Jonathan Q. Richmond

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.

Evolutionary dynamics of a rapidly receding southern range boundary in the threatened California Red‐Legged Frog (Rana draytonii)

Populations forming the edge of a species range are often imperiled by isolation and low genetic diversity, with proximity to human population centers being a major determinant of edge stability in modern landscapes. Since the 1960s, the California red‐legged frog (Rana draytonii) has undergone extensive declines in heavily urbanized southern California, where the range edge has rapidly contracted northward while shifting its cardinal orientation to an east‐west trending axis. We studied the genetic structure and diversity of these frontline populations, tested for signatures of contemporary disturbance, specifically fire, and attempted to disentangle these signals from demographic events extending deeper into the past. Consistent with the genetic expectations of the ‘abundant‐center’ model, we found that diversity, admixture, and opportunity for random mating increases in populations sampled successively further away from the range boundary. Demographic simulations indicate that bottlenecks in peripheral isolates are associated with processes extending tens to a few hundred generations in the past, despite the demographic collapse of some due to recent fire‐flood events. While the effects of recent disturbance have left little genetic imprint on these populations, they likely contribute to an extinction debt that will lead to continued range contraction unless management intervenes to stall or reverse the process.

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.

Niche divergence builds the case for ecological speciation in skinks of the Plestiodon skiltonianus species complex

Abstract Adaptation to different thermal environments has the potential to cause evolutionary changes that are sufficient to drive ecological speciation. Here, we examine whether climate‐based niche divergence in lizards of the Plestiodon skiltonianus species complex is consistent with the outcomes of such a process. Previous work on this group shows that a mechanical sexual barrier has evolved between species that differ mainly in body size and that the barrier may be a by‐product of selection for increased body size in lineages that have invaded xeric environments; however, baseline information on niche divergence among members of the group is lacking. We quantified the climatic niche using mechanistic physiological and correlative niche models and then estimated niche differences among species using ordination techniques and tests of niche overlap and equivalency. Our results show that the thermal niches of size‐divergent, reproductively isolated morphospecies are significantly differentiated and that precipitation may have been as important as temperature in causing increased shifts in body size in xeric habitats. While these findings alone do not demonstrate thermal adaptation or identify the cause of speciation, their integration with earlier genetic and behavioral studies provides a useful test of phenotype–environment associations that further support the case for ecological speciation in these lizards.

An extirpated lineage of a threatened frog species resurfaces in southern California

Southern California has experienced widespread amphibian declines since the 1960s. One species, the Vulnerable California red-legged frog Rana draytonii , is now considered to be extirpated from most of southern California. In February 2017 a population of R. draytonii was discovered in the southern foothills of the San Bernardino Mountains of Riverside County, California, near the edge of the species’ historical distribution. This population belongs to an mtDNA lineage that was presumed to be extirpated within the USA but is still extant in Baja California, Mexico. This discovery increases the potential for future, evolutionarily informed translocations within the southern portion of this species’ range in California.

Loss of dendritic connectivity in southern California's urban riverscape facilitates decline of an endemic freshwater fish

Life history adaptations and spatial configuration of metapopulation networks allow certain species to persist in extreme fluctuating environments, yet long‐term stability within these systems relies on the maintenance of linkage habitat. Degradation of such linkages in urban riverscapes can disrupt this dynamic in aquatic species, leading to increased extinction debt in local populations experiencing environment‐related demographic flux. We used microsatellites and mtDNA to examine the effects of collapsed network structure in the endemic Santa Ana sucker Catostomus santaanae of southern California, a threatened species affected by natural flood–drought cycles, “boom‐and‐bust” demography, hybridization and presumed artificial transplantation. Our results show a predominance of drift‐mediated processes in shaping population structure and that reverse mechanisms for counterbalancing the genetic effects of these phenomena have dissipated with the collapse of dendritic connectivity. We use approximate Bayesian models to support two cases of artificial transplantation and provide evidence that one of the invaded systems better represents the historic processes that maintained genetic variation within watersheds than any remaining drainages where C. santaanae is considered native. We further show that a stable dry gap in the northern range is preventing genetic dilution of pure C. santaanae persisting upstream of a hybrid assemblage involving a non‐native sucker and that local accumulation of genetic variation in the same drainage is influenced by position within the network. This work has important implications for declining species that have historically relied on dendritic metapopulation networks to maintain source–sink dynamics in phasic environments, but no longer possess this capacity in urban‐converted landscapes.

Insular biogeographic origins and high phylogenetic distinctiveness for a recently depleted lizard fauna from Christmas Island, Australia

Striking faunal turnover across Asia and Australasia, most famously along the eastern edge of the Sunda Shelf or ‘Wallaces Line’, has been a focus of biogeographic research for over 150 years. Here, we investigate the origins of a highly threatened endemic lizard fauna (four species) on Christmas Island. Despite occurring less 350 km south of the Sunda Shelf, this fauna mostly comprises species from clades centred on the more distant regions of Wallacea, the Pacific and Australia (more than 1000 km east). The three most divergent lineages show Miocene (approx. 23–5 Ma) divergences from sampled relatives; and have recently become extinct or extinct in the wild, likely owing to the recent introduction of a southeast Asian snake (Lycodon capucinus). Insular distributions, deep phylogenetic divergence and recent decline suggest that rather than dispersal ability or recent origins, environmental and biotic barriers have impeded these lineages from diversifying on the continental Sunda Shelf, and thereby, reinforced faunal differentiation across Wallaces Line. Our new phylogenetically informed perspective further highlights the rapid loss of ancient lineages that has occurred on Christmas Island, and underlines how the evolutionary divergence and vulnerability of many island-associated lineages may continue to be underestimated.

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