used to make inferences regarding both the pattern and timing of diversification for the group. We used the uplift of the Talamanca highlands of Costa Rica and western Panama as a geologic calibration for estimating divergence times on the Pteroglossus tree and compared these results with a standard molecular clock calibration. Then, we used likelihood methods to model the rate of diversification. Based on our analyses, the onset of the Pteroglossus radiation predates the Pleistocene, which has been predicted to have played a pivotal role in diversification in the Amazon rainforest biota. We found a constant rate of diversification in Pteroglossus evolutionary history, and thus no support that events during the Pleistocene caused an increase in diversification. We compare our data to other avian phylogenies to better understand major biogeographic events in the Neotropics. These comparisons support recurring forest connections between the Amazonian and Atlantic forests, and the splitting of cis/trans Andean species after the final uplift of the Andes. At the subspecies level, there is evidence for reciprocal monophyly and groups are often separated by major rivers, demonstrating the important role of rivers in causing or maintaining divergence. Because some of the results presented here conflict with current taxonomy of Pteroglossus, new taxonomic arrangements are suggested.

Multilocus phylogeography of the Wedge-billed Woodcreeper Glyphorynchus spirurus (Aves, Furnariidae) in lowland Amazonia: widespread cryptic diversity and paraphyly reveal a complex diversification pattern.

Amazonian rivers function as important barriers to dispersal of Amazonian birds. Studying population genetics of lineages separated by rivers may help us to uncover the dynamics of biological diversification in the Amazon. We reconstructed the phylogeography of the Wedge-billed Woodcreeper, Glyphorynchus spirurus (Furnariidae) in the Amazon basin. Sampling included 134 individuals from 63 sites distributed in eight Amazonian areas of endemism separated by major Amazonian rivers. Nucleotide sequences were generated for five genes: two mtDNA genes (1047 bp for cyt b and 1002 bp for ND2) and three nuclear genes (647 bp from the sex-linked gene ACO, 319 bp from the intron of G3PDH, and 619 bp from intron 2 of MYO). In addition, 37 individuals were randomly selected from the Rondônia and Inambari areas of endemism for genomic fingerprinting, using five ISSR primers. Our results reveal allopatric and well-supported lineages within G. spirurus with high levels of genetic differentiation (p-distances 0.9-6.3%) across opposite banks of major Amazonian rivers. The multilocus phylogenetic reconstructions obtained reveal several incongruences with current subspecies taxonomy. Within currently recognized subspecies, we found high levels of both paraphyly and genetic differentiation, indicating deep divergences and strong isolation consistent with species-level differences. ISSR fingerprinting supports the existence of genetically differentiated populations on opposite sides of the Madeira River. Molecular dating suggests an initial vicariation event isolating populations from the Guiana center of endemism during the Late Miocene/Early Pliocene, while more recent events subdivided Brazilian Shield populations during the Lower Pleistocene.

CORRELATED EVOLUTION OF BEAK MORPHOLOGY AND SONG IN THE NEOTROPICAL WOODCREEPER RADIATION

Mating signals may diversify as a byproduct of morphological adaptation to different foraging niches, potentially driving speciation. Although many studies have focused on the direct influence of ecological and sexual selection on signal divergence, the role of indirect mechanisms remains poorly understood. Using phenotypic and molecular datasets, we explored the interplay between morphological and vocal evolution in an avian radiation characterized by dramatic beak variation, the Neotropical woodcreepers (Dendrocolaptinae). We found evidence of a trade‐off between the rate of repetition of song syllables and frequency bandwidth: slow paced songs had either narrow or wide frequency bandwidths, and bandwidth decreased as song pace increased. This bounded phenotypic space for song structure supports the hypothesis that passerine birds face a motor constraint during song production. Diversification of acoustic characters within this bounded space was correlated with diversification of beak morphology. In particular, species with larger beaks produced slower songs with narrower frequency bandwidths, suggesting that ecological selection on beak morphology influences the diversification of woodcreeper songs. Because songs in turn mediate mate choice and species recognition in birds, these results indicate a broader role for ecology in avian diversification.