Diversification in the Andes: age and origins of South American Heliotropium lineages (Heliotropiaceae, Boraginales)

The uplift of the Andes was a major factor for plant diversification in South America and had significant effects on the climatic patterns at the continental scale. It was crucial for the formation of the arid environments in south-eastern and western South America. However, both the timing of the major stages of the Andean uplift and the onset of aridity in western South America remain controversial. In this paper we examine the hypothesis that the Andean South American groups of Heliotropium originated and diversified in response to Andean orogeny during the late Miocene and a the subsequent development of aridity. To this end, we estimate divergence times and likely biogeographical origins of the major clades in the phylogeny of Heliotropium, using both Bayesian and likelihood methods. Divergence times of all Andean clades in Heliotropium are estimated to be of late Miocene or Pliocene ages. At least three independent Andean diversification events can be recognized within Heliotropium. Timing of the diversification in the Andean lineages Heliotropium sects.Heliothamnus, Cochranea, Heliotrophytum, Hypsogenia, Plagiomeris, Platygyne clearly correspond to a rapid, late Miocene uplift of the Andes and a Pliocene development of arid environments in South America.     

Evolutionary patterns of diversification in the Andean hummingbird genus Adelomyia

The patterns of genetic diversity and morphological variation are of central importance in understanding the evolutionary process that drive diversification. We use molecular, morphological, and ecological data to explore the influence of geography and ecology in promoting speciation in the widespread Andean hummingbird genus Adelomyia. Six monophyletic clades were recovered which show distributional limits at well-defined geographic barriers. Percentage sequence divergence ranged between 5.8% and 8.2% between phylogroups separated by large (>4000 km) and small (<50 km) distances respectively, suggesting that geographic isolation may be influential at very different scales. We show that morphological traits in independent phylogroups are more related to environmental heterogeneity than to geographic barriers. We provide a molecular reconstruction of relationships within Adelomyia and recommend its use in future comparative studies of historical biogeography and diversification in the Andes.     

Phylogeny and diversification of the cloud forest Morpho sulkowskyi group (Lepidoptera,Nymphalidae) in the evolving Andes

The monophyletic Morpho sulkowskyi butterfly group, endemic of Andean cloud forests, was studied to test the respective contributions of Mio‐Pliocene intense uplift period and Pleistocene glacial cycles on Andean biodiversity. We sampled nine taxa covering the whole geographical range of the group. Two mitochondrial and two nuclear genes were analysed using a Bayesian method. We established a dated phylogeny of the group using a relaxed clock method and a wide‐outgroup approach. To discriminate between two hypotheses, we used a biogeographical probabilistic method. Results suggest that the ancestor of the M. sulkowskyi group originated during the Middle–Late Miocene uplift of the Eastern Cordillera in northern Peru. Biogeographical inference suggests that the M. sulkowskyi and Morpho lympharis clades diverged in the northern Peruvian Andes. The subsequent divergences, from the Late Miocene to the Late Pliocene, should have resulted from a dispersal towards the Northern Andes (M. sulkowskyi clade), after the closure of the West Andean Portal separating the Central and Northern Andes, and a southwards dispersal along the Peruvian and Bolivian Eastern Cordilleras (M. lympharis clade). Only a few divergences occurred at the very end of the Pliocene or during the Pleistocene, a period when the more recent uplifts interfered with Pleistocene glacial cycles.     

Diversification patterns in the CES clade (Brassicaceae tribes Cremolobeae,Eudemeae, Schizopetaleae) in Andean South America

Dated molecular phylogenetic trees show that the Andean uplift had a major impact on South American biodiversity. For many Andean groups, accelerated diversification (radiation) has been documented. However, not all Andean lineages appear to have diversified following the model of rapid radiation, particularly in the central and southern Andes. Here, we investigated the diversification patterns for the largest South American‐endemic lineage of Brassicaceae, composed of tribes Cremolobeae, Eudemeae and Schizopetaleae (CES clade). Species of this group inhabit nearly all Andean biomes and adjacent areas including the Atacama–Sechura desert, the Chilean Matorral and the Patagonian Steppe. First, we studied diversification times and historical biogeography of the CES clade. Second, we analysed diversification rates through time, lineages and associated life forms. Results demonstrate that early diversification of the CES clade occurred in the early to mid‐Miocene (c. 12–19 Mya) and involved the central Andes, the southern Andes and the Patagonian Steppe, and the Atacama–Sechura desert. The Chilean Matorral and northern Andes were colonized subsequently in the early Pliocene (4–5 Mya). Diversification of the CES clade was recovered as a gradual process without any evidence for rate shifts or rapid radiation, in contrast to many other Andean groups analysed so far. Diversification time/rates and biogeographical patterns obtained for the CES clade are discussed and compared with patterns and conclusions reported for other Andean plant lineages.     

The role of geography and ecology in shaping the phylogeography of the speckled hummingbird (Adelomyia melanogenys) in Ecuador

The Andes of South America contain one of the richest avifaunas in the world, but little is known about how this diversity arises and is maintained. Variation in mitochondrial DNA and morphology within the speckled hummingbird (Adelomyia melanogenys) was used to elucidate the phylogeographic pattern along an Ecuadorian elevational gradient, from the coastal cordillera to the inland Andean montane region. We examined sequence, climatic/remote sensing and morphological data to understand the effects of topography and ecology on patterns of variation. Populations on either side of the Andes are genetically divergent and were separated during a period that corresponds to the final stages of Andean uplift during the Pliocene. Despite isolation, these two populations were found to be morphologically similar suggesting a strong effect of stabilizing selection across ecologically similar Andean cloud forests, as assessed using climatic and remote sensing data. In contrast, little genetic divergence was found between coastal and west-Andean individuals, suggesting recent interruption of gene flow between these localities. However, coastal populations were found to inhabit different habitats compared to Andean populations as shown by climatic and remote sensing variables. Furthermore, coastal individuals had significantly longer bills compared to their montane relatives, indicative of differential directional selection and the influence of habitat differences in shaping phenotypic variation. Results highlight the role of both isolation and ecology in diversification in Ecuadorian montane regions, while suggesting the two may not always act in concert to produce divergence in adaptive traits.     

Evolutionary islands in the Andes: persistence and isolation explain high endemism in Andean dry tropical forests

Aim The tropical Andes are a world biodiversity hotspot. With diverse biomes and dramatic, geologically recent mountain uplift, they offer a system to study the relative contributions of geological and biome history to species richness. There are preliminary indications that historical species assembly in the Andes has been influenced by physiographical heterogeneity and that distinct biomes have evolved in relative isolation despite physical proximity. Here we test this ‘Andean biotic separation hypothesis’ by focusing on the low‐elevation, seasonally dry tropical forest (SDTF) biome to determine whether patterns of plant diversification within the SDTF differ from those in mid‐ and high‐elevation biomes. Location Tropical Andes, South America. Methods Densely sampled time‐calibrated phylogenies for five legume genera (Amicia, Coursetia, Cyathostegia, Mimosa and Poissonia) containing species endemic to the Andean SDTF biome were used to investigate divergence times and levels of geographical structure. Geographical structure was measured using isolation‐by‐distance methods. Meta‐analysis of time‐calibrated phylogenies of Andean plant groups was used to compare the pattern and tempo of endemic species diversification between the major Andean biomes. Results Long‐term persistence of SDTF in the Andes is suggested by old stem ages (5–27 Ma) of endemic genera/clades within genera, and deep divergences coupled with strong geographical structure among and within species. Comparison of species diversification patterns among different biomes shows that the relatively old, geographically confined pattern of species diversification in SDTF contrasts with the high‐elevation grasslands that show rapid and recent radiations driven by ecological opportunities. Main conclusions The SDTF biome has a long history in the Andes. We suggest that the diverse SDTF flora has been assembled gradually over the past c. 19 Ma from lineages exhibiting strong phylogenetic niche conservatism. These patterns suggest that Andean SDTFs have formed stable and strongly isolated ‘islands’ despite the upheavals of Andean uplift. Indeed, the Andean SDTFs may represent some of the most isolated and evolutionarily persistent continental plant communities, similar in many respects to floras of remote oceanic islands.     

Patterns of diversification in the high Andean Ponderacris grasshoppers (Orthoptera: Acrididae: Melanoplinae)

The Andes, the world's longest mountain chain, harbours great taxonomic and ecological diversity. Despite their young age, the tropical Andes are highly diverse due to recent geological uplift. Speciation either followed the orogeny closely or occurred after the Andean uplift, as a result of subsequent climatic changes. Different scenarios have been proposed to explain the diversification of high Andean taxa. The Melanoplinae grasshopper Ponderacris Ronderos & Cigliano is endemic to the eastern slopes of the Andes of Peru and Bolivia, mostly distributed between 1000 and 4000 m above sea level. Diversification in several montane habitats of Bolivia and Peru allows tests via cladistic analysis of distinct possible geographic modes of speciation. Eight species are recognized, with three described here as new with revised diagnostic morphological characters provided: Ponderacris carlcarbonelli sp.n., P. chulumaniensis sp.n. and P. amboroensis sp.n. Cladistic analyses of 15 species (8 ingroup and 7 outgroup) and 38 morphological characters, under equal and implied weighting, confirm the monophyly of Ponderacris. Characters from the external morphology and colour pattern provided less phylogenetic information than did the male abdominal terminalia and phallic complex. Species distributed in the Peruvian Andes constituted a monophyletic group, whereas those from the Bolivian Andes formed a basal paraphyletic grade. Dispersal–vicariance analysis resulted in one ancestral distribution reconstruction indicating that the most recent common ancestor was distributed in the Lower Montane Yungas of Bolivia. Eleven dispersal and one vicariant events are postulated, with a South‐to‐North speciation pattern coincident with progressive Andean uplift. Vicariance could relate to fragmentation of montane forest during the dry intervals of the late Cenozoic. From the Bolivian area, ancestral Peruvian Ponderacris may have dispersed northward, coinciding with the rise of the Andes. Ten of 11 dispersal events occurred at terminal taxa and are likely to be recent. However, diversification of Ponderacris cannot be explained solely by the South‐to‐North speciation hypothesis, but may also include both vicariance and dispersal across barriers influenced by Pleistocene climatic cycles.     

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.     

Elevational differentiation accelerates trait evolution but not speciation rates in Amazonian birds

The importance of ecologically mediated divergent selection in accelerating trait evolution has been poorly studied in the most species‐rich biome of the planet, the continental Neotropics. We performed macroevolutionary analyses of trait divergence and diversification rates across closely related pairs of Andean and Amazonian passerine birds, to assess whether the difference in elevational range separating species pairs – a proxy for the degree of ecological divergence – influences the speed of trait evolution and diversification rates. We found that elevational differentiation is associated with faster divergence of song frequency, a trait important for pre‐mating isolation, and several morphological traits, which may contribute to extrinsic post‐mating isolation. However, elevational differentiation did not increase recent speciation rates, possibly due to early bursts of diversification during the uplift of the eastern Andes followed by a slow‐down in speciation rate. Our results suggest that ecological differentiation may speed up trait evolution, but not diversification of Neotropical birds.     

Dispersal,isolation and diversification with continued gene flow in an Andean tropical dry forest

The Andes are the world's longest mountain chain, and the tropical Andes are the world's richest biodiversity hot spot. The origin of the tropical Andean cordillera is relatively recent because the elevation of the mountains was relatively low (400–2500 m palaeoelevations) only 10 MYA with final uplift being rapid. These final phases of the Andean orogeny are thought to have had a fundamental role in shaping processes of biotic diversification and biogeography, with these effects reaching far from the mountains themselves by changing the course of rivers and deposition of mineral‐rich Andean sediments across the massive Amazon basin. In a recent issue of Molecular Ecology, Oswald, Overcast, Mauck, Andersen, and Smith (2017) investigate the biogeography and diversification of bird species in the Andes of Peru and Ecuador. Their study is novel in its focus on tropical dry forests (Figure 1) rather than more mesic biomes such as rain forests, cloud forests and paramos, which tend to be the focus of science and conservation in the Andean hot spot. It is also able to draw powerful conclusions via the first deployment of genomic approaches to a biogeographic question in the threatened dry forests of the New World.     

HISTORICAL DIVERSIFICATION OF BIRDS IN NORTHWESTERN SOUTH AMERICA: A MOLECULAR PERSPECTIVE ON THE ROLE OF VICARIANT EVENTS

Studies of South American biodiversity have identified several areas of endemism that may have enhanced historical diversification of South American organisms. Hypotheses concerning the derivation of birds in the Chocó area of endemism in northwestern South America were evaluated using protein electrophoretic data from 14 taxonomically diverse species groups of birds. Nine of these groups demonstrated that the Chocó area of endemism has a closer historical relationship to Central America than to Amazonia, a result that is consistent with phytogeographic evidence. Within species groups, genetic distances between cis-Andean (east of the Andes) and trans-Andean (west of the Andes) taxa are, on average, roughly twice that between Chocó and Central American taxa. The genetic data are consistent with the hypotheses that the divergence of most cis-Andean and trans-Andean taxa was the result of either the Andean uplift fragmenting a once continuous Amazonian-Pacific population (Andean Uplift Hypothesis), the isolation of the two faunas in forest refugia on opposite sides of the Andes during arid climates (Forest Refugia Hypothesis), or dispersal of Amazonian forms directly across the Andes into the trans-Andean region (Across-Andes Dispersal Hypothesis). Disentangling these hypotheses is difficult due to the complexity of the Andean uplift and to the scant geologic and paleoclimatic information that elucidates diversification events in northwestern South America. Regarding the divergence of cis- and trans-Andean taxa, the genetic, geologic, and paleoclimatic data allow weak rejection of the Andean Uplift Hypothesis and weak support for the Forest Refugia and Andean Dispersal Hypotheses. The subsequent diversification of Chocó and Central American taxa was the result of Pleistocene forest refugia, marine transgressions, or parapatric speciation.     

The roles of wing color pattern and geography in the evolution of Neotropical Preponini butterflies

Diversification rates and evolutionary trajectories are known to be influenced by phenotypic traits and the geographic history of the landscapes that organisms inhabit. One of the most conspicuous traits in butterflies is their wing color pattern, which has been shown to be important in speciation. The evolution of many taxa in the Neotropics has also been influenced by major geological events. Using a dated, species‐level molecular phylogenetic hypothesis for Preponini, a colorful Neotropical butterfly tribe, we evaluated whether diversification rates were constant or varied through time, and how they were influenced by color pattern evolution and biogeographical events. We found that Preponini originated approximately 28 million years ago and that diversification has increased through time consistent with major periods of Andean uplift. Even though some clades show evolutionarily rapid transitions in coloration, contrary to our expectations, these shifts were not correlated with shifts in diversification. Involvement in mimicry with other butterfly groups might explain the rapid changes in dorsal color patterns in this tribe, but such changes have not increased species diversification in this group. However, we found evidence for an influence of major Miocene and Pliocene geological events on the tribe''s evolution. Preponini apparently originated within South America, and range evolution has since been dynamic, congruent with Andean geologic activity, closure of the Panama Isthmus, and Miocene climate variability.     

Out of the Andes: patterns of diversification in clearwing butterflies

Global biodiversity peaks in the tropical forests of the Andes, a striking geological feature that has likely been instrumental in generating biodiversity by providing opportunities for both vicariant and ecological speciation. However, the role of these mountains in the diversification of insects, which dominate biodiversity, has been poorly explored using phylogenetic methods. Here we study the role of the Andes in the evolution of a diverse Neotropical insect group, the clearwing butterflies. We used dated species-level phylogenies to investigate the time course of speciation and to infer ancestral elevation ranges for two diverse genera. We show that both genera likely originated at middle elevations in the Andes in the Middle Miocene, contrasting with most published results in vertebrates that point to a lowland origin. Although we detected a signature of vicariance caused by the uplift of the Andes at the Miocene–Pliocene boundary, most sister species were parapatric without any obvious vicariant barrier. Combined with an overall decelerating speciation rate, these results suggest an important role for ecological speciation and adaptive radiation, rather than simple vicariance.     

Andean uplift promotes lowland speciation through vicariance and dispersal in Dendrocincla woodcreepers

Andean uplift contributed importantly to the build-up of high Neotropical diversity. Final uplift of the Eastern Cordillera of Colombia separated once-contiguous lowland faunas east and west of the Andes between 5 and 3.5 million years ago (Ma hereafter). We used DNA sequences from several moderate- to fast-evolving mitochondrial and two slow-evolving nuclear genes to generate a well-supported phylogeny of Dendrocincla woodcreepers, a genus with multiple species endemic to lowland regions both east and west of the Andes. A time-calibrated phylogeny and dispersal-vicariance analysis indicated that uplift of the Eastern Cordillera of Colombia resulted in the initial vicariant separation of a widespread lowland form east and west of the Andes at c. 3.6 Ma. This was followed by two separate east-to-west dispersal events over or around the completed Andes, each producing a genetically distinct lineage. Our analysis suggests that Andean uplift promoted the build-up of biodiversity in lowland Neotropical faunas both through vicariance-based speciation during uplift and through dispersal-based speciation following uplift. In contrast to the multiple colonizations of the trans-Andean region by Dendrocincla, the Atlantic Forest was colonized from the Amazon only once, followed by in situ diversification.     

Patterns and timing of diversification in a tropical montane butterfly genus,Lymanopoda (Nymphalidae,Satyrinae)

Species distributions are a product of contemporary and historical forces. Using phylogenetic and geographic data, we explore the timing of and barriers to the diversification of the Andean butterfly genus Lymanopoda (Nymphalidae, Satyrinae). Clade and species level diversification is coincident with Andean orogeny and Pleistocene glaciation cycles. Lymanopoda has primarily diversified within elevational bands, radiating horizontally throughout the Andes with occasional speciation across elevational boundaries, often associated with ecotones. Narrow elevational ranges and infrequent speciation into adjacent elevational strata suggest that expansion across elevational gradients is relatively difficult. These results are similar to those found in studies of other Andean taxa.     

Genetic structuring in a Neotropical palm analyzed through an Andean orogenesis‐scenario

Andean orogenesis has driven the development of very high plant diversity in the Neotropics through its impact on landscape evolution and climate. The analysis of the intraspecific patterns of genetic structure in plants would permit inferring the effects of Andean uplift on the evolution and diversification of Neotropical flora. In this study, using microsatellite markers and Bayesian clustering analyses, we report the presence of four genetic clusters for the palm Oenocarpus bataua var. bataua which are located within four biogeographic regions in northwestern South America: (a) Chocó rain forest, (b) Amotape‐Huancabamba Zone, (c) northwestern Amazonian rain forest, and (d) southwestern Amazonian rain forest. We hypothesize that these clusters developed following three genetic diversification events mainly promoted by Andean orogenic events. Additionally, the distinct current climate dynamics among northwestern and southwestern Amazonia may maintain the genetic diversification detected in the western Amazon basin. Genetic exchange was identified between the clusters, including across the Andes region, discarding the possibility of any cluster to diversify as a distinct intraspecific variety. We identified a hot spot of genetic diversity in the northern Peruvian Amazon around the locality of Iquitos. We also detected a decrease in diversity with distance from this area in westward and southward direction within the Amazon basin and the eastern Andean foothills. Additionally, we confirmed the existence and divergence of O. bataua var. bataua from var. oligocarpus in northern South America, possibly expanding the distributional range of the latter variety beyond eastern Venezuela, to the central and eastern Andean cordilleras of Colombia. Based on our results, we suggest that Andean orogenesis is the main driver of genetic structuring and diversification in O. bataua within northwestern South America.     

How mountains shape biodiversity: The role of the Andes in biogeography,diversification, and reproductive biology in South America's most species‐rich lizard radiation (Squamata: Liolaemidae)

Testing hypotheses on drivers of clade evolution and trait diversification provides insight into many aspects of evolutionary biology. Often, studies investigate only intrinsic biological properties of organisms as the causes of diversity, however, extrinsic properties of a clade's environment, particularly geological history, may also offer compelling explanations. The Andes are a young mountain chain known to have shaped many aspects of climate and diversity of South America. The Liolaemidae are a radiation of South American reptiles with over 300 species found across most biomes and with similar numbers of egg‐laying and live‐bearing species. Using the most complete dated phylogeny of the family, we tested the role of Andean uplift in biogeography, diversification patterns, and parity mode of the Liolaemidae. We find that the Andes promoted lineage diversification and acted as a species pump into surrounding biomes. We also find strong support for the role of Andean uplift in boosting the species diversity of these lizards via allopatric fragmentation. Finally, we find repeated shifts in parity mode associated with changing thermal niches, with live‐bearing favored in cold climates and egg‐laying favored in warm climates. Importantly, we find evidence for possible reversals to oviparity, an evolutionary transition believed to be extremely rare.     

Into the Andes: multiple independent colonizations drive montane diversity in the Neotropical clearwing butterflies Godyridina

Understanding why species richness peaks along the Andes is a fundamental question in the study of Neotropical biodiversity. Several biogeographic and diversification scenarios have been proposed in the literature, but there is confusion about the processes underlying each scenario, and assessing their relative contribution is not straightforward. Here, we propose to refine these scenarios into a framework which evaluates four evolutionary mechanisms: higher speciation rate in the Andes, lower extinction rates in the Andes, older colonization times and higher colonization rates of the Andes from adjacent areas. We apply this framework to a species‐rich subtribe of Neotropical butterflies whose diversity peaks in the Andes, the Godyridina (Nymphalidae: Ithomiini). We generated a time‐calibrated phylogeny of the Godyridina and fitted time‐dependent diversification models. Using trait‐dependent diversification models and ancestral state reconstruction methods we then compared different biogeographic scenarios. We found strong evidence that the rates of colonization into the Andes were higher than the other way round. Those colonizations and the subsequent local diversification at equal rates in the Andes and in non‐Andean regions mechanically increased the species richness of Andean regions compared to that of non‐Andean regions (‘species‐attractor’ hypothesis). We also found support for increasing speciation rates associated with Andean lineages. Our work highlights the importance of the Andean slopes in repeatedly attracting non‐Andean lineages, most likely as a result of the diversity of habitats and/or host plants. Applying this analytical framework to other clades will bring important insights into the evolutionary mechanisms underlying the most species‐rich biodiversity hotspot on the planet.     

Mass extinction, gradual cooling, or rapid radiation? Reconstructing the spatiotemporal evolution of the ancient angiosperm genus Hedyosmum (Chloranthaceae) using empirical and simulated approaches

Chloranthaceae is a small family of flowering plants (65 species) with an extensive fossil record extending back to the Early Cretaceous. Within Chloranthaceae, Hedyosmum is remarkable because of its disjunct distribution--1 species in the Paleotropics and 44 confined to the Neotropics--and a long "temporal gap" between its stem age (Early Cretaceous) and the beginning of the extant radiation (late Cenozoic). Is this gap real, reflecting low diversification and a recent radiation, or the signature of extinction? Here we use paleontological data, relaxed-clock molecular dating, diversification analyses, and parametric ancestral area reconstruction to investigate the timing, tempo, and mode of diversification in Hedyosmum. Our results, based on analyses of plastid and nuclear sequences for 40 species, suggest that the ancestor of Chloranthaceae and the Hedyosmum stem lineages were widespread in the Holarctic in the Late Cretaceous. High extinction rates, possibly associated with Cenozoic climatic fluctuations, may have been responsible for the low extant diversity of the family. Crown group Hedyosmum originated c. 36-43 Ma and colonized South America from the north during the Early-Middle Miocene (c. 20 Ma). This coincided with an increase in diversification rates, probably triggered by the uplift of the Northern Andes from the Mid-Miocene onward. This study illustrates the advantages of combining paleontological, phylogenetic, and biogeographic data to reconstruct the spatiotemporal evolution of an ancient lineage, for which the extant diversity is only a remnant of past radiations. It also shows the difficulties of inferring patterns of lineage diversification when incomplete taxon sampling is combined with high extinction rates.     

Pleistocene climatic cycling and diversification of the Andean treefrog, Hypsiboas andinus

Our understanding of the causes of diversification of Neotropical organisms lags behind that of Northern Hemisphere biota, especially for montane and temperate regions of southern South America. We investigated the mitochondrial DNA genealogical patterns in 262 individuals of the frog Hypsiboas andinus from 26 sites across the eastern ranges of the Andes Mountains in Argentina and Bolivia. Our phylogenetic analyses indicate at least three distinct lineages: one representing H. andinus from Northwestern Argentina and southern Bolivia, at least one H. andinus lineage from northern Bolivia, and one clade containing both H. andinus (from the southern portion of the species range) and its putative sister taxon Hypsiboas riojanus. Hypsiboas andinus samples from northern Bolivia are well differentiated and may represent distinct species. The northern Argentine H. andinus lineage and southern H. andinus/H. riojanus lineage likely diverged between 2 and 6 million years ago; their current sympatry may be the result of secondary contact due to range expansion after isolation during Andean uplift or may reflect cryptic species. Within the geographically extensive northern H. andinus clade, we found significant geographical structuring consistent with historical fragmentation and subsequent range expansion. The timing of this fragmentation and range expansion coincide with the Pleistocene, a time of extensive climatic cycling and vegetational shifts. Average divergence among clades is lower than those found for other Neotropical taxa, highlighting the potential importance of recent climatic history in diversification in the southern Andes.