In reptile taxonomy, many subspecies have been described based on subtle variation in morphological traits like colour pattern and scalation. However, the subspecific rank itself has received increasing scrutiny on both conceptual and operational grounds. The species-rich (~100 species) and morphologically diverse Australian lizard genus Lerista Bell, 1833 provides opportunities to assess the evolutionary significance of subspecies taxa, given that subspecies throughout the genus were described before the widespread use of genetic-based assessments of divergence in taxonomy. Based on a combined analysis of patterns of genetic and morphological variation in Leristaplaniventralis (Lucas & Frost, 1902), we found that partitioning of populations into subspecies, namely L. p. planiventralis (Lucas & Frost, 1902), L. p. decora Storr, 1978 and L. p. maryani Storr, 1991, is unwarranted. We found negligible molecular or phenotypic divergence corresponding to those names, revealing continuous, overlapping clinal variation rather than discrete, diagnosable units. Consequently, we synonymise all three subspecies under a single, morphologically variable L. planiventralis and present its revised species-level diagnosis.
ABSTRACT We investigate the ecological and evolutionary variables that best explain spatial diversity patterns of anuran amphibians in three of South America's most diverse and geographically widespread biomes: the Cerrado, Amazonia, and Atlantic Rainforest. We used Conditional Autoregressive Models to assess the potential influence of present‐day climate (temperature and precipitation), historical climate (stability over the last 120,000 years), potential evapotranspiration (PET), and topography (slope, aspect, and rugosity) on spatial variation in taxonomic, functional, and phylogenetic diversity at a resolution of 0.5 × 0.5 degrees. Both taxonomic diversity and phylogenetic diversity increased with long‐term climatic stability in all regions. By contrast, functional diversity was negatively impacted by precipitation in the driest quarter. However, the relative importance of each predictor variable differed among diversity metrics and biomes. In the Atlantic Rainforest, potential evapotranspiration was positively correlated with functional diversity but negatively associated with taxonomic and phylogenetic diversity. In Amazonia, precipitation and relief slopes were positively associated with functional and phylogenetic diversity, respectively, whereas relief slopes were negatively correlated with taxonomic diversity. In the Cerrado, precipitation was negatively correlated with functional diversity, but climatic stability was more strongly associated with phylogenetic and taxonomic diversity. These findings indicate that present‐day climatic factors are critical in forested biomes, whereas a combination of historical and current variables is more relevant in Cerrado's savanna mosaics. Notably, ecotones exhibit significantly higher functional diversity (except for Amazon), reflecting the encounter of faunas from adjacent biomes having distinct ecological regimes and thus associated organismal traits. Characterizing the drivers of heterogeneous biodiversity distribution will offer insights into the assembly of ecological communities in other tropical and transitional ecosystems and can potentially guide conservation strategies globally.
Accurate documentation of biodiversity in the Neotropics is critical, especially as biodiversity hotspots face increasing disturbances. Taxonomic challenges arise in groups where closely related species exhibit minimal morphological variation, complicating species identification. Genomic data have proven essential for uncovering cryptic species and delineating lineages, particularly in biodiversity-rich regions like South America. In this study, we focus on the Copeoglossum nigropunctatum species group, which is widely distributed across northern South America, the Amazon rainforest, Cerrado savannas, Caatinga, and Atlantic Forest. Using a ddRADseq dataset consisting of thousands of nuclear SNPs, we delimit candidate species, clarify phylogenetic relationships, and investigate potential gene flow among lineages. Our results support three major clades (Occidental, Meridional, and Oriental) with evidence of high levels of cryptic divergence and complex genetic structure within each. We identified genetic admixture and introgressive gene flow between putative species within this group. Furthermore, our findings highlight complex species boundaries and provide a foundation for future taxonomic revisions. This study underscores the importance of large-scale genomic data in addressing complex species boundaries in tropical herpetofauna and provides new insights into the evolutionary history of Copeoglossum lizards.
Early burst patterns of speciation—the disproportionate concentration of speciation events early in the history of a radiating clade—are predicted under some models of adaptive radiation. Using time-calibrated phylogenetic trees, researchers have inferred evidence of an early burst for a wide range of organisms. However, the interpretation of these patterns can be fraught with controversy, because taxonomic and sampling biases—a phenomenon we refer to as ‘taxon murk’—can lead to apparent decelerations in the rate of speciation through time. Using Australia’s diverse sphenomorphine scincid lizards as a model, we tested whether multiple forms of tip-level uncertainty, including taxonomic undersampling and lag time for species recognition, could bias inference of speciation rates. To explore the impacts of taxon murk on diversification inference, we constructed a phylogenomic tree for 1941 individuals spanning 211 nominate species of sphenomorphines, including extensive sampling of intraspecific diversity. We found that the Australian sphenomorphine radiation is characterized by a robust early burst pattern that cannot be explained by uncertainty in the nature of tip units. These results are surprising, because extinction-mediated turnover should erode the signal of early burst speciation from molecular phylogenies. We provide a possible resolution to this paradox and consider the implications of our findings for continental radiations more generally. However, profound gaps in our knowledge of sphenomorphine behaviour and ecology limit our ability to test whether sphenomorphine macroevolutionary dynamics are consistent with paradigmatic patterns observed in better-studied radiations.
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.
The subspecies rank has been widely applied by taxonomists to capture infraspecific variation within the Linnaean classification system. Many subspecies described throughout the 20th century were recognised largely based on perceived variation in single morphological characters yet have since been found not to correspond to separately evolving population lineages, thus requiring synonymy or elevation to full species under lineage-based views of species. These modern lineage-based taxonomic resolutions have resulted from a combination of new molecular genetic techniques, improved geographical sampling of specimens, and more sophisticated analyses of morphological variation (e.g., statistical assessments rather than solely univariate descriptive ones). Here, we revisit the current taxonomic arrangement of species-level and subspecific taxa in the Lerista microtis (Gray) group, which is distributed along a narrow ~2000 km strip on the southern coast of Australia. From specimens of the L. microtis group, an additional species (Lerista arenicola) and two additional subspecies (L. m. intermedia and L. m. schwaneri) were described. We collected data on mensural, meristic, and colour pattern characters to explore morpho-spatial relationships among these taxa. Although our morphological analyses revealed some distinctiveness among specimens from locations assigned to each taxon, this variation is continuous along Australia’s southern coastline, assuming the form of a geographic cline rather than discrete forms. For many characters, however, spatial patterns were inconsistent with the original descriptions, particularly of the subspecies. Moreover, analysis of genome wide restriction-associated DNA loci revealed multiple instances of paraphyly among taxa, with phylogenetic clustering of specimens assigned to distinct species and subspecies. These emerging patterns provide no support for L. arenicola as a species evolving separately from L. microtis. Additionally, our findings challenge the presumed distinctiveness and coherence of the three subspecies of L. microtis. We thus synonymise L. arenicola and the L. microtis subspecies with L. microtis and provide a redescription of a single yet morphologically variable species—an arrangement that best reflects evolutionary history and the continuous nature of morphological variation across space.
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.
The accumulation of studies delimiting species in Amazonia has not only shed light on the patterns of its outstanding species richness but also allowed a better understanding of the processes of diversification within this immense region. Nevertheless, vast knowledge gaps remain even for prominent anuran species complexes, such as the Rhinella margaritifera species group. This clade of toads comprises 23 valid species-level taxa, mainly distributed in Amazonia but also in South America's Dry Diagonal and Atlantic and trans-Andean rainforests. Species boundaries and taxonomy in this group are notoriously complex, with studies suggesting the existence of several unnamed species. Available phylogenetic information suggests an Andean-western Amazonian origin of the group with subsequent diversification within Amazonian lowlands during the last 10 Myr and secondary dispersals into other Neotropical regions. To further test this biogeographic scenario and improve knowledge on species diversity, we used an unprecedentedly large mtDNA sampling (>800 16S sequences) across the clade's distribution and comprising all but one described species. We delimited 54 Molecular Operational Taxonomic Units, which we tested further based on patterns of variation of a nuclear locus and acoustic and morphological data. This approach confirmed the existence of at least 25 candidate species, 19 of which correspond to currently recognized taxa whereas 30 remained 'unconfirmed'. Our results clarify the taxonomic status of some species but also suggest multiple introgression events that blur some mtDNA-based species boundaries. Lastly, to provide a temporal framework for the clade's diversification, we generated a time-calibrated phylogenetic tree based on a mitogenomic matrix, which confirmed a Miocene (similar to 9 Ma) western Amazonian origin and six major clades in the group, each having initially diversified in different regions within Amazonia. Most of these clades have later dispersed throughout Amazonia during the establishment of the modern Amazonian hydrographic system, i.e., in the last 6 Myr.
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.
Many subspecies were described to capture phenotypic variation in wide-ranging taxa, with some later being found to correspond to divergent genetic lineages. We investigate whether currently recognized subspecies correspond to distinctive and coherent evolutionary lineages in the widespread Australian lizard Ctenotus pantherinus based on morphological, mitochondrial and genome-wide nuclear variation. We find weak and inconsistent correspondence between morphological patterns and the presumed subspecies ranges, with character polymorphism within regions and broad morphological overlap across regions. Phylogenetic analyses suggest paraphyly of populations assignable to each subspecies, mitonuclear discordance and little congruence between subspecies ranges and the distribution of inferred clades. Genotypic clustering supports admixture across regions. These results undermine the presumed phenotypic and genotypic coherence and distinctiveness of C. pantherinus subspecies. Based on our findings, we comment on the operational and conceptual shortcomings of morphologically defined subspecies and discuss practical challenges in applying the general notion of subspecies as incompletely separated population lineages. We conclude by highlighting a historical asymmetry that has implications for ecology, evolution and conservation: subspecies proposed in the past are difficult to falsify even in the face of new data that challenge their coherence and distinctiveness, whereas modern researchers appear hesitant to propose new subspecies.
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.
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.
Species 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.
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.
Australia harbors the most diverse lizard assemblages on Earth, yet the biodiversity of its vast arid zone remains incompletely characterized. Recent sampling of remote regions has revealed new species with unique phenotypes and unclear evolutionary affinities. Here, we describe a new species of scincid lizard that appears to be widely distributed across the Great Victoria Desert and adjacent regions. The new species was previously overlooked among specimens of the wide-ranging desert taxon Ctenotus schomburgkii but is distinguished from it by coloration and scalation characters. Phylogenetic analyses based on mitochondrial and genome-wide nuclear loci confirmed that the new species is highly divergent from C. schomburgkii, with which it appears to be sympatric across much of its range. In addition to the new species, our survey of genetic variation within C. schomburgkii as currently recognized revealed three additional lineages that approach one another in southern and northwestern Australia, and which may also represent distinct species. These results suggest that our knowledge of the extraordinary biodiversity of arid Australia remains incomplete, with implications for the conservation and management of this unique fauna. The targeted collection of voucher specimens in undersampled regions, coupled with population genetic screening of lineage diversity, will be crucial for characterizing species boundaries and understanding the composition of Australia’s vertebrate communities.
Major historical landscape changes have left significant signatures on species diversification. However, how these changes have affected the build-up and maintenance of Amazonia's megadiversity continues to be debated. Here, we addressed this issue by focusing on the evolutionary history of a pan-Amazonian toad genus that has diversified throughout the Neogene (Amazophrynella). Based on a comprehensive spatial and taxonomic sampling (286 samples, all nominal species), we delimited operational taxonomic units (OTUs) from mitochondrial DNA sequences. We delimited 35 OTUs, among which 13 correspond to nominal species, suggesting a vast underestimation of species richness. Next, we inferred time-calibrated phylogenetic relationships among OTUs based on complete mitogenomic data, which confirmed an ancient divergence between two major clades distributed in eastern and western Amazonia, respectively. Ancestral area reconstruction analyses suggest that the Andean foothills and the Brazilian Shield region represent the ancient core areas for their diversification. These two clades, probably isolated from one other by lacustrine ecosystems in western Amazonia during the Miocene, display a pattern of northward and eastward dispersals throughout the Miocene-Pliocene. Given the ecological association of Amazophrynella with non-flooded forests, our results reinforce the perception that ancient Amazonian landscape changes had a major impact on the diversification of terrestrial vertebrates.
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.
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.
Ichthyology & Herpetology (formerly Copeia) publishes work on the biology of fishes, amphibians, and reptiles, or work using those organisms as models for testing hypotheses of broad significance.