Conceptual and empirical bridges between micro- and macroevolution.

Explaining broad molecular, phenotypic and species biodiversity patterns necessitates a unifying framework spanning multiple evolutionary scales. Here we argue that although substantial effort has been made to reconcile microevolution and macroevolution, much work remains to identify the links between biological processes at play. We highlight four major questions of evolutionary biology whose solutions require conceptual bridges between micro and macroevolution. We review potential avenues for future research to establish how mechanisms at one scale (drift, mutation, migration, selection) translate to processes at the other scale (speciation, extinction, biogeographic dispersal) and vice versa. We propose ways in which current comparative methods to infer molecular evolution, phenotypic evolution and species diversification could be improved to specifically address these questions. We conclude that researchers are in a better position than ever before to build a synthesis to understand how microevolutionary dynamics unfold over millions of years.

Hybridization boosters diversification in a Neotropical Bulbophyllum (Orchidaceae) group.

Genetic data shows that cryptic hybrids are more common than previously thought and that hybridization and introgression are widespread processes. Regardless, studies on hybridization are scarce for the highly speciose Bulbophyllum. The genus presents more than 2,200 species and many examples of recent radiations, in which hybridization is expected to be frequent. Currently, only four natural Bulbophyllum hybrids are recognized, all of them recently described based on morphological evidence. Here we test whether genomic evidence supports the hybrid status of two Neotropical Bulbophyllum species, while also evaluating the impact of this phenomenon on the genomes of the putative parental species. We also assess if there is evidence of hybridization among B. involutum and B. exaltatum, sister species that diverged recently. We leverage the power of next-generation sequence data, associated with model-based analysis for three systems putatively constituted by two parental species and one hybrid. All taxa belong to the Neotropical B. sect. Didactyle clade. We found evidence of hybridization in all studied systems. Despite the occurrence of hybridization, there are no signs of backcrossing. Because of the high propensity of hybridization across many taxa, the common occurrence of hybridization during the evolutionary history of B. sect. Didactyle means it is time to account for and examine its evolutionary role in these orchids.

Geographic isolation alone does not explain divergence of a group of orchid species across Brazil's campos rupestres sky-islandsIsolamento geográfico por si só não explica a divergência de um grupo de espécies de orquídeas nos campos rupestres do Brasil.

Mountains play a crucial role in the origin and maintenance of Neotropical biodiversity, but there are still unanswered questions about the diversification of the campos rupestres (CR), an herbaceous-shrubby sky-island vegetation in eastern South America. For orchids distributed across this disjunct rock habitat, difficulties with distinguishing morphological taxa add an additional challenge to disentangling the history of divergence. Here, we combined the power of ddRAD genomic data with broad sampling of Bulbophyllum sect. Didactyle (Orchidaceae), across the CR and other Neotropical outcrops, to estimate evolutionary relationships and evaluate the biogeography of the group's diversification. Although genetic lineages generally align with geographic disjunctions, we also observe distantly related lineages within some previously recognized species. For such taxa, their lack of monophyly and a shared regional divergence pattern suggests a complex history that may include unrecognized diversity. When viewed through the lens of morphological variability, our study raises intriguing questions about the persistence and permeability of species barriers among orchid populations. These results, in addition to the recency of the divergence history of B. sect. Didactyle, provide insights about hypothesized community level vs. species-specific paths of diversification across the Neotropical sky-islands of the CR.

Landscape connectivity among coastal giant salamander (Dicamptodon tenebrosus) populations shows no association with land use, fire frequency, or river drainage but exhibits genetic signatures of potential conservation concern.

Determining the genetic consequences of both historical and contemporary events can clarify the effects of the environment on population connectivity and inform conservation decisions. Historical events (like glaciations) and contemporary factors (like logging) can disrupt gene flow between populations. This is especially true among species with specialized ecological requirements and low dispersal ability, like amphibians. We test for the genetic consequences of historical and contemporary disturbances in the coastal giant salamander (Dicamptodon tenebrosus) in the Pacific Northwest of the United States. We consider predictions based on the contemporary landscape (habitat connectivity, logging, forest fires, and topography), in addition to relatively ancient post-Pleistocene range expansion (following the last glacial retreat). To assess local versus larger-scale effects, we sampled 318 individuals across 23 sites, which were clustered in five sampling regions. Genetic variation was assessed using five microsatellite markers. We found evidence of (i) historical regional isolation, with decreased genetic diversity among more recently colonized northern sites, as well as (ii) high levels of inbreeding and loss of heterozygosity at local scales, despite relatively low overall population differentiation (FST) or strong evidence for population bottlenecks. Genetic diversity was not associated with contemporary disturbances (logging or fire), and there were no detectable effects on the genetic connectivity of populations based on intervening landscape features (habitat fragmentation and topography). However, lower genetic diversity in more northern regions indicates a lag in recovery of genetic diversity following post-Pleistocene expansion. Additionally, some populations had evidence of having undergone a recent genetic bottleneck or had high inbreeding (FIS) values. Lower genetic diversity in more northern sites means populations may be more vulnerable to future environmental changes, and managing for connectivity alone may not be sufficient given low mobility. Recent apparent reductions in some populations were not clearly linked to anthropogenic disturbances we examined. This suggests the type of disturbances this species is sensitive to may not be well understood.

Hybrid enrichment of adaptive variation revealed by genotype-environment associations in montane sedges.

The role of hybridization in diversification is complex and may result in many possible outcomes. Not only can hybridization produce new lineages, but those lineages may contain unique combinations of adaptive genetic variation derived from parental taxa that allow hybrid-origin lineages to occupy unique environmental space relative to one (or both) parent(s). We document such a case of hybridization between two sedge species, Carex nova and Carex nelsonii (Cyperaceae), that occupy partially overlapping environmental space in the southern Rocky Mountains, USA. In the region hypothesized to be the origin of the hybrid lineage, one parental taxon (C. nelsonii) is at the edge of its environmental tolerance. Hybrid-origin individuals display mixed ancestry between the parental taxa-of nearly 7000 unlinked loci sampled, almost 30% showed evidence of excess ancestry from one parental lineage-approximately half displayed a genomic background skewed towards one parent, and half skewed towards the other. To test whether excess ancestry loci may have conferred an adaptive advantage to the hybrid-origin lineage, we conducted genotype-environment association analyses on different combinations of loci-with and without excess ancestry-and with multiple contrasts between the hybrids and parental taxa. Loci with skewed ancestry showed significant environmental associations distinguishing the hybrid lineage from one parent (C. nelsonii), whereas loci with relatively equal representation of parental ancestries showed no such environmental associations. Moreover, the overwhelming majority of candidate adaptive loci with respect to environmental gradients also had excess ancestry from a parental lineage, implying these loci have facilitated the persistence of the hybrid lineage in an environment unsuitable to at least one parent.

SPART: A versatile and standardized data exchange format for species partition information.

A wide range of data types can be used to delimit species and various computer-based tools dedicated to this task are now available. Although these formalized approaches have significantly contributed to increase the objectivity of species delimitation (SD) under different assumptions, they are not routinely used by alpha-taxonomists. One obvious shortcoming is the lack of interoperability among the various independently developed SD programs. Given the frequent incongruences between species partitions inferred by different SD approaches, researchers applying these methods often seek to compare these alternative species partitions to evaluate the robustness of the species boundaries. This procedure is excessively time consuming at present, and the lack of a standard format for species partitions is a major obstacle. Here, we propose a standardized format, SPART, to enable compatibility between different SD tools exporting or importing partitions. This format reports the partitions and describes, for each of them, the assignment of individuals to the "inferred species". The syntax also allows support values to be optionally reported, as well as original trees and the full command lines used in the respective SD analyses. Two variants of this format are proposed, overall using the same terminology but presenting the data either optimized for human readability (matricial SPART) or in a format in which each partition forms a separate block (SPART.XML). ABGD, DELINEATE, GMYC, PTP and TR2 have already been adapted to output SPART files and a new version of LIMES has been developed to import, export, merge and split them.

Geographical isolation versus dispersal: Relictual alpine grasshoppers support a model of interglacial diversification with limited hybridization.

Alpine biotas are paradigmatic of the countervailing roles of geographical isolation and dispersal during diversification. In temperate regions, repeated distributional shifts driven by Pleistocene climatic oscillations produced both recurrent pulses of population fragmentation and opportunities for gene flow during range expansions. Here, we test whether a model of divergence in isolation vs. with gene flow is more likely in the diversification of flightless alpine grasshoppers of the genus Podisma from the Iberian Peninsula. The answer to this question can also provide key insights about the pace of evolution. Specifically, if the data fit a divergence in isolation model, this suggests rapid evolution of reproductive isolation. Genomic data confirm a Pleistocene origin of the species complex, and multiple analytical approaches revealed limited asymmetric historical hybridization between two taxa. Genomic-based demographic reconstructions, spatial patterns of genetic structure and range shifts inferred from palaeodistribution modelling suggest severe range contraction accompanied by declines in effective population sizes during interglacials (i.e., contemporary populations confined to sky islands are relicts) and expansions during the coldest stages of the Pleistocene in each taxon. Although limited hybridization during secondary contact leads to phylogenetic uncertainty if gene flow is not accommodated when estimating evolutionary relationships, all species exhibit strong genetic cohesiveness. Our study lends support to the notion that the accumulation of incipient differences during periods of isolation were sufficient to lead to lineage persistence, but also that the demographic changes, dispersal constraints and spatial distribution of the sky islands themselves mediated species diversification in temperate alpine biotas.

There Is No 'Rule of Thumb': Genomic Filter Settings for a Small Plant Population to Obtain Unbiased Gene Flow Estimates.

The application of high-density polymorphic single-nucleotide polymorphisms (SNP) markers derived from high-throughput sequencing methods has heralded plenty of biological questions about the linkages of processes operating at micro- and macroevolutionary scales. However, the effects of SNP filtering practices on population genetic inference have received much less attention. By performing sensitivity analyses, we empirically investigated how decisions about the percentage of missing data (MD) and the minor allele frequency (MAF) set in bioinformatic processing of genomic data affect direct (i.e., parentage analysis) and indirect (i.e., fine-scale spatial genetic structure - SGS) gene flow estimates. We focus specifically on these manifestations in small plant populations, and particularly, in the rare tropical plant species Dinizia jueirana-facao, where assumptions implicit to analytical procedures for accurate estimates of gene flow may not hold. Avoiding biases in dispersal estimates are essential given this species is facing extinction risks due to habitat loss, and so we also investigate the effects of forest fragmentation on the accuracy of dispersal estimates under different filtering criteria by testing for recent decrease in the scale of gene flow. Our sensitivity analyses demonstrate that gene flow estimates are robust to different setting of MAF (0.05-0.35) and MD (0-20%). Comparing the direct and indirect estimates of dispersal, we find that contemporary estimates of gene dispersal distance (σ r t = 41.8 m) was ∼ fourfold smaller than the historical estimates, supporting the hypothesis of a temporal shift in the scale of gene flow in D. jueirana-facao, which is consistent with predictions based on recent, dramatic forest fragmentation process. While we identified settings for filtering genomic data to avoid biases in gene flow estimates, we stress that there is no 'rule of thumb' for bioinformatic filtering and that relying on default program settings is not advisable. Instead, we suggest that the approach implemented here be applied independently in each separate empirical study to confirm appropriate settings to obtain unbiased population genetics estimates.

Incorporating the speciation process into species delimitation.

The "multispecies" coalescent (MSC) model that underlies many genomic species-delimitation approaches is problematic because it does not distinguish between genetic structure associated with species versus that of populations within species. Consequently, as both the genomic and spatial resolution of data increases, a proliferation of artifactual species results as within-species population lineages, detected due to restrictions in gene flow, are identified as distinct species. The toll of this extends beyond systematic studies, getting magnified across the many disciplines that rely upon an accurate framework of identified species. Here we present the first of a new class of approaches that addresses this issue by incorporating an extended speciation process for species delimitation. We model the formation of population lineages and their subsequent development into independent species as separate processes and provide for a way to incorporate current understanding of the species boundaries in the system through specification of species identities of a subset of population lineages. As a result, species boundaries and within-species lineages boundaries can be discriminated across the entire system, and species identities can be assigned to the remaining lineages of unknown affinities with quantified probabilities. In addition to the identification of species units in nature, the primary goal of species delimitation, the incorporation of a speciation model also allows us insights into the links between population and species-level processes. By explicitly accounting for restrictions in gene flow not only between, but also within, species, we also address the limits of genetic data for delimiting species. Specifically, while genetic data alone is not sufficient for accurate delimitation, when considered in conjunction with other information we are able to not only learn about species boundaries, but also about the tempo of the speciation process itself.

By Animal, Water, or Wind: Can Dispersal Mode Predict Genetic Connectivity in Riverine Plant Species?

Seed dispersal is crucial to gene flow among plant populations. Although the effects of geographic distance and barriers to gene flow are well studied in many systems, it is unclear how seed dispersal mediates gene flow in conjunction with interacting effects of geographic distance and barriers. To test whether distinct seed dispersal modes (i.e., hydrochory, anemochory, and zoochory) have a consistent effect on the level of genetic connectivity (i.e., gene flow) among populations of riverine plant species, we used unlinked single-nucleotide polymorphisms (SNPs) for eight co-distributed plant species sampled across the Rio Branco, a putative biogeographic barrier in the Amazon basin. We found that animal-dispersed plant species exhibited higher levels of genetic diversity and lack of inbreeding as a result of the stronger genetic connectivity than plant species whose seeds are dispersed by water or wind. Interestingly, our results also indicated that the Rio Branco facilitates gene dispersal for all plant species analyzed, irrespective of their mode of dispersal. Even at a small spatial scale, our findings suggest that ecology rather than geography play a key role in shaping the evolutionary history of plants in the Amazon basin. These results may help improve conservation and management policies in Amazonian riparian forests, where degradation and deforestation rates are high.

Testing which axes of species differentiation underlie covariance of phylogeographic similarity among montane sedge species.

Co-distributed species may exhibit similar phylogeographic patterns due to shared environmental factors or discordant patterns attributed to the influence of species-specific traits. Although either concordant or discordant patterns could occur due to chance, stark differences in key traits (e.g., dispersal ability) may readily explain differences between species. Multiple species' attributes may affect genetic patterns, and it is difficult to isolate the contribution of each. Here we compare the relative importance of two attributes, range size, and niche breadth, in shaping the spatial structure of genetic variation in four sedge species (genus Carex) from the Rocky Mountains. Within two pairs of co-distributed species, one species exhibits narrow niche breadth, while the other species has broad niche breadth. Furthermore, one pair of co-distributed species has a large geographical distribution, while the other has a small distribution. The four species represent a natural experiment to tease apart how these attributes (i.e., range size and niche breadth) affect phylogeographic patterns. Investigations of genetic variation and structure revealed that range size, but not niche breadth, is related to spatial genetic covariation across species of montane sedges. Our study highlights how isolating key attributes across multiple species can inform their impact on processes driving intraspecific differentiation.

Differences in Quaternary co-divergence reveals community-wide diversification in the mountains of southwest China varied among species.

The mountains of southwest China (MSWC) is a biodiversity hotspot with highly complex and unusual terrain. However, with the majority of studies focusing on the biogeographic consequences of massive mountain building, the Quaternary legacy of biodiversity for the MSWC has long been overlooked. Here, we took a statistical comparative phylogeography approach to examine factors that shaped community-wide diversification. With data from 30 vertebrate species, the results reveal spatially concordant genetic structure, and temporally clustered co-divergence events associated with river barriers during severe glacial cycles. This indicates the importance of riverine barriers in the phylogeographic history of the MSWC vertebrate community. We conclude that the repeated glacial cycles are associated with co-divergences that are themselves structured by the heterogeneity of the montane landscape of the MSWC. This orderly process of diversification has profound implications for conservation by highlighting the relative independence of different geographical areas in which some, but not all species in communities have responded similarly to climate change and calls for further comparative phylogeographic investigations to reveal the connection between biological traits and divergence pulses in this biodiversity hotspot.

Using gradient Forest to predict climate response and adaptation in Cork oak.

Climate change is impacting locally adapted species such as the keystone tree species cork oak (Quercus suber L.). Quantifying the importance of environmental variables in explaining the species distribution can help build resilient populations in restoration projects and design forest management strategies. Using landscape genomics, we investigated the population structure and ecological adaptation of this tree species across the Mediterranean Basin. We applied genotyping by sequencing and derived 2,583 single nucleotide polymorphism markers genotyped from 81 individuals across 17 sites in the studied region. We implemented an approach based on the nearest neighbour haplotype 'coancestry' and uncovered a weak population structure along an east-west climatic gradient across the Mediterranean region. We identified genomic regions potentially involved in local adaptation and predicted differences in the genetic composition across the landscape under current and future climates. Variants associated with temperature and precipitation variables were detected, and we applied a nonlinear multivariate association method, gradient forest, to project these gene-environment relationships across space. The model allowed the identification of geographic areas within the western Mediterranean region most sensitive to climate change: south-western Iberia and northern Morocco. Our findings provide a preliminary assessment towards a potential management strategy for the conservation of cork oak in the Mediterranean Basin.

New species boundaries and the diversification history of marsh rat taxa clarify historical connections among ecologically and geographically distinct wetlands of South America.

Taxa with broad geographic ranges that occur in different biomes and exhibit plastic morphological traits and/or adaptations to particular habitats make inferences about species boundaries especially challenging. However, technological and conceptual advances in the generation and analysis of genomic data have advanced the description of biodiversity. Here we address the outstanding questions about the delimitation of species in the genus Holochilus, a rodent with morphological specializations to wetland habitats distributed throughoutthe South America, using genome-wide SNP and morphometric data. Specifically, we apply a Bayesian model-based species delimitation that revealed significant re-arrangements of species boundaries based on consideration of both morphometric and genomic data alone, or in combination. With these shifts in species boundaries, our results provide an insightful framework for inferring the group's biogeographic history and considering possible connections between disjoint biomes in South America. Because of the ecological constraints of the marsh rats, and with the proposed taxonomic re-arrangements, the significance of our findings extends beyond systematics and suggests how diversification might be associated with past ecological/environmental changes during the Pleistocene. Overall, this study highlights how genomic data can provide phylogenetic information for resolving relationships among species of Holochilus, but also the importance of integrative approaches to identify evolutionary independent species. For the relatively understudied vast wetlands of South America, a robust species delimitation framework therefore becomes a critical source of data relevant to hypotheses about the history of the biomes themselves.

Dispersal barriers and opportunities drive multiple levels of phylogeographic concordance in the Southern Alps of New Zealand.

Phylogeographic concordance, or the sharing of phylogeographic patterns among codistributed species, suggests similar responses to topography or climatic history. While the orientation and timing of breaks between lineages are routinely compared, spatial dynamics within regions occupied by individual lineages provide a second opportunity for comparing responses to past events. In environments with complex topography and glacial history, such as New Zealand's South Island, geographically nested comparisons can identify the processes leading to phylogeographic concordance between and within regional genomic clusters. Here, we used single nucleotide polymorphisms (obtained via ddRADseq) for two codistributed forest beetle species, Agyrtodes labralis (Leiodidae) and Brachynopus scutellaris (Staphylinidae), to evaluate the role of climate change and topography in shaping phylogeographic concordance at two, nested spatial scales: do species diverge over the same geographic barriers, with similar divergence times? And within regions delimited by these breaks, do species share similar spatial dynamics of directional expansion or isolation-by-distance? We found greater congruence of phylogeographic breaks between regions divided by the strongest dispersal barriers (i.e., the Southern Alps). However, these shared breaks were not indicative of shared spatial dynamics within the regions they delimit, and the most similar spatial dynamics between species occurred within regions with the strongest gradients in historical climatic stability. Our results indicate that lack of concordance as traditionally detected by lineage turnover does not rule out the possibility of shared histories, and variation in the presence and type of concordance may provide insights into the different processes shaping phylogeographic patterns across geologically dynamic regions.

Macroevolutionary integration of phenotypes within and across ant worker castes.

Phenotypic traits are often integrated into evolutionary modules: sets of organismal parts that evolve together. In social insect colonies, the concepts of integration and modularity apply to sets of traits both within and among functionally and phenotypically differentiated castes. On macroevolutionary timescales, patterns of integration and modularity within and across castes can be clues to the selective and ecological factors shaping their evolution and diversification. We develop a set of hypotheses describing contrasting patterns of worker integration and apply this framework in a broad (246 species) comparative analysis of major and minor worker evolution in the hyperdiverse ant genus Pheidole. Using geometric morphometrics in a phylogenetic framework, we inferred fast and tightly integrated evolution of mesosoma shape between major and minor workers, but slower and more independent evolution of head shape between the two worker castes. Thus, Pheidole workers are evolving as a mixture of intracaste and intercaste integration and rate heterogeneity. The decoupling of homologous traits across worker castes may represent an important process facilitating the rise of social complexity.

Riverscape properties contribute to the origin and structure of a hybrid zone in a Neotropical freshwater fish.

Understanding the structure of hybrid zones provides valuable insights about species boundaries and speciation, such as the evolution of barriers to gene flow and the strength of selection. In river networks, studying evolutionary processes in hybrid zones can be especially challenging, given the influence of past and current river properties along with biological species-specific traits. Here, we suggest that a natural hybrid zone between two divergent lineages of the sexually dimorphic Neotropical fish Nematocharax venustus was probably established by secondary contact as a result of a river capture event between the Contas and Pardo river basins. This putative river capture is supported by hydrogeological evidence of elbows of capture, wind gaps and geological faults. The morphological (colour pattern) and genetic (mtDNA and RADseq) variation reveal a clinal transition between parental lineages along the main river, with predominance of F2 hybrids at the centre of the hybrid zone, absence of early generation backcrosses and different levels of hybridization in the tributaries. We highlight that different sources of information are crucial for understanding how the riverscape spatial history influences the connectivity between and within river systems and, consequently, the dynamics of gene flow between freshwater lineages/species.

Incorporating interspecific interactions into phylogeographic models: A case study with Californian oaks.

It has been long assumed that abiotic factors (i.e., geography and climate) dominate the ecological and evolutionary processes underlying the distribution of species, lineages and genes at broad spatial scales and, as a result, the study of interspecific interactions has largely been overlooked in biogeography research and ignored entirely in phylogeographic inference. Here, we focus on plant-plant interactions and test whether their demographic consequences translate into broad-scale patterns of genomic variation in two Californian oak species. With our process-based analyses and statistical comparison of the likelihoods of alternative models, we show that spatial patterns of genomic variation are better explained by demographic scenarios incorporating interspecific interactions (including both competition and facilitation) than by null models that only consider heterogeneity of environmental suitability across the landscape. Collectively, our integrative approach supports the notion that the consequences of biotic interactions transcend much larger geographical and evolutionary scales than the traditional local focus.

Socially Parasitic Ants Evolve a Mosaic of Host-Matching and Parasitic Morphological Traits.

A basic expectation of evolution by natural selection is that species morphologies will adapt to their ecological niche. In social organisms, this may include selective pressure from the social environment. Many non-ant parasites of ant colonies are known to mimic the morphology of their host species, often in striking fashion [1, 2], indicating there is selection on parasite morphology to match the host (Batesian and/or Wasmannian mimicry [3]). However, ants that parasitize other ant societies are usually closely related to their hosts (Emery's rule) [4-8] and expected to be similar due to common ancestry, making any kind of mimicry difficult to detect [9]. Here, we investigate the diversification of the hyperdiverse ant genus Pheidole in Madagascar, including the evolution of 13 putative social parasite species within a broader radiation of over 100 ant species on the island. We find that the parasitic species are monophyletic and that their associated hosts are spread across the Malagasy Pheidole radiation. This provides an opportunity to test for selection on morphological similarity and divergence between parasites and hosts. Using X-ray microtomography and both linear measurements and three-dimensional (3D) geometric morphometrics, we show that ant social parasite worker morphologies feature a mix of "host-matching" and "parasitic" traits, where the former converge on the host phenotype and the latter diverge from typical Pheidole phenotypes to match a common parasitic syndrome. This finding highlights the role of social context in shaping the evolution of phenotypes and raises questions about the role of morphological sensing in nestmate recognition.

Diversification history of clown tree frogs in Neotropical rainforests (Anura, Hylidae, Dendropsophus leucophyllatus group).

General consensus emphasizes that no single biological process can explain the patterns of species' distributions and diversification in the Neotropics. Instead, the interplay of several processes across space and time must be taken into account. Here we investigated the phylogenetic relationships and biogeographic history of tree frogs in the Dendropsophus leucophyllatus species group (Amphibia: Hylidae), which is distributed across Amazonia and the Atlantic rainforests. Using Next Generation Sequencing (NGS) and double digest restriction-site associated DNA (ddRADseq), we inferred phylogenetic relationships, species limits, and temporal and geographic patterns of diversification relative to the history of these biomes. Our results indicate that the D. leucophyllatus species group includes at least 14 independent lineages, which are currently arranged into ten described species. Therefore, a significant portion of species in the group are still unnamed. Different processes were associated to the group diversification history. For instance, the Andes uplift likely caused allopatric speciation for Cis-Andean species, whereas it may also be responsible for changes in the Amazonian landscape triggering parapatric speciation by local adaptation to ecological factors. Meanwhile, Atlantic Forest ancestors unable to cross the dry diagonal biomes after rainforest's retraction, evolved in isolation into different species. Diversification in the group began in the early Miocene, when connections between Atlantic Forest and the Andes (Pacific Dominion) by way of a south corridor were possible. The historical scenario in Amazonia, characterized by several speciation events and habitat heterogeneity, helped promoting diversification, resulting in the highest species diversity for the group. This marked species diversification did not happen in Atlantic Forest, where speciation is very recent (late Pliocene and Pleistocene), despite its remarkable climatic heterogeneity.