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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. 

Abstract 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: theCtenotus inornatusspecies 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 theC. inornatusspecies 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. 

Abstract 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. 

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. 

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. 

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. 

Abstract Genome-scale data have the potential to clarify phylogenetic relationships across the tree of life but have also revealed extensive gene tree conflict. This seeming paradox, whereby larger data sets both increase statistical confidence and uncover significant discordance, suggests that understanding sources of conflict is important for accurate reconstruction of evolutionary history. We explore this paradox in squamate reptiles, the vertebrate clade comprising lizards, snakes, and amphisbaenians. We collected an average of 5103 loci for 91 species of squamates that span higher-level diversity within the clade, which we augmented with publicly available sequences for an additional 17 taxa. Using a locus-by-locus approach, we evaluated support for alternative topologies at 17 contentious nodes in the phylogeny. We identified shared properties of conflicting loci, finding that rate and compositional heterogeneity drives discordance between gene trees and species tree and that conflicting loci rarely overlap across contentious nodes. Finally, by comparing our tests of nodal conflict to previous phylogenomic studies, we confidently resolve 9 of the 17 problematic nodes. We suggest this locus-by-locus and node-by-node approach can build consensus on which topological resolutions remain uncertain in phylogenomic studies of other contentious groups. [Anchored hybrid enrichment (AHE); gene tree conflict; molecular evolution; phylogenomic concordance; target capture; ultraconserved elements (UCE).]