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Saw-scaled vipers (genus Echis) are small (up to 58 cm snout-to-vent length), venomous, eastern hemisphere snakes of the subfamily Viperinae. They are distributed across northern Africa, the Arabian Peninsula, and southwestern Asia. This group has been separated into four species complexes and twelve proposed species, however the true diversity within these groups is unclear even given numerous studies on this genus. This is partly due to uneven geographic sampling of specimens and tissue samples, overlapping distributions, and historically difficult to access species’ ranges making this genus difficult to research. Furthermore, previous studies have not used objective species delimitation approaches with either molecular or morphological data. Using recently collected tissue samples, we generate cytochrome b sequences for 24 specimens and combine these with sequences available on GenBank in order to create a time-calibrated phylogeny and estimate species level diversity using single locus species delimitation methods. We couple this with morphological analysis of specimens from the California Academy of Sciences and UC Berkeley Museum of Vertebrate Zoology collections, in order to determine if these genetically delimited species are morphologically diverged. These data can further aid in identifying specimens to species in this genus, as was demonstrated by classifying individuals to species within the Academy’s collection. 

The number of reference genomes of snakes lags behind several other vertebrate groups (e.g. birds and mammals). However, in the last two years, a concerted effort by researchers from around the world has produced new genomes of snakes representing members from several new families. Here, we present a high-quality, annotated genome of the central ratsnake (Pantherophis alleghaniensis), a member of the most diverse snake lineage, Colubroidea. Pantherophis alleghaniensis is found in the central part of the Nearctic, east of the Mississippi River. This genome was sequenced using 10X Chromium synthetic long reads and polished using Illumina short reads. The final genome assembly had an N50 of 21.82 Mb and an L50 of 22 scaffolds with a maximum scaffold length of 82.078 Mb. The genome is composed of 49.24% repeat elements dominated by long interspersed elements. We annotated this genome using transcriptome assemblies from 14 tissue types and recovered 28,368 predicted proteins. Finally, we estimated admixture proportions between two species of ratsnakes and discovered that this specimen is an admixed individual containing genomes from the western (Pantherophis obsoletus) and central ratsnakes (P. alleghaniensis). We discuss the importance of considering interspecific admixture in downstream approaches for inferring demography and phylogeny.

 

Abstract Comparisons of intraspecific genetic diversity across species can reveal the roles of geography, ecology, and life history in shaping biodiversity. The wide availability of mitochondrial DNA (mtDNA) sequences in open-access databases makes this marker practical for conducting analyses across several species in a common framework, but patterns may not be representative of overall species diversity. Here, we gather new and existing mtDNA sequences and genome-wide nuclear data (genotyping-by-sequencing; GBS) for 30 North American squamate species sampled in the Southeastern and Southwestern United States. We estimated mtDNA nucleotide diversity for 2 mtDNA genes, COI (22 species alignments; average 16 sequences) and cytb (22 species; average 58 sequences), as well as nuclear heterozygosity and nucleotide diversity from GBS data for 118 individuals (30 species; 4 individuals and 6,820 to 44,309 loci per species). We showed that nuclear genomic diversity estimates were highly consistent across individuals for some species, while other species showed large differences depending on the locality sampled. Range size was positively correlated with both cytb diversity (phylogenetically independent contrasts: R2 = 0.31, P = 0.007) and GBS diversity (R2 = 0.21; P = 0.006), while other predictors differed across the top models for each dataset. Mitochondrial and nuclear diversity estimates were not correlated within species, although sampling differences in the data available made these datasets difficult to compare. Further study of mtDNA and nuclear diversity sampled across species’ ranges is needed to evaluate the roles of geography and life history in structuring diversity across a variety of taxonomic groups. 

Abstract Despite the medical significance to humans and important ecological roles filled by vipers, few high-quality genomic resources exist for these snakes outside of a few genera of pitvipers. Here we sequence, assemble, and annotate the genome of Fea’s Viper (Azemiops feae). This taxon is distributed in East Asia and belongs to a monotypic subfamily, sister to the pitvipers. The newly sequenced genome resulted in a 1.56 Gb assembly, a contig N50 of 1.59 Mb, with 97.6% of the genome assembly in contigs >50 Kb, and a BUSCO completeness of 92.4%. We found that A. feae venom is primarily composed of phospholipase A2 (PLA2) proteins expressed by genes that likely arose from lineage-specific PLA2 gene duplications. Additionally, we show that renin, an enzyme associated with blood pressure regulation in mammals and known from the venoms of two viper species including A. feae, is expressed in the venom gland at comparative levels to known toxins and is present in the venom proteome. The cooption of this gene as a toxin may be more widespread in viperids than currently known. To investigate the historical population demographics of A. feae, we performed coalescent-based analyses and determined that the effective population size has remained stable over the last 100 kyr. This suggests Quaternary glacial cycles likely had minimal influence on the demographic history of A. feae. This newly assembled genome will be an important resource for studying the genomic basis of phenotypic evolution and understanding the diversification of venom toxin gene families. 

Species‐level taxonomy derives from empirical sources (data and techniques) that assess the existence of spatiotemporal evolutionary lineages via various species “concepts.” These concepts determine if observed lineages are independent given a particular methodology and ontology, which relates the metaphysical species concept to what “kind” of thing a species is in reality. Often, species concepts fail to link epistemology back to ontology. This lack of coherence is in part responsible for the persistence of the subspecies rank, which in modern usage often functions as a placeholder between the evolutionary events of divergence or collapse of incipient species. Thus, prospective events like lineages merging or diverging require information from unknowable future information. This is also conditioned on evidence that the lineage already has a detectably distinct evolutionary history. Ranking these lineages as subspecies can seem attractive given that many lineages do not exhibit intrinsic reproductive isolation. We argue that using subspecies is indefensible on philosophical and empirical grounds. Ontologically, the rank of subspecies is either identical to that of species or undefined in the context of evolutionary lineages representing spatiotemporally defined individuals. Some species concepts more inclined to consider subspecies, like the Biological Species Concept, are disconnected from evolutionary ontology and do not consider genealogy. Even if ontology is ignored, methods addressing reproductive isolation are often indirect and fail to capture the range of scenarios linking gene flow to species identity over space and time. The use of subspecies and reliance on reproductive isolation as a basis for an operational species concept can also conflict with ethical issues governing the protection of species. We provide a way forward for recognizing and naming species that links theoretical and operational species concepts regardless of the magnitude of reproductive isolation.

 

Genetic structure can be influenced by local adaptation to environmental heterogeneity and biogeographic barriers, resulting in discrete population clusters. Geographic distance among populations, however, can result in continuous clines of genetic divergence that appear as structured populations. Here, we evaluate the relevant importance of these three factors over a landscape characterized by environmental heterogeneity and the presence of a hypothesized biogeographic barrier in producing population genetic structure within 13 codistributed snake species using a genomic data set. We demonstrate that geographic distance and environmental heterogeneity across western North America contribute to population genomic divergence. Surprisingly, landscape features long thought to contribute to biogeographic barriers play little role in divergence community wide. Our results suggest that isolation by environment is the most important contributor to genomic divergence. Furthermore, we show that models of population clustering that incorporate spatial information consistently outperform nonspatial models, demonstrating the importance of considering geographic distances in population clustering. We argue that environmental and geographic distances as drivers of community‐wide divergence should be explored before assuming the role of biogeographic barriers.

 

Secondary sympatry amongst sister lineages is strongly associated with genetic and ecological divergence. This pattern suggests that for closely related species to coexist in secondary sympatry, they must accumulate differences in traits that mediate ecological and/or reproductive isolation. Here, we characterized inter‐ and intraspecific divergence in three giant tree frog species whose distributions stretch across West and Central Africa. Using genome‐wide single‐nucleotide polymorphism data, we demonstrated that species‐level divergence coincides temporally and geographically with a period of large‐scale forest fragmentation during the late Pliocene. Our environmental niche models further supported a dynamic history of climatic suitability and stability, and indicated that all three species occupy distinct environmental niches. We found modest morphological differentiation amongst the species with significant divergence in tympanum diameter and male advertisement call. In addition, we confirmed that two species occur in secondary sympatry in Central Africa but found no evidence of hybridization. These patterns support the hypothesis that cycles of genetic exchange and isolation across West and Central Africa have contributed to globally significant biodiversity. Furthermore, divergence in both ecology and reproductive traits appear to have played important roles in maintaining distinct lineages. At the intraspecific level, we found that climatic refugia, precipitation gradients, marine incursions, and potentially riverine barriers generated phylogeographic structure throughout the Pleistocene and into the Holocene. Further studies examining phenotypic divergence and secondary contact amongst these geographically structured populations may demonstrate how smaller scale and more recent biogeographic barriers contribute to regional diversification.