Landscape genetics across the Andes mountains: Environmental variation drives genetic divergence in the leaf-cutting ant Atta cephalotes.

Distinguishing among the mechanisms underlying the spatial distribution of genetic variation resulting from the environmental or physical barriers from those arising due to simple geographic distance is challenging in complex landscapes. The Andean uplift represents one of the most heterogeneous habitats where multiple mechanisms may interact, confounding their relative roles. We explore this broad question in the leaf-cutting ant Atta cephalotes, a species that is distributed across the Andes mountains, using nuclear microsatellite markers and mtCOI gene sequences. We investigate spatial genetic divergence across the western range of the northern Andes in Colombia by testing the relative role of alternative scenarios of population divergence, including isolation by geographic distance (IBD), climatic conditions (IBE), and the physical barriers presented by the Andes mountains (IBB). Our results reveal substantial genetic differentiation among A. cephalotes populations for both types of markers, but only nuclear divergence followed a hierarchical pattern with multiple models of genetic divergence imposed by the western range. Model selection showed that the IBD, IBE (temperature and precipitation), and IBB (Andes mountains) models, often proposed as individual drivers of genetic divergence, interact, and explain up to 33% of the genetic divergence in A. cephalotes. The IBE model remained significant after accounting for IBD, suggesting that environmental factors play a more prominent role than IBB. These factors, in combination with the idiosyncratic dispersal patterns of ants, appear to determine the hierarchical patterns of gene flow. This study enriches our understanding of the forces shaping population divergence in complex habitat landscapes.

Out of the shadows: Multilocus systematics and biogeography of night monkeys suggest a Central Amazonian origin and a very recent widespread southeastward expansion in South America.

Night monkeys (Aotus, Cebidae) are a widely distributed genus of Neotropical primates with a poorly understood taxonomy and biogeography. The number of species in the genus varies from one to nine, depending on the author, and there are at least 18 known karyotypes, varying from 2n = 46 to 2n = 58. Historically, night monkeys are divided into two species groups: red- and grey-necked groups from south and north of the Amazon-Solimões River, respectively. Here, we used 10 nuclear and 10 mitochondrial molecular markers from a wide taxonomic and geographic sample to infer phylogeny, divergence times, and biogeography of the genus. For phylogenetic reconstruction we used Maximum Likelihood (ML) and Bayesian Inferences (BI). Biogeographic models were generated using the 'BioGeoBEARS' software. We found support for nine taxa of Aotus and rejected the existence of monophyletic "red necked" and "grey necked" species groups. We suggest a taxonomic reclassification of the genus, which is better represented by two clades named northern group, which contains Aotus miconax, A. nancymae, A. trivirgatus, A. vociferans, A. lemurinus, A. griseimembra, A. zonalis, and A. brumbacki, and southern group, which contains A. nigriceps, A. boliviensis, A. infulatus, and A. azarae. The results suggest that the most recent common ancestor of all species of Aotus arose in the central Amazon basin in the Early Pliocene. The evolutionary history of night monkeys was guided by dispersal, vicariance and founder events. The end of the Andean uplift and the subsequent changes in the Amazon landscape, as well as the Amazon-Solimões and Tapajós rivers may have played an important role in the origin and diversification of Aotus, respectively. However, most of the Amazonian rivers seem not to have been geographical barriers to dispersal of night monkeys. The herein named southern group is fruit of a very recent diversification guided by dispersal, crossing the Tapajós, Xingú, Tocantins, and Guapore rivers and reaching the Cerrado in the last 1.6 My.

Phylogenomic relationships and historical biogeography in the South American vegetable ivory palms (Phytelepheae).

The palm tribe Phytelepheae form a clade of three genera and eight species whose phylogenetic relationships and historical biogeography are not fully understood. Based on morphological similarities and phylogenetic relatedness, it has been suggested that Phytelephas seemannii and Phytelephas schottii are synonyms of Phytelephas macrocarpa, implying the existence of only six species within the Phytelepheae. In addition, uncertainty in their phylogenetic relationships in turn results in blurred biogeographic history. We inferred the phylogenomic relationships in the Phytelepheae by target-capturing 176 nuclear genes and estimated divergence times by using four fossils for time calibration. We lastly explored the biogeographic history of the tribe by inferring its ancestral range evolution. Our phylogenomic trees showed that P. seemannii and P. schottii are not closely related with P. macrocarpa, and therefore, support the existence of eight species in the Phytelepheae. The ancestor of the tribe was widely-distributed in the Chocó, Magdalena, and Amazonia during the Miocene at 19.25 Ma. Early diversification in Phytelephas at 5.27 Ma could have occurred by trans-Andean vicariance after the western Andes uplifted rapidly at âˆ¼ 10 Ma. Our results show the utility of phylogenomic approaches to shed light on species relationships and their biogeographic history.

Andean uplift, drainage basin formation, and the evolution of plants living in fast-flowing aquatic ecosystems in northern South America.

Northern South America is a geologically dynamic and species-rich region. Fossil and stratigraphic data show that mountain uplift in the tropical Andes reconfigured river drainages. These landscape changes shaped the evolution of the flora in the region, yet the impacts on aquatic taxa have been overlooked. We explore the role of landscape change on the evolution of plants living strictly in rivers across drainage basins in northern South America by conducting population structure, phylogenetic inference, and divergence-dating analyses for two species in the genus Marathrum (Podostemaceae). Mountain uplift and drainage basin formation isolated populations of M. utile and M. foeniculaceum in northern South America and created barriers to gene flow across river drainages. Sympatric species hybridize and the hybrids show the phenotype of one parental line. We propose that the pattern of divergence of populations reflects the formation of river drainages, which was not complete until < 4.1 million yr ago (Ma). Our study provides a clear picture of the role of landscape change on the evolution of plants living strictly in rivers in northern South America. By shifting the focus to aquatic taxa, we provide a novel perspective on the processes shaping the evolution of the Neotropical flora.

An exploration of the complex biogeographical history of the Neotropical banner-wing damselflies (Odonata: Polythoridae).

BACKGROUND: The New World Tropics has experienced a dynamic landscape across evolutionary history and harbors a high diversity of flora and fauna. While there are some studies addressing diversification in Neotropical vertebrates and plants, there is still a lack of knowledge in arthropods. Here we examine temporal and spatial diversification patterns in the damselfly family Polythoridae, which comprises seven genera with a total of 58 species distributed across much of Central and South America. RESULTS: Our time-calibrated phylogeny for 48 species suggests that this family radiated during the late Eocene (~ 33 Ma), diversifying during the Miocene. As with other neotropical groups, the Most Recent Common Ancestor (MRCA) of most of the Polythoridae genera has a primary origin in the Northern Andes though the MRCA of at least one genus may have appeared in the Amazon Basin. Our molecular clock suggests correlations with some major geographical events, and our biogeographical modeling (with BioGeoBEARS and RASP) found a significant influence of the formation of the Pebas and Acre systems on the early diversification of these damselflies, though evidence for the influence of the rise of the different Andean ranges was mixed. Diversification rates have been uniform in all genera except one-Polythore-where a significant increase in the late Pliocene (~ 3 mya) may have been influenced by recent Andean uplift. CONCLUSION: The biogeographical models implemented here suggest that the Pebas and Acre Systems were significant geological events associated with the diversification of this damselfly family; while diversification in the tree shows some correlation with mountain building events, it is possible that other abiotic and biotic changes during our study period have influenced diversification as well. The high diversification rate observed in Polythore could be explained by the late uplift of the Northern Andes. However, it is possible that other intrinsic factors like sexual and natural selection acting on color patterns could be involved in the diversification of this genus.

Special issue: Comparative biogeography of Neotropical primates.

New research presented in this special issue of Molecular Phylogenetics and Evolution on the "Phylogeny and Biogeography of Neotropical Primates" greatly improves our understanding of the evolutionary history of the New World monkeys and provides insights into the multiple platyrrhine radiations, diversifications, extinctions, and recolonizations that have taken place over time and over space in the Neotropics. Here, we synthesize genetic and biogeographic research from the past several years to construct an overarching hypothesis for platyrrhine evolution. We also highlight continuing controversies in Neotropical primate biogeography, such as whether the location of origin of platyrrhines was Africa or Asia; whether Patagonian fossil primates are stem or crown platyrrhines; and whether cis- and trans-Andean Neotropical primates were subject to vicariance through Andes mountain building, or instead diversified through isolation in mountain valleys after skirting around the Andes on the northwestern coast of South America. We also consider the role of the Amazon River and its major tributaries in shaping platyrrhine biodiversity, and how and when primates from the Amazon reached the Atlantic Forest. A key focus is on primate colonizations and extirpations in Central America, the Andes, and the seasonally dry tropical forests and savannas (such as the Llanos, Caatinga, and Cerrado habitats), all ecosystems that have been understudied up until now for primates. We suggest that most primates currently inhabiting drier open habitats are relatively recent arrivals, having expanded from rainforest habitats in the Pleistocene. We point to the Pitheciidae as the taxonomic group most in need of further phylogenetic and biogeographic research. Additionally, genomic studies on the Platyrrhini are deeply needed and are expected to bring new surprises and insights to the field of Neotropical primate biogeography.

The rapid radiation of Bomarea (Alstroemeriaceae: Liliales), driven by the rise of the Andes.

Geological events such as mountain uplift affect how, when, and where species diversify, but measuring those effects is a longstanding challenge. Andean orogeny impacted the evolution of regional biota by creating barriers to gene flow, opening new habitats, and changing local climate. B⁢o⁢m⁢a⁢r⁢e⁢a (Alstroemeriaceae) are tropical plants with (often) small, isolated ranges; in total, B⁢o⁢m⁢a⁢r⁢e⁢a species occur from central Mexico to central Chile. This genus appears to have evolved rapidly and quite recently, and rapid radiations are often challenging to resolve with traditional phylogenetic inference. In this study, we apply phylogenomics-with hundreds of loci, gene-tree-based data curation, and a multispecies-coalescent approach-to infer the phylogeny of B⁢o⁢m⁢a⁢r⁢e⁢a. We use this phylogeny to untangle the potential drivers of diversification and biogeographic history. In particular, we test if Andean orogeny contributed to the diversification of B⁢o⁢m⁢a⁢r⁢e⁢a. We find that B⁢o⁢m⁢a⁢r⁢e⁢a originated in the central Andes during the mid-Miocene, then spread north, following the trajectory of mountain uplift. Furthermore, Andean lineages diversified faster than non-Andean relatives. B⁢o⁢m⁢a⁢r⁢e⁢a thus demonstrates that-at least in some cases-geological change rather than environmental stability has driven high species diversity in a tropical biodiversity hotspot. These results also demonstrate the utility (and danger) of genome-scale data for making macroevolutionary inferences.

Biogeography and spatio-temporal diversification of Selenidera and Andigena toucans (Aves: Ramphastidae).

Andean uplift, Plio-Pleistocene climatic fluctuation, and river dynamics in the Amazon basin have all been implicated in the diversification of the South American avifauna. We reconstructed phylogenetic relationships in the genus Selenidera, which has served as a classic case of putative refugial speciation, and the closely related genus Andigena, to better understand the processes driving their diversification. Using mitochondrial and nuclear DNA sequences, we constructed a phylogeny to estimate the pattern and timing of divergence within and between seven lowland Selenidera toucanets and the five species of Andigena mountain-toucans, which together form a single clade. All phylogenetic analyses supported the monophyly of the montane genus Andigena, but indicated that the genus Selenidera is likely paraphyletic with respect to Andigena. Our time tree analysis is consistent with the orogenic uplift of the northern Andean range having initiated the divergence between Selenidera and Andigena, and that the movement and fragmentation of montane habitats in response to Pleistocene climatic oscillations likely influenced diversification within Andigena. Estimated divergence times for lowland Amazonian Selenidera did not support the Last Glacial Maximum (LGM) refuge hypothesis as an important biogeographic factor for the diversification of lineages studied here. The timing of divergence within Selenidera is consistent with the hypothesis that geographic isolation of areas of endemism generated by Amazonian river dynamics during the Plio-Pleistocene contributed to Selenidera speciation and current species distributions.

Synthesis of geological data and comparative phylogeography of lowland tetrapods suggests recent dispersal through lowland portals crossing the Eastern Andean Cordillera.

Vicariance is the simplest explanation for divergence between sister lineages separated by a potential barrier, and the northern Andes would seem to provide an ideal example of a vicariant driver of divergence. We evaluated the potential role of the uplift of the Eastern Cordillera (EC) of the Colombian Andes and the Mérida Andes (MA) of Venezuela as drivers of vicariance between lowland populations co-distributed on both flanks. We synthesized published geological data and provided a new reconstruction showing that the EC-MA grew from north to south, reaching significant heights and separating drainages and changing sediment composition by 38-33 million years ago (Ma). A few lowland passes across the EC-MA may have reached their current heights (~1,900 m a.s.l.) at 3-5 Ma. We created a comparative phylogeographic data set for 37 lineages of lowland tetrapods. Based on molecular phylogenetic analyses, most divergences between sister populations or species across the EC-MA occurred during Pliocene and the Quaternary and a few during the latest Miocene, and coalescent simulations rejected synchronous divergence for most groups. Divergence times were on average slightly but significantly more recent in homeotherms relative to poikilotherms. Because divergence ages are mostly too recent relative to the geological history and too asynchronous relative to each other, divergence across the northern Andes may be better explained by organism-environment interactions concomitant with climate oscillations during the Pleistocene, and/or dispersal across portals through the Andes.

The Origin and Diversification of the Hyperdiverse Flora in the Chocó Biogeographic Region.

Extremely high levels of plant diversity in the American tropics are derived from multiple interactions between biotic and abiotic factors. Previous studies have focused on macro-evolutionary dynamics of the Tropical Andes, Amazonia, and Brazil's Cerrado and Atlantic forests during the last decade. Yet, other equally important Neotropical biodiversity hotspots have been severely neglected. This is particularly true for the Chocó region on the north-western coast of South and Central America. This geologically complex region is Earth's ninth most biodiverse hotspot, hosting approximately 3% of all known plant species. Here, we test Gentry's [1982a,b] hypothesis of a northern Andean-Central American Pleistocene origin of the Chocoan flora using phylogenetic reconstructions of representative plant lineages in the American tropics. We show that plant diversity in the Chocó is derived mostly from Andean immigrants. Contributions from more distant biogeographical areas also exist but are fewer. We also identify a strong floristic connection between the Chocó and Central America, revealed by multiple migrations into the Chocó during the last 5 Ma. The dated phylogenetic reconstructions suggest a Plio-Pleistocene onset of the extant Chocó flora. Taken together, these results support to a limited extend Gentry's hypothesis of a Pleistocene origin and of a compound assembly of the Chocoan biodiversity hotspot. Strong Central American-Chocoan floristic affinity may be partly explained by the accretion of a land mass derived from the Caribbean plate to north-western South America. Additional densely sampled phylogenies of Chocoan lineages also well represented across the Neotropics could enlighten the role of land mass movements through time in the assembly of floras in Neotropical biodiversity hotspots.

Phylogeny, time divergence, and historical biogeography of the South American Liolaemus alticolor-bibronii group (Iguania: Liolaemidae).

The genus Liolaemus comprises more than 260 species and can be divided in two subgenera: Eulaemus and Liolaemus sensu stricto. In this paper, we present a phylogenetic analysis, divergence times, and ancestral distribution ranges of the Liolaemus alticolor-bibronii group (Liolaemus sensu stricto subgenus). We inferred a total evidence phylogeny combining molecular (Cytb and 12S genes) and morphological characters using Maximum Parsimony and Bayesian Inference. Divergence times were calculated using Bayesian MCMC with an uncorrelated lognormal distributed relaxed clock, calibrated with a fossil record. Ancestral ranges were estimated using the Dispersal-Extinction-Cladogenesis (DEC-Lagrange). Effects of some a priori parameters of DEC were also tested. Distribution ranged from central Perú to southern Argentina, including areas at sea level up to the high Andes. The L. alticolor-bibronii group was recovered as monophyletic, formed by two clades: L. walkeri and L. gracilis, the latter can be split in two groups. Additionally, many species candidates were recognized. We estimate that the L. alticolor-bibronii group diversified 14.5 Myr ago, during the Middle Miocene. Our results suggest that the ancestor of the Liolaemus alticolor-bibronii group was distributed in a wide area including Patagonia and Puna highlands. The speciation pattern follows the South-North Diversification Hypothesis, following the Andean uplift.

Gene flow and Andean uplift shape the diversification of Gasteracantha cancriformis (Araneae: Araneidae) in Northern South America.

The Andean uplift has played a major role in shaping the current Neotropical biodiversity. However, in arthropods other than butterflies, little is known about how this geographic barrier has impacted species historical diversification. Here, we examined the phylogeography of the widespread color polymorphic spider Gasteracantha cancriformis to evaluate the effect of the northern Andean uplift on its divergence and assess whether its diversification occurred in the presence of gene flow. We inferred phylogenetic relationships and divergence times in G. cancriformis using mitochondrial and nuclear data from 105 individuals in northern South America. Genetic diversity, divergence, and population structure were quantified. We also compared multiple demographic scenarios for this species using a model-based approach (phrapl) to determine divergence with or without gene flow. At last, we evaluated the association between genetic variation and color polymorphism. Both nuclear and mitochondrial data supported two well-differentiated clades, which correspond to populations occurring on opposite sides of the Eastern cordillera of the Colombian Andes. The final uplift of this cordillera was identified as the most likely force that shaped the diversification of G. cancriformis in northern South America, resulting in a cis- and trans-Andean phylogeographic structure for the species. We also found shared genetic variation between the cis- and trans-Andean clades, which is better explained by a scenario of historical divergence in the face of gene flow. This has been likely facilitated by the presence of low-elevation passes across the Eastern Colombian cordillera. Our work constitutes the first example in which the Andean uplift coupled with gene flow influenced the evolutionary history of an arachnid lineage.