Dustin A. Wood

Novel patterns of historical isolation, dispersal, and secondary contact across Baja California in the Rosy Boa (Lichanura trivirgata)

Mitochondrial DNA (mtDNA) sequence variation was examined in 131 individuals of the Rosy Boa (Lichanura trivirgata) from across the species range in southwestern North America. Bayesian inference and nested clade phylogeographic analyses (NCPA) were used to estimate relationships and infer evolutionary processes. These patterns were evaluated as they relate to previously hypothesized vicariant events and new insights are provided into the biogeographic and evolutionary processes important in Baja California and surrounding North American deserts. Three major lineages (Lineages A, B, and C) are revealed with very little overlap. Lineage A and B are predominately separated along the Colorado River and are found primarily within California and Arizona (respectively), while Lineage C consists of disjunct groups distributed along the Baja California peninsula as well as south-central Arizona, southward along the coastal regions of Sonora, Mexico. Estimated divergence time points (using a Bayesian relaxed molecular clock) and geographic congruence with postulated vicariant events suggest early extensions of the Gulf of California and subsequent development of the Colorado River during the Late Miocene-Pliocene led to the formation of these mtDNA lineages. Our results also suggest that vicariance hypotheses alone do not fully explain patterns of genetic variation. Therefore, we highlight the importance of dispersal to explain these patterns and current distribution of populations. We also compare the mtDNA lineages with those based on morphological variation and evaluate their implications for taxonomy.

Refugial isolation and divergence in the Narrowheaded Gartersnake species complex (Thamnophis rufipunctatus) as revealed by multilocus DNA sequence data

Glacial–interglacial cycles of the Pleistocene are hypothesized as one of the foremost contributors to biological diversification. This is especially true for cold‐adapted montane species, where range shifts have had a pronounced effect on population‐level divergence. Gartersnakes of the Thamnophis rufipunctatus species complex are restricted to cold headwater streams in the highlands of the Sierra Madre Occidental and southwestern USA. We used coalescent and multilocus phylogenetic approaches to test whether genetic diversification of this montane‐restricted species complex is consistent with two prevailing models of range fluctuation for species affected by Pleistocene climate changes. Our concatenated nuDNA and multilocus species analyses recovered evidence for the persistence of multiple lineages that are restricted geographically, despite a mtDNA signature consistent with either more recent connectivity (and introgression) or recent expansion (and incomplete lineage sorting). Divergence times estimated using a relaxed molecular clock and fossil calibrations fall within the Late Pleistocene, and zero gene flow scenarios among current geographically isolated lineages could not be rejected. These results suggest that increased climate shifts in the Late Pleistocene have driven diversification and current range retraction patterns and that the differences between markers reflect the stochasticity of gene lineages (i.e. ancestral polymorphism) rather than gene flow and introgression. These results have important implications for the conservation of T. rufipunctatus (sensu novo), which is restricted to two drainage systems in the southwestern US and has undergone a recent and dramatic decline.

Testing for multiple invasion routes and source populations for the invasive brown treesnake (Boiga irregularis) on Guam: implications for pest management

The brown treesnake (Boiga irregularis) population on the Pacific island of Guam has reached iconic status as one of the most destructive invasive species of modern times, yet no published works have used genetic data to identify a source population. We used DNA sequence data from multiple genetic markers and coalescent-based phylogenetic methods to place the Guam population within the broader phylogeographic context of B. irregularis across its native range and tested whether patterns of genetic variation on the island are consistent with one or multiple introductions from different source populations. We also modeled a series of demographic scenarios that differed in the effective size and duration of a population bottleneck immediately following the invasion on Guam, and measured the fit of these simulations to the observed data using approximate Bayesian computation. Our results exclude the possibility of serial introductions from different source populations, and instead verify a single origin from the Admiralty Archipelago off the north coast of Papua New Guinea. This finding is consistent with the hypothesis that B. irregularis was accidentally transported to Guam during military relocation efforts at the end of World War II. Demographic model comparisons suggest that multiple snakes were transported to Guam from the source locality, but that fewer than 10 individuals could be responsible for establishing the population. Our results also provide evidence that low genetic diversity stemming from the founder event has not been a hindrance to the ecological success of B. irregularis on Guam, and at the same time offers a unique ‘genetic opening’ to manage snake density using classical biological approaches.

Fuzzy boundaries: color and gene flow patterns among parapatric lineages of the western shovel-nosed snake and taxonomic implication

Accurate delineation of lineage diversity is increasingly important, as species distributions are becoming more reduced and threatened. During the last century, the subspecies category was often used to denote phenotypic variation within a species range and to provide a framework for understanding lineage differentiation, often considered incipient speciation. While this category has largely fallen into disuse, previously recognized subspecies often serve as important units for conservation policy and management when other information is lacking. In this study, we evaluated phenotypic subspecies hypotheses within shovel-nosed snakes on the basis of genetic data and considered how evolutionary processes such as gene flow influenced possible incongruence between phenotypic and genetic patterns. We used both traditional phylogenetic and Bayesian clustering analyses to infer range-wide genetic structure and spatially explicit analyses to detect possible boundary locations of lineage contact. Multilocus analyses supported three historically isolated groups with low to moderate levels of contemporary gene exchange. Genetic data did not support phenotypic subspecies as exclusive groups, and we detected patterns of discordance in areas where three subspecies are presumed to be in contact. Based on genetic and phenotypic evidence, we suggested that species-level diversity is underestimated in this group and we proposed that two species be recognized, Chionactis occipitalis and C. annulata. In addition, we recommend retention of two subspecific designations within C. annulata (C. a. annulata and C. a. klauberi) that reflect regional shifts in both genetic and phenotypic variation within the species. Our results highlight the difficultly in validating taxonomic boundaries within lineages that are evolving under a time-dependent, continuous process.

Lineage diversification of fringe-toed lizards (Phrynosomatidae: Uma notata complex) in the Colorado Desert: Delimiting species in the presence of gene flow

Multi-locus nuclear DNA data were used to delimit species of fringe-toed lizards of the Uma notata complex, which are specialized for living in wind-blown sand habitats in the deserts of southwestern North America, and to infer whether Quaternary glacial cycles or Tertiary geological events were important in shaping the historical biogeography of this group. We analyzed ten nuclear loci collected using Sanger sequencing and genome-wide sequence/single-nucleotide polymorphism (SNP) data collected using restriction-associated DNA (RAD) sequencing. A combination of species discovery methods (concatenated phylogenies, parametric and non-parametric clustering algorithms) and species validation approaches (coalescent-based species tree/isolation-with-migration models) were used to delimit species, infer phylogenetic relationships, and to estimate effective population sizes, migration rates, and speciation times. Uma notata, U. inornata, U. cowlesi, and an undescribed species from Mohawk Dunes, Arizona (U. sp.) were supported as distinct in the concatenated analyses and by clustering algorithms, and all operational taxonomic units were decisively supported as distinct species by ranking hierarchical nested speciation models with Bayes factors based on coalescent-based species tree methods. However, significant unidirectional gene flow (2NM>1) from U. cowlesi and U. notata into U. rufopunctata was detected under the isolation-with-migration model. Therefore, we conservatively delimit four species-level lineages within this complex (U. inornata, U. notata, U. cowlesi, and U. sp.), treating U. rufopunctata as a hybrid population (U. notata×cowlesi). Both concatenated and coalescent-based estimates of speciation times support the hypotheses that speciation within the complex occurred during the late Pleistocene, and that the geological evolution of the Colorado River delta during this period was an important process shaping the observed phylogeographic patterns.

A century of landscape disturbance and urbanization of the San Francisco Bay region affects the present-day genetic diversity of the California Ridgway’s rail (Rallus obsoletus obsoletus)

Fragmentation and loss of natural habitat have important consequences for wild populations and can negatively affect long-term viability and resilience to environmental change. Salt marsh obligate species, such as those that occupy the San Francisco Bay Estuary in western North America, occupy already impaired habitats as result of human development and modifications and are highly susceptible to increased habitat loss and fragmentation due to global climate change. We examined the genetic variation of the California Ridgway’s rail (Rallus obsoletus obsoletus), a state and federally endangered species that occurs within the fragmented salt marsh of the San Francisco Bay Estuary. We genotyped 107 rails across 11 microsatellite loci and a single mitochondrial gene to estimate genetic diversity and population structure among seven salt marsh fragments and assessed demographic connectivity by inferring patterns of gene flow and migration rates. We found pronounced genetic structuring among four geographically separate genetic clusters across the San Francisco Bay. Gene flow analyses supported a stepping stone model of gene flow from south-to-north. However, contemporary gene flow among the regional embayments was low. Genetic diversity among occupied salt marshes and genetic clusters were not significantly different. We detected low effective population sizes and significantly high relatedness among individuals within salt marshes. Preserving genetic diversity and connectivity throughout the San Francisco Bay may require attention to salt marsh restoration in the Central Bay where habitat is both most limited and most fragmented. Incorporating periodic genetic sampling into the management regime may help evaluate population trends and guide long-term management priorities.

Persistence of historical population structure in an endangered species despite near-complete biome conversion in California's San Joaquin Desert

Genomic responses to habitat conversion can be rapid, providing wildlife managers with time‐limited opportunities to enact recovery efforts that use population connectivity information that reflects predisturbance landscapes. Despite near‐complete biome conversion, such opportunities may still exist for the endemic fauna and flora of Californias San Joaquin Desert, but comprehensive genetic data sets are lacking for nearly all species in the region. To fill this knowledge gap, we studied the rangewide population structure of the endangered blunt‐nosed leopard lizard Gambelia sila, a San Joaquin Desert endemic, using restriction site‐associated DNA (RAD), microsatellite and mtDNA data to test whether admixture patterns and estimates of effective migration surfaces (EEMS) can identify land areas with high population connectivity prior to the conversion of native xeric habitats. Clustering and phylogenetic analyses indicate a recent shared history between numerous isolated populations and EEMS reveals latent signals of corridors and barriers to gene flow over areas now replaced by agriculture and urbanization. Conflicting histories between the mtDNA and nuclear genomes are consistent with hybridization with the sister species G. wislizenii, raising important questions about where legal protection should end at the southern range limit of G. sila. Comparative analysis of different data sets also adds to a growing list of advantages in using RAD loci for genetic studies of rare species. We demonstrate how the results of this work can serve as an evolutionary guidance tool for managing endemic, arid‐adapted taxa in one of the worlds most compromised landscapes.

Historical Habitat Barriers Prevent Ring-like Genetic Continuity Throughout the Distribution of Threatened Alameda Striped Racers (Coluber lateralis euryxanthus)

Abstract:  We used microsatellites and mtDNA sequences to examine the mixed effects of geophysical, habitat, and contemporary urban barriers on the genetics of threatened Alameda Striped Racers (Coluber lateralis euryxanthus), a species with close ties to declining coastal scrub and chaparral habitat in the eastern San Francisco Bay area of California. We used cluster assignments to characterize population genetic structuring with respect to land management units and approximate Bayesian analysis to rank the ability of five alternative evolutionary hypotheses to explain the inferred structure. Then, we estimated rates of contemporary and historical migration among the major clusters and measured the fit of different historical migration models to better understand the formation of the current population structure. Our results reveal a ring-like pattern of historical connectivity around the Tri-Valley area of the East Bay (i.e., San Ramon, Amador, and Livermore valleys), with clusters largely corresponding to different management units. We found no evidence of continuous gene flow throughout the ring, however, and that the main gap in continuity is centered across the Livermore Valley. Historical migration models support higher rates of gene flow away from the terminal ends of the ring on the north and south sides of the Valley, compared with rates into those areas from western sites that border the interior San Francisco Bay. We attribute the break in ring-like connectivity to the presence of unsuitable habitat within the Livermore Valley that has been reinforced by 20th century urbanization, and the asymmetry in gene flow rates to spatial constraints on movement and east–west environmental gradients influenced by the proximity of the San Francisco Bay.

Genome-wide SNP data and morphology support the distinction of two new species of Kovarikia Soleglad, Fet & Graham, 2014 endemic to California (Scorpiones, Vaejovidae)

Abstract Morphologically conserved taxa such as scorpions represent a challenge to delimit. We recently discovered populations of scorpions in the genus Kovarikia Soleglad, Fet & Graham, 2014 on two isolated mountain ranges in southern California. We generated genome-wide single nucleotide polymorphism data and used Bayes factors species delimitation to compare alternative species delimitation scenarios which variously placed scorpions from the two localities with geographically adjacent species or into separate lineages. We also estimated a time-calibrated phylogeny of Kovarikia and examined and compared the morphology of preserved specimens from across its distribution. Genetic results strongly support the distinction of two new lineages, which we describe and name here. Morphology among the species of Kovarikia was relatively conserved, despite deep genetic divergences, consistent with recent studies of stenotopic scorpions with limited vagility. Phylogeographic structure discovered in several previously described species also suggests additional cryptic species are probably present in the genus.

Data release for persistence of historical population structure in an endangered species despite near-complete biome conversion in California s San Joaquin Desert

The recency of large-scale land conversion in California s San Joaquin Desert raises the probability that the region s numerous endemic species still retain genetic signatures of historical population connectivity. If so, genomic data can serve as a guidance tool for conserving lands that once supported habitat for gene movement. We studied the genetic structuring of the endangered blunt-nosed leopard lizard Gambelia sila, a San Joaquin Desert endemic, to (1) test whether patterns of population admixture could be used to delimit former habitat corridors in the pre-converted landscape, (2) evaluate whether restriction site associated DNA sequencing (RADseq) from a subset of samples can resolve structure at the same spatial scale as mtDNA and microsatellite data collected on the full sample, and (3) inform recovery efforts lacking direction from genetics. Cluster and tree-based analyses reveal a recent shared history between many populations that are now isolated, and that contemporary structure is linked to geophysical features that influence precipitation patterns and locations of former suitable habitat. Past hybridization with the sister species Gambelia wislizenii in southern San Joaquin Desert has generated a stable, but now-isolated population with different species identities for the mtDNA and nuclear genomes. The three marker types converged on similar themes, despite substantially fewer samples in the RADseq datasets; however, RADseq inferences were sensitive to dataset assembly filters that account for sequencing error, particularly cluster assignments. We suggest ways in which these data can be used to improve recovery efforts for G. sila and offer guidelines for RADseq dataset assembly in studies of intraspecific population structure. These data support the findings of the following publication: Richmond JQ, Wood DA, Westphal MF, et al. Persistence of historical population structure in an endangered species despite near-complete biome conversion in Californias San Joaquin Desert. Mol Ecol. 2017;00:1 19. https://doi.org/10.1111/mec.14125