Title: Puma genomes from North and South America provide insights into the genomic consequences of inbreeding
Abstract
Pumas are the most widely distributed felid in the Western Hemisphere. Increasingly, however, human persecution and habitat loss are isolating puma populations. To explore the genomic consequences of this isolation, we assemble a draft puma genome and a geographically broad panel of resequenced individuals. We estimate that the lineage leading to present-day North American pumas diverged from South American lineages 300–100 thousand years ago. We find signatures of close inbreeding in geographically isolated North American populations, but also that tracts of homozygosity are rarely shared among these populations, suggesting that assisted gene flow would restore local genetic diversity. The genome of a Florida panther descended from translocated Central American individuals has long tracts of homozygosity despite recent outbreeding. This suggests that while translocations may introduce diversity, sustaining diversity in small and isolated populations will require either repeated translocations or restoration of landscape connectivity. Our approach provides a framework for genome-wide analyses that can be applied to the management of similarly small and isolated populations.
Klingler, Kelly B.; Jahner, Joshua P.; Parchman, Thomas L.; Ray, Chris; Peacock, Mary M.(
, BMC Ecology and Evolution)
AbstractBackground
Distributional responses by alpine taxa to repeated, glacial-interglacial cycles throughout the last two million years have significantly influenced the spatial genetic structure of populations. These effects have been exacerbated for the American pika (Ochotona princeps), a small alpine lagomorph constrained by thermal sensitivity and a limited dispersal capacity. As a species of conservation concern, long-term lack of gene flow has important consequences for landscape genetic structure and levels of diversity within populations. Here, we use reduced representation sequencing (ddRADseq) to provide a genome-wide perspective on patterns of genetic variation across pika populations representing distinct subspecies. To investigate how landscape and environmental features shape genetic variation, we collected genetic samples from distinct geographic regions as well as across finer spatial scales in two geographically proximate mountain ranges of eastern Nevada.
Results
Our genome-wide analyses corroborate range-wide, mitochondrial subspecific designations and reveal pronounced fine-scale population structure between the Ruby Mountains and East Humboldt Range of eastern Nevada. Populations in Nevada were characterized by low genetic diversity (π = 0.0006–0.0009; θW = 0.0005–0.0007) relative to populations in California (π = 0.0014–0.0019; θW = 0.0011–0.0017) and the Rocky Mountains (π = 0.0025–0.0027; θW = 0.0021–0.0024), indicating substantial genetic drift in these isolated populations. Tajima’sDwas positive for all sites (D = 0.240–0.811), consistent with recent contraction in population sizesmore »range-wide.
Conclusions
Substantial influences of geography, elevation and climate variables on genetic differentiation were also detected and may interact with the regional effects of anthropogenic climate change to force the loss of unique genetic lineages through continued population extirpations in the Great Basin and Sierra Nevada.
Wilder, Aryn P; Dudchenko, Olga; Curry, Caitlin; Korody, Marisa; Turbek, Sheela P; Daly, Mark; Misuraca, Ann; Wang, Gaojianyong; Khan, Ruqayya; Weisz, David; et al(
, Genome Biology and Evolution)
Enard, David
(Ed.)
Abstract High-quality reference genomes are fundamental tools for understanding population history, and can provide estimates of genetic and demographic parameters relevant to the conservation of biodiversity. The federally endangered Pacific pocket mouse (PPM), which persists in three small, isolated populations in southern California, is a promising model for studying how demographic history shapes genetic diversity, and how diversity in turn may influence extinction risk. To facilitate these studies in PPM, we combined PacBio HiFi long reads with Omni-C and Hi-C data to generate a de novo genome assembly, and annotated the genome using RNAseq. The assembly comprised 28 chromosome-length scaffolds (N50 = 72.6 MB) and the complete mitochondrial genome, and included a long heterochromatic region on chromosome 18 not represented in the previously available short-read assembly. Heterozygosity was highly variable across the genome of the reference individual, with 18% of windows falling in runs of homozygosity (ROH) >1 MB, and nearly 9% in tracts spanning >5 MB. Yet outside of ROH, heterozygosity was relatively high (0.0027), and historical Ne estimates were large. These patterns of genetic variation suggest recent inbreeding in a formerly large population. Currently the most contiguous assembly for a heteromyid rodent, this reference genome provides insight into the past and recent demographicmore »history of the population, and will be a critical tool for management and future studies of outbreeding depression, inbreeding depression, and genetic load.« less
Shastry, Vivaswat; Bell, Katherine L.; Buerkle, C. Alex; Fordyce, James A.; Forister, Matthew L.; Gompert, Zachariah; Lebeis, Sarah L.; Lucas, Lauren K.; Marion, Zach H.; Nice, Chris C.; et al(
, G3 Genes|Genomes|Genetics)
Abstract
Infections by maternally inherited bacterial endosymbionts, especially Wolbachia, are common in insects and other invertebrates but infection dynamics across species ranges are largely under studied. Specifically, we lack a broad understanding of the origin of Wolbachia infections in novel hosts, and the historical and geographical dynamics of infections that are critical for identifying the factors governing their spread. We used Genotype-by-Sequencing data from previous population genomics studies for range-wide surveys of Wolbachia presence and genetic diversity in North American butterflies of the genus Lycaeides. As few as one sequence read identified by assembly to a Wolbachia reference genome provided high accuracy in detecting infections in host butterflies as determined by confirmatory PCR tests, and maximum accuracy was achieved with a threshold of only 5 sequence reads per host individual. Using this threshold, we detected Wolbachia in all but 2 of the 107 sampling localities spanning the continent, with infection frequencies within populations ranging from 0% to 100% of individuals, but with most localities having high infection frequencies (mean = 91% infection rate). Three major lineages of Wolbachia were identified as separate strains that appear to represent 3 separate invasions of Lycaeides butterflies by Wolbachia. Overall, we found extensive evidence for acquisitionmore »of Wolbachia through interspecific transfer between host lineages. Strain wLycC was confined to a single butterfly taxon, hybrid lineages derived from it, and closely adjacent populations in other taxa. While the other 2 strains were detected throughout the rest of the continent, strain wLycB almost always co-occurred with wLycA. Our demographic modeling suggests wLycB is a recent invasion. Within strain wLycA, the 2 most frequent haplotypes are confined almost exclusively to separate butterfly taxa with haplotype A1 observed largely in Lycaeides melissa and haplotype A2 observed most often in Lycaeides idas localities, consistent with either cladogenic mode of infection acquisition from a common ancestor or by hybridization and accompanying mutation. More than 1 major Wolbachia strain was observed in 15 localities. These results demonstrate the utility of using resequencing data from hosts to quantify Wolbachia genetic variation and infection frequency and provide evidence of multiple colonizations of novel hosts through hybridization between butterfly lineages and complex dynamics between Wolbachia strains.
Weiss-Penzias, Peter S.; Bank, Michael S.; Clifford, Deana L.; Torregrosa, Alicia; Zheng, Belle; Lin, Wendy; Wilmers, Christopher C.(
, Scientific Reports)
Abstract
Coastal marine atmospheric fog has recently been implicated as a potential source of ocean-derived monomethylmercury (MMHg) to coastal terrestrial ecosystems through the process of sea-to-land advection of foggy air masses followed by wet deposition. This study examined whether pumas (Puma concolor) in coastal central California, USA, and their associated food web, have elevated concentrations of MMHg, which could be indicative of their habitat being in a region that is regularly inundated with marine fog. We found that adult puma fur and fur-normalized whiskers in our marine fog-influenced study region had a mean (±SE) total Hg (THg) (a convenient surrogate for MMHg) concentration of 1544 ± 151 ng g−1(N = 94), which was three times higher (P < 0.01) than mean THg in comparable samples from inland areas of California (492 ± 119 ng g−1, N = 18). Pumas in California eat primarily black-tailed and/or mule deer (Odocoileus hemionus), and THg in deer fur from the two regions was also significantly different (coastal 28.1 ± 2.9, N = 55, vs. inland 15.5 ± 1.5 ng g−1, N = 40). We suggest that atmospheric deposition of MMHg through fog may be contributing to this pattern, as we also observed significantly higher MMHg concentrations in lace lichen (Ramalina menziesii), a deer food and a bioindicator of atmospheric deposition, at sites with the highest fog frequencies. Atmore »these ocean-facing sites, deer samples had significantly higher THg concentrations compared to those from more inland bay-facing sites. Our results suggest that fog-borne MMHg, while likely a small fraction of Hg in all atmospheric deposition, may contribute, disproportionately, to the bioaccumulation of Hg to levels that approach toxicological thresholds in at least one apex predator. As global mercury levels increase, coastal food webs may be at risk to the toxicological effects of increased methylmercury burdens.
Byerly, Paige A.; Chesser, R. Terry; Fleischer, Robert C.; McInerney, Nancy; Przelomska, Natalia A. S.; Leberg, Paul L.(
, Integrative and Comparative Biology)
Abstract
Connectivity among wildlife populations facilitates exchange of genetic material between groups. Changes to historical connectivity patterns resulting from anthropogenic activities can therefore have negative consequences for genetic diversity, particularly for small or isolated populations. DNA obtained from museum specimens can enable direct comparison of temporal changes in connectivity among populations, which can aid in conservation planning and contribute to the understanding of population declines. However, museum DNA can be degraded and only available in low quantities, rendering it challenging for use in population genomic analyses. Applications of genomic methodologies such as targeted sequencing address this issue by enabling capture of shared variable sites, increasing quantity and quality of recovered genomic information. We used targeted sequencing of ultra-conserved Elements (UCEs) to evaluate potential changes in connectivity and genetic diversity of roseate terns (Sterna dougallii) with a breeding distribution in the northwestern Atlantic and the Caribbean. Both populations experienced range contractions and population declines due to anthropogenic activity in the 20th century, which has the potential to alter historical connectivity regimes. Instead, we found that the two populations were differentiated historically as well as contemporaneously, with little evidence of migration between them for either time period. We also found no evidencemore »for temporal changes in genetic diversity, although these interpretations may have been limited due to sequencing artifacts caused by the degraded nature of the museum samples. Population structuring in migratory seabirds is typically reflective of low rates of divergence and high connectivity among geographically segregated subpopulations. Our contrasting results suggest the potential presence of ecological mechanisms driving population differentiation, and highlight the value of targeted sequencing on DNA derived from museum specimens to uncover long-term patterns of genetic differentiation in wildlife populations.
Saremi, Nedda F., Supple, Megan A., Byrne, Ashley, Cahill, James A., Coutinho, Luiz Lehmann, Dalén, Love, Figueiró, Henrique V., Johnson, Warren E., Milne, Heather J., O’Brien, Stephen J., O’Connell, Brendan, Onorato, David P., Riley, Seth P. D., Sikich, Jeff A., Stahler, Daniel R., Villela, Priscilla Marqui Schmidt, Vollmers, Christopher, Wayne, Robert K., Eizirik, Eduardo, Corbett-Detig, Russell B., Green, Richard E., Wilmers, Christopher C., and Shapiro, Beth. Puma genomes from North and South America provide insights into the genomic consequences of inbreeding. Nature Communications 10.1 Web. doi:10.1038/s41467-019-12741-1.
Saremi, Nedda F., Supple, Megan A., Byrne, Ashley, Cahill, James A., Coutinho, Luiz Lehmann, Dalén, Love, Figueiró, Henrique V., Johnson, Warren E., Milne, Heather J., O’Brien, Stephen J., O’Connell, Brendan, Onorato, David P., Riley, Seth P. D., Sikich, Jeff A., Stahler, Daniel R., Villela, Priscilla Marqui Schmidt, Vollmers, Christopher, Wayne, Robert K., Eizirik, Eduardo, Corbett-Detig, Russell B., Green, Richard E., Wilmers, Christopher C., & Shapiro, Beth. Puma genomes from North and South America provide insights into the genomic consequences of inbreeding. Nature Communications, 10 (1). https://doi.org/10.1038/s41467-019-12741-1
Saremi, Nedda F., Supple, Megan A., Byrne, Ashley, Cahill, James A., Coutinho, Luiz Lehmann, Dalén, Love, Figueiró, Henrique V., Johnson, Warren E., Milne, Heather J., O’Brien, Stephen J., O’Connell, Brendan, Onorato, David P., Riley, Seth P. D., Sikich, Jeff A., Stahler, Daniel R., Villela, Priscilla Marqui Schmidt, Vollmers, Christopher, Wayne, Robert K., Eizirik, Eduardo, Corbett-Detig, Russell B., Green, Richard E., Wilmers, Christopher C., and Shapiro, Beth.
"Puma genomes from North and South America provide insights into the genomic consequences of inbreeding". Nature Communications 10 (1). Country unknown/Code not available: Nature Publishing Group. https://doi.org/10.1038/s41467-019-12741-1.https://par.nsf.gov/biblio/10153543.
@article{osti_10153543,
place = {Country unknown/Code not available},
title = {Puma genomes from North and South America provide insights into the genomic consequences of inbreeding},
url = {https://par.nsf.gov/biblio/10153543},
DOI = {10.1038/s41467-019-12741-1},
abstractNote = {Abstract Pumas are the most widely distributed felid in the Western Hemisphere. Increasingly, however, human persecution and habitat loss are isolating puma populations. To explore the genomic consequences of this isolation, we assemble a draft puma genome and a geographically broad panel of resequenced individuals. We estimate that the lineage leading to present-day North American pumas diverged from South American lineages 300–100 thousand years ago. We find signatures of close inbreeding in geographically isolated North American populations, but also that tracts of homozygosity are rarely shared among these populations, suggesting that assisted gene flow would restore local genetic diversity. The genome of a Florida panther descended from translocated Central American individuals has long tracts of homozygosity despite recent outbreeding. This suggests that while translocations may introduce diversity, sustaining diversity in small and isolated populations will require either repeated translocations or restoration of landscape connectivity. Our approach provides a framework for genome-wide analyses that can be applied to the management of similarly small and isolated populations.},
journal = {Nature Communications},
volume = {10},
number = {1},
publisher = {Nature Publishing Group},
author = {Saremi, Nedda F. and Supple, Megan A. and Byrne, Ashley and Cahill, James A. and Coutinho, Luiz Lehmann and Dalén, Love and Figueiró, Henrique V. and Johnson, Warren E. and Milne, Heather J. and O’Brien, Stephen J. and O’Connell, Brendan and Onorato, David P. and Riley, Seth P. D. and Sikich, Jeff A. and Stahler, Daniel R. and Villela, Priscilla Marqui Schmidt and Vollmers, Christopher and Wayne, Robert K. and Eizirik, Eduardo and Corbett-Detig, Russell B. and Green, Richard E. and Wilmers, Christopher C. and Shapiro, Beth},
}