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Visual systems adapt to different light environments through several avenues including optical changes to the eye and neurological changes in how light signals are processed and interpreted. Spectral sensitivity can evolve via changes to visual pigments housed in the retinal photoreceptors through gene duplication and loss, differential and coexpression, and sequence evolution. Frogs provide an excellent, yet understudied, system for visual evolution research due to their diversity of ecologies (including biphasic aquatic-terrestrial life cycles) that we hypothesize imposed different selective pressures leading to adaptive evolution of the visual system, notably the opsins that encode the protein component of the visual pigments responsible for the first step in visual perception. Here, we analyze the diversity and evolution of visual opsin genes from 93 new eye transcriptomes plus published data for a combined dataset spanning 122 frog species and 34 families. We find that most species express the four visual opsins previously identified in frogs but show evidence for gene loss in two lineages. Further, we present evidence of positive selection in three opsins and shifts in selective pressures associated with differences in habitat and life history, but not activity pattern. We identify substantial novel variation in the visual opsins and, using microspectrophotometry, find highly variable spectral sensitivities, expanding known ranges for all frog visual pigments. Mutations at spectral-tuning sites only partially account for this variation, suggesting that frogs have used tuning pathways that are unique among vertebrates. These results support the hypothesis of adaptive evolution in photoreceptor physiology across the frog tree of life in response to varying environmental and ecological factors and further our growing understanding of vertebrate visual evolution.
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Opsinas , Pigmentos da Retina , Humanos , Animais , Opsinas/genética , Anuros/genética , Duplicação Gênica , MicroespectrofotometriaRESUMO
Snakes and lizards (Squamata) represent a third of terrestrial vertebrates and exhibit spectacular innovations in locomotion, feeding, and sensory processing. However, the evolutionary drivers of this radiation remain poorly known. We infer potential causes and ultimate consequences of squamate macroevolution by combining individual-based natural history observations (>60,000 animals) with a comprehensive time-calibrated phylogeny that we anchored with genomic data (5400 loci) from 1018 species. Due to shifts in the dynamics of speciation and phenotypic evolution, snakes have transformed the trophic structure of animal communities through the recurrent origin and diversification of specialized predatory strategies. Squamate biodiversity reflects a legacy of singular events that occurred during the early history of snakes and reveals the impact of historical contingency on vertebrate biodiversity.
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Evolução Biológica , Serpentes , Animais , Biodiversidade , Genômica , Lagartos/classificação , Locomoção , Filogenia , Serpentes/classificação , Serpentes/genéticaRESUMO
The iconic mountains of the Pantepui biogeographical region host many early-diverging endemic animal and plant lineages, concurring with Conan Doyle's novel about an ancient "Lost World". While this is the case of several frog lineages, others appear to have more recent origins, adding to the controversy around the diversification processes in this region. Due to its remoteness, Pantepui is challenging for biological surveys, and only a glimpse of its biodiversity has been described, which hampers comprehensive evolutionary studies in many groups. During a recent expedition to the Neblina massif on the Brazil-Venezuela border, we sampled two new frog species that could not be assigned to any known genus. Here, we perform phylogenetic analyses of mitogenomic and nuclear loci to infer the evolutionary relationships of the new taxa and support their description. We find that both species represent single lineages deeply nested within Brachycephaloidea, a major Neotropical clade of direct-developing frogs. Both species diverged >45 Ma from their closest relatives: the first is sister to all other Brachycephaloidea except for Ceuthomantis, another Pantepui endemic, and the second is sister to Brachycephalidae, endemic to the Brazilian Atlantic Forest. In addition to these considerable phylogenetic and biogeographic divergences, external morphology and osteological features support the proposition of two new family and genus-level taxa to accommodate these new branches of the amphibian tree of life. These findings add to other recently described ancient vertebrate lineages from the Neblina massif, providing a bewildering reminder that our perception of the Pantepui's biodiversity remains vastly incomplete. It also provides insights into how these mountains acted as "museums" during the diversification of Brachycephaloidea and of Neotropical biotas more broadly, in line with the influential "Plateau theory". Finally, these discoveries point at the yet unknown branches of the tree of life that may go extinct, due to global climate change and zoonotic diseases, before we even learn about their existence, amphibians living at higher elevations being particularly at risk.
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Anuros , Museus , Animais , Filogenia , Anuros/genética , Biodiversidade , Evolução BiológicaRESUMO
Genomic-scale datasets, sophisticated analytical techniques, and conceptual advances have disproportionately failed to resolve species boundaries in some groups relative to others. To understand the processes that underlie taxonomic intractability, we dissect the speciation history of an Australian lizard clade that arguably represents a "worst-case" scenario for species delimitation within vertebrates: the Ctenotus inornatus species group, a clade beset with decoupled genetic and phenotypic breaks, uncertain geographic ranges, and parallelism in purportedly diagnostic morphological characters. We sampled hundreds of localities to generate a genomic perspective on population divergence, structure, and admixture. Our results revealed rampant paraphyly of nominate taxa in the group, with lineages that are either morphologically cryptic or polytypic. Isolation-by-distance patterns reflect spatially continuous differentiation among certain pairs of putative species, yet genetic and geographic distances are decoupled in other pairs. Comparisons of mitochondrial and nuclear gene trees, tests of nuclear introgression, and historical demographic modelling identified gene flow between divergent candidate species. Levels of admixture are decoupled from phylogenetic relatedness; gene flow is often higher between sympatric species than between parapatric populations of the same species. Such idiosyncratic patterns of introgression contribute to species boundaries that are fuzzy while also varying in fuzziness. Our results suggest that "taxonomic disaster zones" like the C. inornatus species group result from spatial variation in the porosity of species boundaries and the resulting patterns of genetic and phenotypic variation. This study raises questions about the origin and persistence of hybridizing species and highlights the unique insights provided by taxa that have long eluded straightforward taxonomic categorization.
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Discordance between different genomic regions, often identified through multilocus sequencing of selected markers, presents particular difficulties in identifying historical processes which drive species diversity and boundaries. Mechanisms causing discordance, such as incomplete lineage sorting or introgression due to interspecific hybridization, are better identified based on population-level genomic datasets. In the toads of the Rhinella granulosa species group, patterns of mito-nuclear discordance and potential hybridization have been reported by several studies. However, these patterns were proposed based on few loci, such that alternative mechanisms behind gene-tree heterogeneity cannot be ruled out. Using genome-wide ddRADseq loci from a subset of species within this clade, we found only partial concordance between currently recognized species-level taxon boundaries and patterns of genetic structure. While most taxa within the R. granulosa group correspond to clades, genetic clustering analyses sometimes grouped distinct taxonomic units into a single cluster. Moreover, levels of admixture between inferred clusters were limited and restricted to a single taxon pair which is best explained by incomplete lineage sorting as opposed to introgressive hybridization, according to D-statistics results. These findings contradict previous assertions of widespread cryptic diversity and gene flow within the R. granulosa clade. Lastly, our analyses suggest that diversification events within the Rhinella granulosa group mostly dated back to the early Pliocene, being generally younger than species divergences in other closely related clades that present high levels of cross-species gene flow. This finding uniquely contradicts common assertions that this young clade of toads exhibits interspecific hybridization.
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Anuros , DNA Mitocondrial , Introgressão Genética , DNA Mitocondrial/genética , Fluxo Gênico , Genoma , Hibridização Genética , Filogenia , Anuros/genética , Comportamento Sexual , Comportamento AnimalRESUMO
The use of genome-scale data in phylogenetics has enabled recent strides in determining the relationships between taxa that are taxonomically problematic because of extensive morphological variation. Here, we employ a phylogenomic approach to infer evolutionary relationships within Ranitomeya (Anura: Dendrobatidae), an Amazonian lineage of poison frogs consisting of 16 species with remarkable diversity in color pattern, range size, and parental care behavior. We infer phylogenies with all described species of Ranitomeya from ultraconserved nuclear genomic elements (UCEs) and also estimate divergence times. Our results differ from previous analyses regarding interspecific relationships. Notably, we find that R. toraro and R. defleri are not sister species but rather distantly related, contrary to previous analyses based on smaller genetic datasets. We recover R. uakarii as paraphyletic, designate certain populations formerly assigned to R. fantastica from Peru as R. summersi, and transfer the French Guianan and eastern Brazilian R. amazonica populations to R. variabilis. By clarifying both inter- and intraspecific relationships within Ranitomeya, our study paves the way for future tests of hypotheses on color pattern evolution and historical biogeography.
Assuntos
Venenos , Animais , Anuros , Guiana Francesa , Peru , FilogeniaRESUMO
Rates of species formation vary widely across the tree of life and contribute to massive disparities in species richness among clades. This variation can emerge from differences in metapopulation-level processes that affect the rates at which lineages diverge, persist, and evolve reproductive barriers and ecological differentiation. For example, populations that evolve reproductive barriers quickly should form new species at faster rates than populations that acquire reproductive barriers more slowly. This expectation implicitly links microevolutionary processes (the evolution of populations) and macroevolutionary patterns (the profound disparity in speciation rate across taxa). Here, leveraging extensive field sampling from the Neotropical Cerrado biome in a biogeographically controlled natural experiment, we test the role of an important microevolutionary process-the propensity for population isolation-as a control on speciation rate in lizards and snakes. By quantifying population genomic structure across a set of codistributed taxa with extensive and phylogenetically independent variation in speciation rate, we show that broad-scale patterns of species formation are decoupled from demographic and genetic processes that promote the formation of population isolates. Population isolation is likely a critical stage of speciation for many taxa, but our results suggest that interspecific variability in the propensity for isolation has little influence on speciation rates. These results suggest that other stages of speciation-including the rate at which reproductive barriers evolve and the extent to which newly formed populations persist-are likely to play a larger role than population isolation in controlling speciation rate variation in squamates.
Assuntos
Evolução Biológica , Especiação Genética , Isolamento Reprodutivo , Répteis/genética , Animais , Biodiversidade , Evolução Molecular , Genética Populacional , Lagartos/classificação , Lagartos/genética , Filogenia , Filogeografia , Répteis/classificação , Serpentes/classificação , Serpentes/genéticaRESUMO
AbstractSpecies vary extensively in geographic range size and climatic niche breadth. If range limits are primarily determined by climatic factors, species with broad climatic tolerances and those that track geographically widespread climates should have large ranges. However, large ranges might increase the probability of population fragmentation and adaptive divergence, potentially decoupling climatic niche breadth and range size. Conversely, ecological generalism in large-ranged species might lead to higher gene flow across climatic transitions, increasing species' cohesion and thus decreasing genetic isolation by distance (IBD). Focusing on Australia's iconic Ctenotus lizard radiation, we ask whether species range size scales with climatic niche breadth and the degree of population isolation. To this end, we infer independently evolving operational taxonomic units (OTUs), their geographic and climatic ranges, and the strength of IBD within OTUs based on genome-wide loci from 722 individuals spanning 75 taxa. Large-ranged OTUs were common and had broader climatic niches than small-ranged OTUs; thus, large ranges do not appear to simply result from passive tracking of widespread climatic zones. OTUs with larger ranges and broader climatic niches showed relatively weaker IBD, suggesting that large-ranged species might possess intrinsic attributes that facilitate genetic cohesion across large distances and varied climates. By influencing population divergence and persistence, traits that affect species cohesion may play a central role in large-scale patterns of diversification and species richness.
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Lagartos , Animais , Austrália , Ecossistema , Fluxo Gênico , Humanos , Lagartos/genética , FilogeniaRESUMO
The effects of genetic introgression on species boundaries and how they affect species' integrity and persistence over evolutionary time have received increased attention. The increasing availability of genomic data has revealed contrasting patterns of gene flow across genomic regions, which impose challenges to inferences of evolutionary relationships and of patterns of genetic admixture across lineages. By characterizing patterns of variation across thousands of genomic loci in a widespread complex of true toads (Rhinella), we assess the true extent of genetic introgression across species thought to hybridize to extreme degrees based on natural history observations and multilocus analyses. Comprehensive geographic sampling of five large-ranged Neotropical taxa revealed multiple distinct evolutionary lineages that span large geographic areas and, at times, distinct biomes. The inferred major clades and genetic clusters largely correspond to currently recognized taxa; however, we also found evidence of cryptic diversity within taxa. While previous phylogenetic studies revealed extensive mitonuclear discordance, our genetic clustering analyses uncovered several admixed individuals within major genetic groups. Accordingly, historical demographic analyses supported that the evolutionary history of these toads involved cross-taxon gene flow both at ancient and recent times. Lastly, ABBA-BABA tests revealed widespread allele sharing across species boundaries, a pattern that can be confidently attributed to genetic introgression as opposed to incomplete lineage sorting. These results confirm previous assertions that the evolutionary history of Rhinella was characterized by various levels of hybridization even across environmentally heterogeneous regions, posing exciting questions about what factors prevent complete fusion of diverging yet highly interdependent evolutionary lineages.
Uma atenção crescente tem sido dada aos efeitos da introgressão genética nos limites das espécies e como eles afetam a integridade e a persistência das espécies ao longo do tempo evolutivo. A crescente disponibilidade de dados genômicos revelou padrões contrastantes de fluxo gênico entre regiões do genoma, o que impõe desafios às inferências de relações evolutivas e de padrões de mistura genética entre linhagens. Com base em padrões de variação em milhares de marcadores genômicos em um complexo amplamente distribuído de sapos (Rhinella), avaliamos a extensão de introgressão genética entre espécies que, acredita-se, hibridizam amplamente com base em observações de história natural e análises multi-locus. Nossa amostragem geográfica abrangente de cinco táxons neotropicais revelou várias linhagens evolutivas distintas que abrangem grandes áreas geográficas e, por vezes, biomas distintos. Os principais clados e grupos genéticos inferidos correspondem em grande parte aos táxons atualmente reconhecidos; no entanto, também encontramos evidência de diversidade críptica. De acordo com estudos filogenéticos anteriores que revelaram extensa discordância mitonuclear, nossas análises de agrupamento genético revelaram vários indivíduos geneticamente misturados. Adicionalmente, análises demográficas históricas sugerem que a história evolutiva desses sapos envolveu fluxo gênico entre táxons tanto em épocas antigas quanto recentes. Por fim, testes ABBA-BABA revelaram amplo compartilhamento de alelos entre espécies, um padrão que pode ser atribuído à introgressão genética ao invés de sorteamento incompleto de alelos entre linhagens. Esses resultados confirmam sugestões anteriores de que a história evolutiva de Rhinella foi caracterizada por vários níveis de hibridização, mesmo entre ambientes distintos, levantando questões sobre quais fatores impedem a fusão completa de linhagens evolutivas divergentes porém altamente interdependentes.
Assuntos
Bufonidae , Fluxo Gênico , Hibridização Genética , Alelos , Animais , Bufonidae/genética , Demografia , Filogenia , América do SulRESUMO
A period of isolation in allopatry typically precedes local adaptation and subsequent divergence among lineages. Alternatively, locally adapted phenotypes may arise and persist in the face of gene flow, resulting in strong correlations between ecologically-relevant phenotypic variation and corresponding environmental gradients. Quantifying genetic, ecological, and phenotypic divergence in such lineages can provide insights into the abiotic and biotic mechanisms that structure populations and drive the accumulation of phenotypic and taxonomic diversity. Low-vagility organisms whose distributions span ephemeral geographic barriers present the ideal evolutionary context within which to address these questions. Here, we combine genetic (mtDNA and genome-wide SNPs) and phenotypic data to investigate the divergence history of caecilians (Amphibia: Gymnophiona) endemic to the oceanic island of São Tomé in the Gulf of Guinea archipelago. Consistent with a previous mtDNA study, we find two phenotypically and genetically distinct lineages that occur along a north-to-south axis with extensive admixture in the centre of the island. Demographic modelling supports divergence in allopatry (~300 kya) followed by secondary contact (~95 kya). Consequently, in contrast to a morphological study that interpreted latitudinal phenotypic variation in these caecilians as a cline within a single widespread species, our analyses suggest a history of allopatric lineage divergence and subsequent hybridization that may have blurred species boundaries. We propose that late Pleistocene volcanic activity favoured allopatric divergence between these lineages with local adaptation to climate maintaining a stable hybrid zone in the centre of São Tomé Island. Our study joins a growing number of systems demonstrating lineage divergence on volcanic islands with stark environmental transitions across small geographic distances.
Um período de isolamento em alopatria geralmente precede adaptação local e divergência subsequente entre linhagens evolutivas. Alternativamente, fenótipos adaptados localmente podem surgir e persistir apesar de fluxo gênico, resultando em fortes correlações entre variação fenotípica ecologicamente relevante e os gradientes ambientais correspondentes. Quantificar divergência genética, ecológica e fenotípica em tais linhagens pode ajudar a clarificar os mecanismos abióticos e bióticos que estruturam as populações e levam ao acúmulo de diversidade fenotípica e taxonômica. Organismos de baixa vagilidade, cujas áreas de distribuição incluem barreiras geográficas efêmeras, representam um contexto evolutivo ideal para abordar essas questões. Neste estudo, combinamos dados genéticos (mtDNA e SNPs genômicos) e fenotípicos para investigar a história de divergência de cecílias endêmicas da ilha oceânica de São Tomé, no arquipélago do Golfo da Guiné. Consistentemente com um estudo anterior de mtDNA, encontramos duas linhagens fenotipicamente e geneticamente distintas que ocorrem ao longo de um eixo norte-sul, com extensa mistura genética no centro da ilha. Modelagem demográfica suportou um cenário de divergência em alopatria (~ 300 mil anos atrás) seguida de contato secundário (~ 95 mil anos atrás). Ao contrário de um estudo morfológico que interpretou a variação fenotípica latitudinal nessas cecílias como uma clina dentro de uma única espécie amplamente difundida, nossas análises sugerem uma história de divergência de linhagens em alopatria e subsequente hibridização que pode ter confundido os limites das espécies. Propomos que atividade vulcânica durante o Pleistoceno tardio favoreceu divergência alopátrica entre essas linhagens, com adaptação local ao clima mantendo uma zona híbrida estável no centro da Ilha de São Tomé. Nosso estudo se une a um número crescente de sistemas que demonstram divergência entre linhagens em ilhas vulcânicas com transições ambientais marcantes ao longo de distâncias geográficas curtas.
Assuntos
Anfíbios , Fluxo Gênico , Animais , Especiação Genética , Guiné , Ilhas , FilogeniaRESUMO
Phenotypic variation among populations, as seen in the signaling traits of many species, provides an opportunity to test whether similar factors generate repeated phenotypic patterns in different parts of a species' range. We investigated whether genetic divergence, abiotic gradients, and sympatry with closely related species explain variation in the dewlap colors of Amazon Slender Anoles, Anolis fuscoauratus. To this aim, we characterized dewlap diversity in the field with respect to population genetic structure and evolutionary relationships, assessed whether dewlap phenotypes are associated with climate or landscape variables, and tested for nonrandom associations in the distributions of A. fuscoauratus phenotypes and sympatric Anolis species. We found that dewlap colors vary among but not within sites in A. fuscoauratus. Regional genetic clusters included multiple phenotypes, while populations with similar dewlaps were often distantly related. Phenotypes did not segregate in environmental space, providing no support for optimized signal transmission at a local scale. Instead, we found a negative association between certain phenotypes and sympatric Anolis species with similar dewlap color attributes, suggesting that interactions with closely related species promoted dewlap divergence among A. fuscoauratus populations. Amazon Slender Anoles emerge as a promising system to address questions about parallel trait evolution and the contribution of signaling traits to speciation.
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Deriva Genética , Lagartos/genética , Caracteres Sexuais , Simpatria , Animais , Evolução Biológica , Clima , Meio Ambiente , Genética Populacional , Lagartos/classificação , Fenótipo , Pigmentação/genética , América do SulRESUMO
Howler monkeys (Alouatta), comprising between nine and 14 species and ranging from southern Mexico to northern Argentina, are the most widely distributed platyrrhines. Previous phylogenetic studies of howlers have used chromosomal and morphological characters and a limited number of molecular markers; however, branching patterns conflict between studies or remain unresolved. We performed a new phylogenetic analysis of Alouatta using both concatenated and coalescent-based species tree approaches based on 14 unlinked non-coding intergenic nuclear regions. Our taxon sampling included five of the seven South American species (Alouatta caraya, Alouatta belzebul, Alouatta guariba, Alouatta seniculus, Alouatta sara) and the two recognized species from Mesoamerica (Alouatta pigra, Alouatta palliata). Similarly to previous studies, our phylogenies supported a Mesoamerican clade and a South American clade. For the South American howlers, both methods recovered the Atlantic Forest endemic A. guariba as sister to all remaining South American species, albeit with moderate support. Moreover, we found no support for the previously proposed sister relationship between A. guariba and A. belzebul. For the first time, a clade composed of A. sara and A. caraya was identified. The relationships among the other South American howlers, however, were not fully supported. Our estimates for divergence times within Alouatta are generally older compared to estimates in earlier studies. However, they conform to recent studies proposing a Miocene age for the Isthmus of Panama and for the uplift of the northern Andes. Our results also point to an early genetic isolation of A. guariba in the Atlantic Forest, in agreement with the hypothesis of biotic exchange across South American rain forests in the Miocene. Collectively, these findings contribute to a better understanding of the diversification processes among howler monkey species; however, they also suggest that further comprehension of the evolutionary history of the Alouatta radiation will rely on broadened taxonomic, geographic, and genomic sampling.
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Alouatta/classificação , Evolução Biológica , Filogenia , Alouatta/genética , Animais , Análise de Sequência de DNARESUMO
In this issue of Molecular Ecology, Yamasaki et al. (2020) use genetic data from extensive sampling of Rhinogobius goby fish across the Ryukyu Archipelago in Japan to demonstrate the parallel speciation of a freshwater form from an ancestral amphidromous form. They then show that ecosystem size strongly predicts the probability of speciation between the two forms across islands. In doing so, this study connects population-level processes (microevolution) to broad-scale biodiversity patterns (macroevolution), an important but understudied link in evolutionary biology. Moving forward, we can build on this research to (a) more directly determine how geographic, ecological and historical factors influence the different stages of the speciation process, and (b) understand whether mechanisms inferred from insular radiations extend to those on continents, where both demographic histories and environmental regimes are likely more complex.
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Ecossistema , Especiação Genética , Animais , Biodiversidade , Evolução Biológica , Água Doce , Japão , ProbabilidadeRESUMO
The Amazonian poison frog genus Ameerega is one of the largest yet most understudied of the brightly colored genera in the anuran family Dendrobatidae, with 30 described species ranging throughout tropical South America. Phylogenetic analyses of Ameerega are highly discordant, lacking consistency due to variation in data types and methods, and often with limited coverage of species diversity in the genus. Here, we present a comprehensive phylogenomic reconstruction of Ameerega, utilizing state-of-the-art sequence capture techniques and phylogenetic methods. We sequenced thousands of ultraconserved elements from over 100 tissue samples, representing almost every described Ameerega species, as well as undescribed cryptic diversity. We generated topologies using maximum likelihood and coalescent methods and compared the use of maximum likelihood and Bayesian methods for estimating divergence times. Our phylogenetic inference diverged strongly from those of previous studies, and we recommend steps to bring Ameerega taxonomy in line with the new phylogeny. We place several species in a phylogeny for the first time, as well as provide evidence for six potential candidate species. We estimate that Ameerega experienced a rapid radiation approximately 7-11 million years ago and that the ancestor of all Ameerega was likely an aposematic, montane species. This study underscores the utility of phylogenomic data in improving our understanding of the phylogeny of understudied clades and making novel inferences about their evolution.
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Anuros/classificação , Animais , Anuros/genética , Teorema de Bayes , Genômica , Filogenia , América do SulRESUMO
Knowledge of how contemporary and historical factors drive patterns of genetic structure across geographic space can shed light on the processes underlying diversification. This approach is especially fruitful in studies of widespread species or species clades that occur across multiple environmental conditions and biomes. In the Neotropics, specifically, molecular data from widespread vertebrate species have revealed high levels of lineage diversity and spatial genetic structure - yet studies that explore the possible correlates of local structure patterns are lacking. We investigate the distribution of lineage diversity within two widespread South American skink species complexes of the genus Mabuya. We characterize genetic structure and diversity in these widely ranged lizards, and identify potential geographic and environmental correlates, to shed light on the processes that promote lineage diversification across the heterogeneous landscapes which they occupy. In both groups, we found mitochondrial lineages to be spatially structured along the coastal forests and the savannas of Brazil. These mtDNA patterns are, however, not shared with those inferred from nuclear DNA markers. The geographic location of major mitochondrial genetic breaks is consistent with those of other taxa, suggesting common responses to former landscape change in eastern South America, particularly along geological faults. Genetic differentiation is correlated with environmental turnover and geographic separation in one, but not in the other, group of skinks. Compared to other studies of similarly widely distributed organisms, the link between spatial environmental gradients and genetic differentiation is not as strong or consistent, suggesting a more complex history underlying current phylogeographic patterns. Our genetic data indicate the existence of yet undescribed diversity in wide-ranging lizards, and the value of phylogenetic and phylogeographic studies of similarly understudied species.
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Lagartos/classificação , Lagartos/genética , Animais , Brasil , Núcleo Celular/genética , DNA Mitocondrial/química , Ecossistema , Florestas , Estruturas Genéticas , Variação Genética , Pradaria , Filogenia , Filogeografia , Clima TropicalRESUMO
Ecological studies of species pairs showed that biotic interactions promote phenotypic change and eco-evolutionary feedbacks. However, it is unclear how phenotypes respond to synergistic interactions with multiple taxa. We investigate whether interactions with multiple prey species explain spatially structured variation in the skin toxins of the neotropical poison frog Oophaga pumilio. Specifically, we assess how dissimilarity (i.e., beta diversity) of alkaloid-bearing arthropod prey assemblages (68 ant species) and evolutionary divergence between frog populations (from a neutral genetic marker) contribute to frog poison dissimilarity (toxin profiles composed of 230 different lipophilic alkaloids sampled from 934 frogs at 46 sites). We find that models that incorporate spatial turnover in the composition of ant assemblages explain part of the frog alkaloid variation, and we infer unique alkaloid combinations across the range of O. pumilio. Moreover, we find that alkaloid variation increases weakly with the evolutionary divergence between frog populations. Our results pose two hypotheses: First, the distribution of only a few prey species may explain most of the geographic variation in poison frog alkaloids; second, different codistributed prey species may be redundant alkaloid sources. The analytical framework proposed here can be extended to other multitrophic systems, coevolutionary mosaics, microbial assemblages, and ecosystem services.
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Environmental gradients constrain physiological performance and thus species' ranges, suggesting that species occurrence in diverse environments may be associated with local adaptation. Genome-environment association analyses (GEAA) have become central for studies of local adaptation, yet they are sensitive to the spatial orientation of historical range expansions relative to landscape gradients. To test whether potentially adaptive genotypes occur in varied climates in wide-ranged species, we implemented GEAA on the basis of genomewide data from the anole lizards Anolis ortonii and Anolis punctatus, which expanded from Amazonia, presently dominated by warm and wet settings, into the cooler and less rainy Atlantic Forest. To examine whether local adaptation has been constrained by population structure and history, we estimated effective population sizes, divergence times, and gene flow under a coalescent framework. In both species, divergence between Amazonian and Atlantic Forest populations dates back to the mid-Pleistocene, with subsequent gene flow. We recovered eleven candidate genes involved with metabolism, immunity, development, and cell signaling in A. punctatus and found no loci whose frequency is associated with environmental gradients in A. ortonii. Distinct signatures of adaptation between these species are not associated with historical constraints or distinct climatic space occupancies. Similar patterns of spatial structure between selected and neutral SNPs along the climatic gradient, as supported by patterns of genetic clustering in A. punctatus, may have led to conservative GEAA performance. This study illustrates how tests of local adaptation can benefit from knowledge about species histories to support hypothesis formulation, sampling design, and landscape gradient characterization.
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Data on species ranges and phylogenetic relationships are key in historical biogeographical inference. In South America, our understanding of the evolutionary processes that underlie biodiversity patterns varies greatly across regions. Little is known, for instance, about the drivers of high endemism in the southern montane region of the Atlantic Rainforest. In this region, former biogeographic connections with other South American ecosystems have been invoked to explain the phylogenetic affinities of a number of endemic taxa. This may also be the case of the montane anole lizards Anolis nasofrontalis and A. pseudotigrinus, known from few specimens collected more than 40years ago. We combine new genetic data with published sequences of species in the Dactyloa clade of Anolis to investigate the phylogenetic relationships of A. nasofrontalis and A. pseudotigrinus, as well as estimate divergence times from their closest relatives. Based on newly sampled and previously overlooked specimens, we provide a taxonomic re-description of those two taxa. Our phylogenetic analysis recovered six main clades within Dactyloa, five of which were previously referred to as species series (aequatorialis, heterodermus, latifrons, punctatus, roquet). A sixth clade clustered A. nasofrontalis and A. pseudotigrinus with A. dissimilis from western Amazonia, A. calimae from the Andes, A. neblininus from the Guiana Shield, and two undescribed Andean taxa. We therefore define a sixth species series within Dactyloa: the neblininus series. Close phylogenetic relationships between highly disjunct, narrowly-distributed anoles suggest that patches of suitable habitat connected the southern Atlantic Forest to western South America during the Miocene, in agreement with the age of former connections between the central Andes and the Brazilian Shield as a result of Andean orogeny. The data also support the view of recurrent evolution (or loss) of a twig anole-like phenotype in mainland anoles, in apparent association with the occurrence in montane settings. Our findings stress the value of complementary genetic sampling efforts across South American countries to advance studies of mainland anole taxonomy and evolution.
Assuntos
Ecossistema , Florestas , Lagartos/fisiologia , Filogenia , Filogeografia , Animais , Oceano Atlântico , Brasil , Feminino , Lagartos/anatomia & histologia , Lagartos/genética , Masculino , Pigmentação , Fatores de TempoRESUMO
Shifts in the geographic distribution of habitats over time can promote dispersal and vicariance, thereby influencing large-scale biogeographic patterns and ecological processes. An example is that of transient corridors of suitable habitat across disjunct but ecologically similar regions, which have been associated with climate change over time. Such connections likely played a role in the assembly of tropical communities, especially within the highly diverse Amazonian and Atlantic rainforests of South America. Although these forests are presently separated by open and dry ecosystems, paleoclimatic and phylogenetic evidence suggest that they have been transiently connected in the past. However, little is known about the timing, magnitude and the distribution of former forest connections. We employ sequence data at multiple loci from three codistributed arboreal lizards (Anolis punctatus, Anolis ortonii and Polychrus marmoratus) to infer the phylogenetic relationships among Amazonian and Atlantic Forest populations and to test alternative historical demographic scenarios of colonization and vicariance using coalescent simulations and approximate Bayesian computation (ABC). Data from the better-sampled Anolis species support colonization of the Atlantic Forest from eastern Amazonia. Hierarchical ABC indicates that the three species colonized the Atlantic Forest synchronously during the mid-Pleistocene. We find support of population bottlenecks associated with founder events in the two Anolis, but not in P. marmoratus, consistently with their distinct ecological tolerances. Our findings support that climatic fluctuations provided key opportunities for dispersal and forest colonization in eastern South America through the cessation of environmental barriers. Evidence of species-specific histories strengthens assertions that biological attributes play a role in responses to shared environmental change.
Assuntos
Distribuição Animal , Lagartos/genética , Filogenia , Floresta Úmida , Animais , Teorema de Bayes , Mudança Climática , Lagartos/classificação , Modelos Genéticos , Filogeografia , Análise de Sequência de DNA , América do SulRESUMO
We apply a comparative framework to test for concerted demographic changes in response to climate shifts in the neotropical lowland forests, learning from the past to inform projections of the future. Using reduced genomic (SNP) data from three lizard species codistributed in Amazonia and the Atlantic Forest (Anolis punctatus, Anolis ortonii, and Polychrus marmoratus), we first reconstruct former population history and test for assemblage-level responses to cycles of moisture transport recently implicated in changes of forest distribution during the Late Quaternary. We find support for population shifts within the time frame of inferred precipitation fluctuations (the last 250,000 y) but detect idiosyncratic responses across species and uniformity of within-species responses across forest regions. These results are incongruent with expectations of concerted population expansion in response to increased rainfall and fail to detect out-of-phase demographic syndromes (expansions vs. contractions) across forest regions. Using reduced genomic data to infer species-specific demographical parameters, we then model the plausible spatial distribution of genetic diversity in the Atlantic Forest into future climates (2080) under a medium carbon emission trajectory. The models forecast very distinct trajectories for the lizard species, reflecting unique estimated population densities and dispersal abilities. Ecological and demographic constraints seemingly lead to distinct and asynchronous responses to climatic regimes in the tropics, even among similarly distributed taxa. Incorporating such constraints is key to improve modeling of the distribution of biodiversity in the past and future.