The role of biogeographical barriers on the historical dynamics of passerine birds with a circum-Amazonian distribution.

Common distributional patterns have provided the foundations of our knowledge of Neotropical biogeography. A distinctive pattern is the "circum-Amazonian distribution", which surrounds Amazonia across the forested lowlands south and east of the basin, the Andean foothills, the Venezuelan Coastal Range, and the Tepuis. The underlying evolutionary and biogeographical mechanisms responsible for this widespread pattern of avian distribution have yet to be elucidated. Here, we test the effects of biogeographical barriers in four species in the passerine family Thamnophilidae by performing comparative demographic analyses of genome-scale data. Specifically, we used flanking regions of ultraconserved regions to estimate population historical parameters and genealogical trees and tested demographic models reflecting contrasting biogeographical scenarios explaining the circum-Amazonian distribution. We found that taxa with circum-Amazonian distribution have at least two main phylogeographical clusters: (1) Andes, often extending into Central America and the Tepuis; and (2) the remaining of their distribution. These clusters are connected through corridors along the Chaco-Cerrado and southeastern Amazonia, allowing gene flow between Andean and eastern South American populations. Demographic histories are consistent with Pleistocene climatic fluctuations having a strong influence on the diversification history of circum-Amazonian taxa, Refugia played a crucial role, enabling both phenotypic and genetic differentiation, yet maintaining substantial interconnectedness to keep considerable levels of gene flow during different dry/cool and warm/humid periods. Additionally, steep environmental gradients appear to play a critical role in maintaining both genetic and phenotypic structure.

Evidence of past forest fragmentation in the Congo Basin from the phylogeography of a shade-tolerant tree with limited seed dispersal: Scorodophloeus zenkeri (Fabaceae, Detarioideae).

BACKGROUND: Comparative phylogeographic studies on rainforest species that are widespread in Central Africa often reveal genetic discontinuities within and between biogeographic regions, indicating (historical) barriers to gene flow, possibly due to repeated and/or long-lasting population fragmentation during glacial periods according to the forest refuge hypothesis. The impact of forest fragmentation seems to be modulated by the ecological amplitude and dispersal capacities of each species, resulting in different demographic histories. Moreover, while multiple studies investigated the western part of Central Africa (Lower Guinea), few have sufficiently sampled the heart of the Congo Basin (Congolia). In this study, we look for genetic discontinuities between populations of the widespread tropical tree Scorodophloeus zenkeri Harms (Fabaceae, Detarioideae) in Central Africa. Additionally, we characterize genetic diversity, selfing rate and fine-scale spatial genetic structure within populations to estimate the gene dispersal capacity of the species. RESULTS: Clear intraspecific genetic discontinuities occur throughout the species' distribution range, with two genetic clusters in Congolia and four in Lower Guinea, and highest differentiation occurring between these bioregions. Genetic diversity is higher in Lower Guinea than Congolia. A spatial genetic structure characteristic of isolation by distance occurs within the genetic clusters. This allowed us to estimate gene dispersal distances (σg) for this outcrossing species with ballistic seed dispersal, which range between 100 and 250 m in areas where S. zenkeri occurs in high densities, and are in the low range of σg values compared to other tropical trees. Gene dispersal distances are larger in low density populations, probably due to extensive pollen dispersal capacity. CONCLUSIONS: Fragmentation of S. zenkeri populations seems to have occurred not only in Lower Guinea but also in the Congo Basin, though not necessarily according to previously postulated forest refuge areas. The lower genetic diversity in Congolia compared to Lower Guinea parallels the known gradient of species diversity, possibly reflecting a stronger impact of past climate changes on the forest cover in Congolia. Despite its bisexual flowers, S. zenkeri appears to be mostly outcrossing. The limited dispersal observed in this species implies that genetic discontinuities resulting from past forest fragmentation can persist for a long time before being erased by gene flow.

Comparative phylogeographic and demographic analyses reveal a congruent pattern of sister relationships between bird populations of the northern and south-central Atlantic Forest.

The Pernambuco Center of Endemism (PCE) is the northernmost strip of the Atlantic Forest (AF). Biogeographic affinities among avifaunas in the PCE, the southern-central Atlantic Forest (SCAF), and Amazonia (AM) have not been studied comprehensively, and current patterns of genetic diversity in the PCE remain unclear. The interplay between species' ecological attributes and historical processes, such as Pleistocene climate fluctuations or the appearance of rivers, may have affected population genetic structures in the PCE. Moreover, the role of past connections between the PCE and AM and the elevational distribution of species in assembling the PCE avifauna remain untested. Here, we investigated the biogeographic history of seven taxa endemic to the PCE within a comparative phylogeographic framework based on a mean of 3,618 independent single nucleotide polymorphisms (SNPs) extracted from flanking regions of ultraconserved elements (UCEs) and one mitochondrial gene. We found that PCE populations were more closely related to SCAF populations than they were to those in AM, regardless of their elevational range, with divergence times placed during the Mid-Pleistocene. These splits were consistent with a pattern of allopatric divergence with gene flow until the upper Pleistocene and no signal of rapid changes in population sizes. Our results support the existence of a Pleistocene refugium driving current genetic diversity in the PCE, thereby rejecting the role of the São Francisco River as a primary barrier for population divergence. Additionally, we found that connections with Amazonia also played a significant role in assembling the PCE avifauna through subsequent migration events.

Phylogeography of the Variable Antshrike (Thamnophilus caerulescens), a South American passerine distributed along multiple environmental gradients.

The Neotropics show a wealth of distributional patterns shared by many co-distributed species. A distinctive pattern is the so-called "circum-Amazonian distribution," which is observed in species that do not occur in Amazonia but rather along a belt of forested habitats spanning south and east of Amazonia, the Andean foothills, and often into the Venezuelan Coastal Range and the Tepuis. Although this pattern is widespread across animals and plants, its underlying biogeographic mechanisms remain poorly understood. The Variable Antshrike (Thamnophilus caerulescens) is a sexually dimorphic suboscine passerine that exhibits extreme plumage variation and occurs along the southern portion of the circum-Amazonian belt. We describe broad-scale phylogeographic patterns of T. caerulescens and assess its demographic history using DNA sequences from the mitochondrion and ultraconserved elements (UCEs). We identified three genomic clusters: a) northern Atlantic Forest; b) southeastern Cerrado and central-southern Atlantic Forest, and c) Chaco and Andes. Our results were consistent with Pleistocene divergence followed by gene flow, mainly between the latter two clusters. There were no genetic signatures of rapid population expansions or bottlenecks. The population from the northern Atlantic Forest was the most genetically divergent group within the species. The demographic history of T. caerulescens was probably affected by series of humid and dry periods throughout the Quaternary that generated subtle population expansions and contractions allowing the intermittent connection of habitats along the circum-Amazonian belt. Recognizing the dynamic history of climate-mediated forest expansions, contractions, and connections during the South American Pleistocene is central toward a mechanistic understanding of circum-Amazonian distributions.

Rain forest shifts through time and riverine barriers shaped the diversification of South American terrestrial pit vipers (Bothrops jararacussu species group)

Aim To investigate (a) historical biogeographical connections and species interchange among rain forest habitats and (b) the role of riverine barriers on population divergence and speciation in the Neotropical region. Location Amazonia and Atlantic Forest in South America. Taxon Bothrops jararacussu species group (Serpentes: Viperidae). Methods We inferred phylogenetic relationships within Bothrops with an emphasis on the jararacussu species group under a Bayesian framework based on six molecular loci. We also used genetic coalescent simulations and approximate Bayesian computation to infer historical demography within the jararacussu group based on tests of alternative scenarios. Results We found the jararacussu species group to be monophyletic. The Atlantic Forest species B. pirajai and B. muriciensis were inferred nested within this group, closely related to B. jararacussu, confirming that Atlantic Forest species form a clade. The historical demographic analyses support vicariant separation between populations of B. brazili north and south of the Amazon River during the Miocene–Pliocene border, as well as colonization of the Atlantic Forest by a northern Amazonian ancestor in the Pleistocene. Main Conclusion The evolutionary history of the jararacussu species group sheds light on the dynamism of Neotropical rain forests over time, with at least one event of forest expansion leading to faunal interchange between Amazonian and Atlantic forests in the Pleistocene. Moreover, tests of alternative demographic scenarios suggest that the populations of B. brazili from north and south of the Amazon River originated from a vicariant event during the Miocene–Pliocene border, in agreement with the proposed age of establishment of the modern Amazon River drainage. Our results also have taxonomic implications for these medically important venomous snakes, supporting unrecognized diversity at the species level.

Evaluating mechanisms of diversification in a Guineo-Congolian tropical forest frog using demographic model selection.

The accumulation of biodiversity in tropical forests can occur through multiple allopatric and parapatric models of diversification, including forest refugia, riverine barriers and ecological gradients. Considerable debate surrounds the major diversification process, particularly in the West African Lower Guinea forests, which contain a complex geographic arrangement of topographic features and historical refugia. We used genomic data to investigate alternative mechanisms of diversification in the Gaboon forest frog, Scotobleps gabonicus, by first identifying population structure and then performing demographic model selection and spatially explicit analyses. We found that a majority of population divergences are best explained by allopatric models consistent with the forest refugia hypothesis and involve divergence in isolation with subsequent expansion and gene flow. These population divergences occurred simultaneously and conform to predictions based on climatically stable regions inferred through ecological niche modelling. Although forest refugia played a prominent role in the intraspecific diversification of S. gabonicus, we also find evidence for potential interactions between landscape features and historical refugia, including major rivers and elevational barriers such as the Cameroonian Volcanic Line. We outline the advantages of using genomewide variation in a model-testing framework to distinguish between alternative allopatric hypotheses, and the pitfalls of limited geographic and molecular sampling. Although phylogeographic patterns are often species-specific and related to life-history traits, additional comparative studies incorporating genomic data are necessary for separating shared historical processes from idiosyncratic responses to environmental, climatic and geological influences on diversification.

Demographical history and palaeodistribution modelling show range shift towards Amazon Basin for a Neotropical tree species in the LGM.

BACKGROUND: We studied the phylogeography and demographical history of Tabebuia serratifolia (Bignoniaceae) to understand the disjunct geographical distribution of South American seasonally dry tropical forests (SDTFs). We specifically tested if the multiple and isolated patches of SDTFs are current climatic relicts of a widespread and continuously distributed dry forest during the last glacial maximum (LGM), the so called South American dry forest refugia hypothesis, using ecological niche modelling (ENM) and statistical phylogeography. We sampled 235 individuals of T. serratifolia in 17 populations in Brazil and analysed the polymorphisms at three intergenic chloroplast regions and ITS nuclear ribosomal DNA. RESULTS: Coalescent analyses showed a demographical expansion at the last c. 130 ka (thousand years before present). Simulations and ENM also showed that the current spatial pattern of genetic diversity is most likely due to a scenario of range expansion and range shift towards the Amazon Basin during the colder and arid climatic conditions associated with the LGM, matching the expected for the South American dry forest refugia hypothesis, although contrasting to the Pleistocene Arc hypothesis. Populations in more stable areas or with higher suitability through time showed higher genetic diversity. Postglacial range shift towards the Southeast and Atlantic coast may have led to spatial genome assortment due to leading edge colonization as the species tracks suitable environments, leading to lower genetic diversity in populations at higher distance from the distribution centroid at 21 ka. CONCLUSION: Haplotype sharing or common ancestry among populations from Caatinga in Northeast Brazil, Atlantic Forest in Southeast and Cerrado biome and ENM evince the past connection among these biomes.

Trans-Amazon dispersal potential for Crotalus durissus during Pleistocene climate events / Potencial de dispersión trans-Amazónica de Crotalus durissus durante el Pleistoceno

Two disjunct distributional areas of Crotalus durissus (Neotropical rattlesnake) are in open habitats north and south of the Amazon Basin and are presently separated by humid rainforest habitats. We used ecological niche modeling to identify and investigate potential dispersal pathways for this species between the two areas during the late Pleistocene. Niches estimated for the two populations did not differ significantly. Our analyses indicated two possible, but a single most likely, potential routes of dispersal during the last glacial cycle. These results are important to understanding the history of Amazon Basin humid forest biotas, as they suggest agents of isolation among putative humid forest refugia in the form of dry forest and scrub, and associated biotas.

Actualmente existen dos áreas de distribución disyuntas de la serpiente de cascabel Crotalus durissus, afín a hábitats abiertos, al norte y al sur de la cuenca del Río Amazonas, separadas por selvas húmedas. Usamos técnicas de modelado de nicho ecológico para identificar corredores potenciales de dispersión para esta especie entre las dos áreas en el Pleistoceno tardío. Los nichos estimados para las poblaciones de cada una de las áreas de distribución no presentaron diferencias significativas. Nuestros análisis identificaron un corredor de dispersión más probable para esta especie durante el Último Máximo Glaciar. Estos resultados tienen implicaciones para el entendimiento de la historia de las biotas de las selvas húmedas del Amazonas, ya que sugieren causas de aislamiento entre refugios potenciales de selva húmeda, en la forma de selva seca y matorral.

Prediction of phylogeographic endemism in an environmentally complex biome.

Phylogeographic endemism, the degree to which the history of recently evolved lineages is spatially restricted, reflects fundamental evolutionary processes such as cryptic divergence, adaptation and biological responses to environmental heterogeneity. Attempts to explain the extraordinary diversity of the tropics, which often includes deep phylogeographic structure, frequently invoke interactions of climate variability across space, time and topography. To evaluate historical versus contemporary drivers of phylogeographic endemism in a tropical system, we analyse the effects of current and past climatic variation on the genetic diversity of 25 vertebrates in the Brazilian Atlantic rainforest. We identify two divergent bioclimatic domains within the forest and high turnover around the Rio Doce. Independent modelling of these domains demonstrates that endemism patterns are subject to different climatic drivers. Past climate dynamics, specifically areas of relative stability, predict phylogeographic endemism in the north. Conversely, contemporary climatic heterogeneity better explains endemism in the south. These results accord with recent speleothem and fossil pollen studies, suggesting that climatic variability through the last 250 kyr impacted the northern and the southern forests differently. Incorporating sub-regional differences in climate dynamics will enhance our ability to understand those processes shaping high phylogeographic and species endemism, in the Neotropics and beyond.

Uncovering cryptic diversity and refugial persistence among small mammal lineages across the Eastern Afromontane biodiversity hotspot.

The Eastern Afromontane region of Africa is characterized by striking levels of endemism and species richness accompanied by significant conservation threat, a pattern typical across biodiversity hotspots. Using multi-locus molecular data under a coalescent species tree framework we identify major cryptic biogeographic patterns within and between two endemic montane small mammal species complexes, Hylomyscus mice and Sylvisorex shrews, co-distributed across the Albertine Rift and Kenya Highlands of the Eastern Afromontane Biodiversity Hotspot (EABH). Hypotheses put forward to account for the high diversity of the region include retention of older palaeo-endemic lineages across major regions in climatically stable refugia, as well as the accumulation of lineages associated with more recent differentiation between allopatric populations separated by unsuitable habitat during periods of Pleistocene aridification. Sympatric pairs of sister lineages were found to have significantly older divergence times than allopatric pairs. Genetic analyses and historical distribution modeling suggest that regional meta-populations have persisted since the Pliocene to mid-Pleistocene across a climatic gradient from the Albertine Rift in the west to the Kenya Highlands in the east for both focal taxa. Differing patterns of regional sub-division and demographic expansion were detected and are consistent with differing life histories as well as shared responses to regional variation in stability of suitable habitat. There is also strong support in both mice and shrew species for Late Miocene divergence with subsequent range expansion into sympatry in previously unidentified cryptic species pairs. These results highlight the broad temporal scale at which climatic and geological changes may have facilitated rare dispersal events between montane habitats as well as the long-term persistence of populations in both the Albertine Rift and the Kenyan Highlands that together contributed to the high species diversity and endemism in the EABH.

The biogeographical assignment of a west Kenyan rain forest remnant: further evidence from analysis of its reptile fauna.

Aim The Kakamega Forest, western Kenya, has been biogeographically assigned to both lowland and montane forest biomes, or has even been considered to be unique. Most frequently it has been linked with the Guineo-Congolian rain forest block. The present paper aims to test six alternative hypotheses of the zoogeographical relationships between this forest remnant and other African forests using reptiles as a model group. Reptiles are relatively slow dispersers, compared with flying organisms (Aves and Odonata) on which former hypotheses have been based, and may thus result in a more conservative biogeographical analysis. Location Kakamega Forest, Kenya, Sub-Saharan Africa. Methods The reptile diversity of Kakamega Forest was evaluated by field surveys and data from literature resources. Faunal comparisons of Kakamega Forest with 16 other African forests were conducted by the use of the 'coefficient of biogeographic resemblance' using the reptile communities as zoogeographic indicators. Parsimony Analysis of Endemism and Neighbour Joining Analysis of Endemism were used to generate relationship trees based on an occurrence matrix with paup*. Results The analysis clearly supports the hypothesis that the Kakamega Forest is the easternmost fragment of the Guineo-Congolian rain forest belt, and thus more closely related to the forests of that Central-West African complex than to any forest further east, such as the Kenyan coastal forests. Many Kenyan reptile species occur exclusively in the Kakamega Forest and its associated forest fragments. Main conclusions The Kakamega Forest is the only remnant of the Guineo-Congolian rain forest in the general area. We assume that the low degree of resemblance identified for the Guineo-Congolian forest and the East African coastal forest reflect the long history of isolation of the two forest types from each other. Kenyan coastal forests may have been historically connected through forest 'bridges' of the southern highlands with the Congo forest belt, allowing reptile species to migrate between them. The probability of a second 'bridge' located in the region of southern Tanzanian inselbergs is discussed. Although not particularly rich in reptile species, the area should be considered of high national priority for conservation measures.