Population genomic data reveal extreme geographic subdivision and novel conservation actions for the declining foothill yellow-legged frog

Abstract

Genomic data have the potential to inform high resolution landscape genetic and biological conservation studies that go far beyond recent mitochondrial and microsatellite analyses. We characterize the relationships of populations of the foothill yellow-legged frog, Rana boylii, a declining, "sentinel" species for stream ecosystems throughout its range in California and Oregon. We generated RADseq data and applied phylogenetic methods, hierarchical Bayesian clustering, PCA and population differentiation with admixture analyses to characterize spatial genetic structure across the species range. To facilitate direct comparison with previous analyses, we included many localities and individuals from our earlier work based on mitochondrial DNA. The results are striking, and emphasize the power of our landscape genomic approach. We recovered five extremely differentiated primary clades that indicate that R. boylii may be the most genetically differentiated anuran yet studied. Our results provide better resolution and more spatially consistent patterns than our earlier work, confirming the increased resolving power of genomic data compared to single-locus studies. Genomic structure is not equal across the species distribution. Approximately half the range of R. boylii consists of a single, relatively uniform population, while Sierra Nevada and coastal California clades are deeply, hierarchically substructured with biogeographic breaks observed in other codistributed taxa. Our results indicate that clades should serve as management units for R. boylii rather than previously suggested watershed boundaries, and that the near-extinct population from southwestern California is particularly diverged, exhibits the lowest genetic diversity, and is a critical conservation target for species recovery.

Hybridization between two parapatric ranid frog species in the northern Sierra Nevada, California, USA

“…As far as we are aware, there have been no molecular analyses across deeply divergent ranid species which occur parapatrically. Thus the high level of genetic differentiation between R. boylii and R. sierrae, as well as within species across biogeographic breaks (Macey et al, 2001;McCartney-Melstad et al, 2018) largely supports these previous studies, with the exception of a novel identification of two hybrid individuals. There remains the potential for low-levels of naturally occurring hybridization and introgression between R. boylii and R. sierrae, but currently both species appear to have clear genotypic divergence even in an area of co-occurrence.…”

“…As far as we are aware, there have been no molecular analyses across deeply divergent ranid species which occur parapatrically. Thus the high level of genetic differentiation between R. boylii and R. sierrae , as well as within species across biogeographic breaks (Macey et al, ; McCartney‐Melstad et al, ) largely supports these previous studies, with the exception of a novel identification of two hybrid individuals.…”

Whole genome duplication potentiates inter-specific hybridisation and niche shifts in Australian burrowing frogs Neobatrachus

“…The results on the changing suitable areas for the Neobatrachus species highlight the importance of continuous observation of their population dynamics. Monitoring the current status of biodiversity through collection of species occurrence data and population genetic data allows the prediction of population dynamics and hopefully timely response in conservation efforts in the face of rapidly changing environments 62,63 . Emerging methods of public engagement to collect occurrence and other data (video and audio; www.frogid.net.au) have potential to provide essential information on the state of frog species.…”

An empirical pipeline for choosing the optimal clustering threshold in RADseq studies

“…These reads represent 93 samples from 50 localities from across California and Oregon (Figure ), sequenced across two 100 bp single‐end Illumina HiSeq 2,000 lanes. For full sample information and laboratory procedures, see McCartney‐Melstad, Gidiş, et al ().…”