Jonathan Q. Richmond

Speciation proceeds independently across lineages, generating varying levels of genetic divergence that are difficult to translate into discrete species boundaries. Widely used empirical heuristics such as genetic distance thresholds, DNA barcoding gaps, and measures of gene tree exclusivity provide practical tools for species delimitation, but their reliance on arbitrary cutoffs can strongly bias the number of delimited species. Here, we evaluate a coalescent-based alternative, the genealogical divergence index (gdi), which uses Bayesian estimates of divergence times, population sizes, and migration rates to explicitly quantify genealogical independence along the speciation continuum. We explore the utility of gdi by applying it to genomic data from 76 species and 113 populations of North American lizards. We test whether gdi reliably distinguishes populations from recognized species, if a biologically meaningful tipping point exists, and how empirical patterns align with commonly used species delimitation thresholds. We show that while gdi captures key features of the population–species continuum, it inconsistently separates populations from species. At the recommended species-level threshold of gdi = 0.7, the predicted probability of species status is approximately 0.5 in our test data. Among the population parameters examined, unscaled divergence (measured in substitutions per site) is the strongest predictor of species status, followed by migration rate. By conducting a quantitative review of the literature, we show that the pattern of continuous gdi variation across populations and species holds true in a more diverse set of taxa. Our results highlight the importance of considering gdi as part of a multievidence and reference-based framework for species delimitation, rather than a binary decision metric.

We report on an annotated chromosome-level genome assembly for the long-nosed leopard lizard, Gambelia wislizenii, as part of the California Conservation Genomics Project (CCGP). All 17 species of reptiles, including two turtles, seven lizards, and seven snakes targeted for reference genome sequencing by the CCGP are now complete and posted on NCBI, and this article is the third of seven CCGP lizard release papers to be published. It is also the first species of the family Crotaphytidae to have a released reference genome. Following the CCGP pipeline, the G. wislizenii genome was produced using Pacific Biosciences HiFi long reads and Omni-C proximity ligation data. The de novo assembly includes 69 scaffolds and has a total length of ~ 2.47 Gb, a scaffold N50 length of 380.1 Mb, and a BUSCO completeness score of 97.4% based on the tetrapod gene set. We improved the annotation of the genome using transcriptome sequencing (seven tissue types), identifying 23,279 genes, with BUSCO completeness of 98.9%. This reference genome, when combined with CCGP’s on-going state-wide resequencing efforts for the three species of Gambelia in California, including the federally endangered blunt-nosed leopard lizard (Gambelia sila), and Cope’s leopard lizard (Gambelia copei), will be a powerful tool enabling researchers to characterize hybridization dynamics between Gambelia species, document the remaining diversity within G. sila, and explore the genetic underpinnings of key traits that vary between the three Gambelia species, such as territoriality, sexual size dimorphism, presence versus absence of male breeding coloration, and skull morphologies.

Advances in genomic studies are revealing that gene flow between species is more frequent than previously understood, although the ways in which hybridization can bias gene flow across species boundaries or the extent to which introgression might be adaptive remain unexplored in most systems. We report on an annotated chromosome-level genome assembly for the Gilbert’s skink, Plestiodon gilberti, one of 18 clades of reptiles and amphibians selected for reference genome sequencing in the California Conservation Genomics Project. This assembly was produced using Pacific Biosciences HiFi long reads and Omni-C proximity ligation data. Although members of the Scincidae comprise nearly one-quarter of all lizard species (1785 described species), this de novo assembly represents one of only 10 skink species globally and the first North American skink with a reference genome. The assembly has a total length of ~ 1.57 Gb, a scaffold N50 length of ~ 231.32 Mb, read coverage of ~56X, and BUSCO completeness score of 97.2% based on the Tetrapoda ortholog database. Plestiodon gilberti is a member of the Plestiodon skiltonianus species complex, a group with many of the characteristics of ecological speciation but where ancient hybridization and biased introgression present challenges to retracing the initial patterns of lineage divergence. Combined with dense sampling of resequenced genomes in the California Conservation Genomics Project, including other members of the P. skiltonianus complex, this reference genome will enable future analyses of the links between divergent selection and the genes underlying speciation, as well as the potential for introgression to enable adaptation to new or changing environments.

Parallel evolution of the same reproductive isolation barrier within a taxon is an indicator of ecology’s role in speciation (i.e., parallel speciation), yet spatiotemporal variability in the efficacy of the barrier can present challenges to retracing how it evolved. Here, we revisit the evidence for a candidate example of parallel speciation in a clade of scincid lizards (the Plestiodon skiltonianus complex) using genomic data, with emphasis on determining whether hybridization may have confounded the phylogenetic signals of parallelism for this group. Our results show a striking case of genealogical discordance, in which mitochondrial loci support multiple origins of a derived large-bodied morphotype (Plestiodon gilberti) within a small-bodied ancestor (Plestiodon skiltonianus), whereas nuclear loci indicate a single origin. We attribute the discordance to separate, temporally-spaced hybridization events that led to asymmetric capture of P. skiltonianus mitochondria in different regional lineages of P. gilberti. Nuclear introgression showed a similar directional bias but was less pervasive. We demonstrate how a mechanical reproductive barrier previously identified for this group explains the asymmetry of mitochondrial introgression, given that hybrid matings are most likely when the male is P. gilberti and the female is P. skiltonianus. We then use permutation tests of morphological data to provide evidence that the mechanical barrier is less stringent in areas where hybridization is inferred to have occurred. Our results demonstrate how biased hybridization can dictate which genetic variants are transmitted between species and emphasize the importance of accounting for introgression and deep coalescence in identifying phyletic signatures of parallel speciation.

Species occupying dryland river ecosystems often experience “boom‐and‐bust” demographic cycles that coincide with shifts in habitat availability. Knowing whether declines are within natural thresholds versus those caused by acute human disturbance is critical for managing protected species. We investigated temporal shifts in abundance and habitat use of an endangered population of the threespine stickleback Gasterosteus aculeatus in southern California, where a Mediterranean climate leads to ephemeral habitat in one of the regions' least hydrologically modified rivers, the Santa Clara River. We conducted population surveys over a period of below‐average rainfall in the upper watershed in Soledad Canyon, with predefined reaches surveyed multiple times per year to capture different hydrologic conditions. Abundances were stable across years but varied significantly depending on location, with some reaches remaining dry and others drying seasonally to varying degrees. Occupancy models showed that the presence of stable perennial reaches, drying regime, and other site‐specific factors were important predictors of habitat use, and that certain reaches may be key to ensuring source‐sink dynamics as flow dissipates over the dry season. Low occupancy in two sections was driven by different predominant mechanisms, one by diel cycles of evapotranspiration and the other by cattails (Typha spp.), with both having greater effects during the hotter, drier parts of the year. As dryland river ecosystems are vulnerable to the effects of anthropogenic‐induced climate change, this study demonstrates how temporal monitoring can delimit dry‐state benchmarks for improving management interventions (i.e., translocation and habitat restoration) for protected species under conditions that are predicted to worsen in the coming years.

Bulletin of the Southern California Academy of Sciences publishes original research from all fields of science relevant to Baja and southern California.

Corrigendum: Impacts of a non-indigenous ecosystem engineer, the American beaver (Castor canadensis), in a biodiversity hotspot

Risk analysis protocols for prioritizing the management of non-native species are numerous, yet few incorporate risk and management in the same analysis or accommodate a broad diversity of taxa outside of a specific geographic area. We adapted a protocol that accounts for these factors to address non-native animal species in the Southern California/Northern Baja California Coast Ecoregion near the international border in San Diego County, an area with high indigenous biodiversity and high numbers of species of conservation concern. This stepwise, semi-quantitative protocol is applicable to any animal group in any predefined geographic area, relies on consensus-building among taxonomic experts, and has been vetted through previous use and in peer-reviewed literature. Our results show that the final prioritization was driven mainly by management feasibility, with top-ranked species having multitrophic effects that favor other non-native invaders over native residents. Conditions within the assessment area required some modification to the protocol as it was originally designed, namely a shift in emphasis from eradication to control, given that eradication is implausible for most non-native species in the assessment area. We call attention to taxon-specific issues that surfaced during the analysis, identify areas for improvement in this first-ever risk assessment for invasive animal species in the Natural Communities Conservation Plan/Habitat Conservation Plan (NCCP/HCP) reserve system of San Diego County, and provide suggestions for further refinement of the protocol. This study builds on the effort to standardize risk analysis for invasive species globally, given that many of the same invaders present threats to indigenous biodiversity worldwide.

Genome assemblies are increasingly being used to identify adaptive genetic variation that can help prioritize the population management of protected species. This approach may be particularly relevant to species like Blainville’s horned lizard, Phrynosoma blainvillii, due to its specialized diet on noxious harvester ants, numerous adaptative traits for avoiding predation (e.g., cranial horns, dorsoventrally compressed body, cryptic coloration, and blood squirting from the orbital sinuses), and status as Species of Special Concern in California. Rangewide decline since the early 20 ^th century, the basis of its conservation status, has been driven mainly by habitat conversion, over-collecting, and invasion of a non-native ant that displaces its native ant prey base. Here, we report on a scaffold-level genome assembly for P. blainvillii as part of the California Conservation Genomics Project (CCGP), produced using Pacific Biosciences HiFi long reads and Hi-C chromatin-proximity sequencing technology. The de novo assembly has 78 scaffolds, a total length of ~2.21 Gb, a scaffold N50 length of ~352 Mb, and BUSCO score of 97.4%. This is the second species of Phrynosoma for which a reference genome has been assembled and represents a considerable improvement in terms of contiguity and completeness. Combined with the landscape genomics data being compiled by the CCGP, this assembly will help strategize efforts to maintain and/or restore local genetic diversity, where interventions like genetic rescue, translocation, and strategic land preservation may be the only means by which P. blainvillii and other low vagility species can survive in the fragmented habitats of California.

Habitat loss, flood control infrastructure, and drought have left most of southern California and northern Baja California's native freshwater fish near extinction, including the endangered unarmoured threespine stickleback (Gasterosteus aculeatus williamsoni). This subspecies, an unusual morph lacking the typical lateral bony plates of theG. aculeatuscomplex, occurs at arid southern latitudes in the eastern Pacific Ocean and survives in only three inland locations. Managers have lacked molecular data to answer basic questions about the ancestry and genetic distinctiveness of unarmoured populations. These data could be used to prioritize conservation efforts. We sampledG. aculeatusfrom 36 localities and used microsatellites and whole genome data to place unarmoured populations within the broader evolutionary context ofG. aculeatusacross southern California/northern Baja California. We identified three genetic groups with none consisting solely of unarmoured populations. UnlikeG. aculeatusat northern latitudes, where Pleistocene glaciation has produced similar historical demographic profiles across populations, we found markedly different demographics depending on sampling location, with inland unarmoured populations showing steeper population declines and lower heterozygosity compared to low armoured populations in coastal lagoons. One exception involved the only high elevation population in the region, where the demography and alleles of unarmoured fish were similar to low armoured populations near the coast, exposing one of several cases of artificial translocation. Our results suggest that the current “management‐by‐phenotype” approach, based on lateral plates, is incidentally protecting the most imperilled populations; however, redirecting efforts toward evolutionary units, regardless of phenotype, may more effectively preserve adaptive potential.