Nedda F. Saremi’s research while affiliated with University of California, Santa Cruz and other places

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Publications (14)


An Annotated Draft Genome for the Andean Bear, Tremarctos ornatus
  • Article
  • Full-text available

April 2021

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168 Reads

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10 Citations

Journal of Heredity

Nedda F Saremi

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Jonas Oppenheimer

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Christopher Vollmers

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[...]

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The Andean bear is the only extant member of the Tremarctine subfamily and the only extant ursid species to inhabit South America. Here, we present an annotated de novo assembly of a nuclear genome from a captive-born female Andean bear, Mischief, generated using a combination of short and long DNA and RNA reads. Our final assembly has a length of 2.23 Gb, and a scaffold N50 of 21.12 Mb, contig N50 of 23.5 kb, and BUSCO score of 88%. The Andean bear genome will be a useful resource for exploring the complex phylogenetic history of extinct and extant bear species and for future population genetics studies of Andean bears.

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Figure 2. Working model of American black bear phylogeography (A) Pre-LGM-LGM conditions, with the ice sheet extending at $21.5 kyr BP, and the hypothesized refugia to which the pre-LGM black bear population was suppressed. (B) Post-LGM conditions, with gray arrows indicating the northward recolonization of ice-free areas. See also Figures S3 and S4 and Table S2.
Figure 4. Giant short-faced bear genomic and population estimates (A) Biallelic transversion SNPs in UE1605, partitioned by read mapping (uniquely to the black bear mitochondrion, uniquely to Andean bear, or shared) and placed onto a mitochondrial Ursid tree. Lines above the black backbone lines of the tree indicate SNPs mapping uniquely to Andean bear; lines below the tree indicate mapping uniquely to black bear. The (+1) indicates a single supporting SNP in the black bear mapping leading to the Andean bear clade. (B) Phylogenetic tree and divergence times of the eight extant bear species and the extinct giant short-faced bear, as inferred from analysis of nuclear genomes. Branch lengths represent time before present (mya). The mean age of each node is shown, with 95% credibility intervals in parentheses and depicted as blue bars around each node. (C) PSMC plot for YG 546.562. See Figures S1 and S2 and Data S1.
Environmental Genomics of Late Pleistocene Black Bears and Giant Short-Faced Bears

April 2021

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716 Reads

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65 Citations

Current Biology

Analysis of ancient environmentalDNA(eDNA) has revolutionized our ability to describe biological communities in space and time, by allowing for parallel sequencing of DNA from all trophic levels. However, because environmental samples contain sparse and fragmented data from multiple individuals, and often contain closely related species, the field of ancient eDNA has so far been limited to organellar genomes in its contribution to population and phylogenetic studies. This is in contrast to data from fossils, where full-genome studies are routine, despite these being rare and their destruction for sequencing undesirable. Here, we report the retrieval of three low-coverage (0.033) environmental genomes from American black bear (Ursus americanus) and a 0.043 environmental genome of the extinct giant short-faced bear (Arctodus simus) from cave sediment samples from northern Mexico dated to 16–14 thousand calibrated years before present (cal kyr BP), which we contextualize with a new high-coverage (263) and two lower-coverage giant short-faced bear genomes obtained from fossils recovered from Yukon Territory, Canada, which date to �22–50 cal kyr BP. We show that the Late Pleistocene black bear population in Mexico is ancestrally related to the presentday Eastern American black bear population, and that the extinct giant short-faced bears present in Mexico were deeply divergent from the earlier Beringian population. Our findings demonstrate the ability to separately analyze genomic-scale DNA sequences of closely related species co-preserved in environmental samples, which brings the use of ancient eDNA into the era of population genomics and phylogenetics.


Map of dire wolf remains and morphological differentiation with wolf-like canids
a, Right, map representing the geographical range of the canid species investigated in this study. The data (shape file) for this plot were obtained from the IUCN Red List database³⁶ and plotted using R³⁷. Left, map representing the distribution of sites in the Americas where dire wolf remains (Canis dirus) have been identified (Supplementary Data 1, 2). Coloured circles represent the locations and approximate ages of the remains, with crossed circles representing the five samples from Idaho (2), Ohio (1), Tennessee (1) and Wyoming (1) that yielded sufficient endogenous DNA to reconstruct both mitochondrial genomes and low-coverage nuclear genome sequences. b, Procrustes distances between the combined mandible and M¹ shape of dire wolf and other extant canid species. Pairwise Procrustes distances were calculated by superimposing landmarks from molar and mandibular shapes between pairs of specimens and by computing the square root of the squared differences between the coordinates of corresponding landmarks, with and without correction for allometry (Supplementary Information). The centre of the box represents the median, the box bounds represent the quartiles, the whiskers represent maximum and minimum values (±1.5× the interquartile range) and dots represent outliers.
Relationships among living and extinct wolf-like canids
a, Time-scaled nuclear phylogeny generated in MCMCtree based on the best-scoring maximum likelihood species tree topology obtained from BPP and SNAPP. Values associated with nodes are mean age estimates (millions of years before present) and bars represent 95% highest posterior densities. The inset table shows the levels of support for the three possible arrangements of the dire wolf (red), the African jackals (orange) and the remaining wolf-like canids (blue) that we obtained using different analytical frameworks when including either one or both of our two highest coverage dire wolf samples (DireSP and DireGB). Although only one dire wolf branch is depicted in the tree, multiple dire wolf individuals were included in some analyses as they form a monophyletic clade (for example, Supplementary Figs. 12, 13, 15). b, Results of D-statistics used to assess the possibility of gene flow between the dire wolf and extant North American canids. Each dot represents the mean D calculated along the genome and the error bar represents 3 standard deviations computed using a weighted block jackknife procedure over 5-Mb blocks across the genome. Z values of |Z| > 3 were considered significant. These plots show that the dire wolf genomes do not share significantly more derived alleles with extant North American canids compared to Eurasian wolves (values of D were not significantly different from zero), suggesting that no hybridization occurred between the dire wolf and the ancestor of extant North American canids. Non-significant D-statistics were also obtained using an alternative reference genome and using the African wolf as P2 (Supplementary Fig. 18 and Supplementary Data 14). c, Results of D-statistics showing the existence of an ancient gene flow event between the ancestor of the dhole, Ethiopian wolf, African wolf, grey wolf and coyotes and the lineage of the dire wolf (consistently non-zero values of D regardless of P1). P1, P2 and P3 in the tree schematic represent genomes that are used in the admixture test.
Dire wolves were the last of an ancient New World canid lineage

March 2021

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2,397 Reads

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57 Citations

Nature

Dire wolves are considered to be one of the most common and widespread large carnivores in Pleistocene America¹, yet relatively little is known about their evolution or extinction. Here, to reconstruct the evolutionary history of dire wolves, we sequenced five genomes from sub-fossil remains dating from 13,000 to more than 50,000 years ago. Our results indicate that although they were similar morphologically to the extant grey wolf, dire wolves were a highly divergent lineage that split from living canids around 5.7 million years ago. In contrast to numerous examples of hybridization across Canidae2,3, there is no evidence for gene flow between dire wolves and either North American grey wolves or coyotes. This suggests that dire wolves evolved in isolation from the Pleistocene ancestors of these species. Our results also support an early New World origin of dire wolves, while the ancestors of grey wolves, coyotes and dholes evolved in Eurasia and colonized North America only relatively recently.


Figure 2. Genome Contiguity. (A) The read density map for Hi-C read pairs mapped onto the five largest contigs in our final assembly. (B) Dot plot of Hi-C scaffold assembly mapped to the dm6 reference genome. Continuous diagonal lines represent full length scaffolds of all major chromosome arms. For clarity of visualization, we restricted this plot to alignments of 5 kb or more using delta-filter in the mummerplot package.
Summary of sequencing data used for assembly and scaffolding
Sequence uniqueness strongly impacts assembly coverage
One fly-one genome: Chromosome-scale genome assembly of a single outbred Drosophila melanogaster

June 2020

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191 Reads

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32 Citations

Nucleic Acids Research

A high quality genome assembly is a vital first step for the study of an organism. Recent advances in technology have made the creation of high quality chromosome scale assemblies feasible and low cost. However, the amount of input DNA needed for an assembly project can be a limiting factor for small organisms or precious samples. Here we demonstrate the feasibility of creating a chromosome scale assembly using a hybrid method for a low input sample, a single outbred Drosophila melanogaster. Our approach combines an Illumina shotgun library, Oxford nanopore long reads, and chromosome conformation capture for long range scaffolding. This single fly genome assembly has a N50 of 26 Mb, a length that encompasses entire chromosome arms, contains 95% of expected single copy orthologs, and a nearly complete assembly of this individual's Wolbachia endosymbiont. The methods described here enable the accurate and complete assembly of genomes from small, field collected organisms as well as precious clinical samples.


Figure 2: Genome Contiguity. ​ (A) The read density map for Hi-C read pairs mapped onto the five largest contigs in our final assembly. (B) Dot plot of Hi-C scaffold assembly mapped to the dm6 reference genome. Continuous diagonal lines represent full length scaffolds of all major chromosome arms.
Chromosome-scale genome assembly of a single outbred Drosophila melanogaster

December 2019

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42 Reads

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2 Citations

A high quality genome assembly is a vital first step for the study of an organism. Recent advances in technology have made the creation of high quality chromosome scale assemblies feasible and low cost. However, the amount of input DNA needed for an assembly project can be a limiting factor for small organisms or precious samples. Here we demonstrate the feasibility of creating a chromosome scale assembly using a hybrid method for a low input sample, a single outbred Drosophila melanogaster. Our approach combines an Illumina shotgun library, Oxford nanopore long reads, and chromosome conformation capture for long range scaffolding. This single fly genome assembly has a N50 of 26 Mb, a length that encompasses entire chromosome arms, contains 95% of expected single copy orthologs, and a nearly complete assembly of this individual's Wolbachia endosymbiont. The methods described here enable the accurate and complete assembly of genomes from small, field collected organisms as well as precious clinical samples.


Author Correction: Puma genomes from North and South America provide insights into the genomic consequences of inbreeding

November 2019

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223 Reads

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16 Citations

An amendment to this paper has been published and can be accessed via a link at the top of the paper.


Fig. 1 Puma range past and present. The current range of pumas (hashed) compared to their historic range (blue). Circles denote the geographic coordinates of the puma populations sampled in this study. Panels show zoom-ins of puma habitat distribution (dark gray) within the known range of the species in the contiguous United States as predicted by the USGS 59 . Current range data are from the IUCN Red List of Threatened Species 60 . Historic range data are approximated based on prior reports 12 . Base map generated with Natural Earth
Demographic history of pumas. a Mitochondrial maximum likelihood phylogeny of the ten pumas in this study plus an additional puma from Big Cypress (KP202261.1) and the African cheetah (KP202271.1) as the outgroup. We calculated divergence times by determining the number of pairwise divergences between sequences and used a mitochondrial divergence rate of 1.15% bp per Myr7,⁵⁷. We estimate a common maternal ancestor of these pumas 278,000 ± 5,639 years ago (star; 100% bootstrap support), divergence between North American and South American mitochondrial lineages 201,000 ± 1952 years ago (pentagon; 63% bootstrap support), and a common maternal ancestor of North American pumas 21,000 ± 10,412 years ago (circle; 100% bootstrap support). b Inferred changes in effective population size (Ne) over time using the pairwise sequentially Markovian coalescent (PSMC) model²⁹ for the ten pumas. We assume a generation time of 5 years and a per generation mutation rate of 0.5e-8 per bp per generation⁶¹. The PSMC model for EVG21 shows a sharp increase in inferred Ne that is probably attributable to its hybrid ancestry³¹.
Stratification of pumas based on the geographic population. a Principal component analysis of 166,037 sites separates the sampled pumas based on population. The first component primarily separates South and North American pumas, while the second component distinguishes the variation within North America. All California pumas (Santa Cruz and Santa Monica) cluster closely. b TreeMix⁶² analysis, using the African cheetah as the outgroup, indicates the best tree separates pumas based on population and includes one migration event (weight = 0.453911) from the branch of South American diversity into the admixed Everglades puma (EVG21). c The mean of ten permuted matrices of STRUCTURE⁶³ analysis for each of K = 2 through 4, performed using CLUMPP⁶⁴. Both delta K and L(K) values indicated that K = 3 was the best K (Supplementary Fig. 10)⁶⁵.
Heterozygosity and runs of homozygosity. a Sliding window heterozygosity (black dots) and called ROH (colored boxes) across a single scaffold for three pumas from three different populations (Big Cypress, Yellowstone, and Brazil). Plots for all pumas are provided as Supplementary Fig. 12. b Average genome-wide heterozygosity versus the proportion of the genome in ROH for the ten pumas sequenced. c Distribution of lengths of ROH. The length in Mb is indicated, as is the associated expected number of generations since the individual’s maternal and paternal lineages shared a common ancestor. d Heat map showing the percent of the genomes that are in ROH that are shared IBD between pairs of pumas (Supplementary Table 6).
Puma genomes from North and South America provide insights into the genomic consequences of inbreeding

October 2019

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1,391 Reads

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82 Citations

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.



Figures
Mountain lion genomes provide insights into genetic rescue of inbred populations:

November 2018

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406 Reads

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4 Citations

Introduction paragraph/Abstract Across the geographic range of mountain lions, which includes much of North and South America, populations have become increasingly isolated due to human persecution and habitat loss. To explore the genomic consequences of these processes, we assembled a high-quality mountain lion genome and analyzed a panel of resequenced individuals from across their geographic range. We found strong geographical structure and signatures of severe inbreeding in all North American populations. Tracts of homozygosity were rarely shared among populations, suggesting that assisted gene flow would restore local genetic diversity. However, the genome of an admixed Florida panther that descended from a translocated individual from Central America had surprisingly long tracts of homozygosity, indicating that genomic gains from translocation were quickly lost by local inbreeding. Thus, to sustain diversity, genetic rescue will need to occur at regular intervals, through repeated translocations or restoring landscape connectivity. Mountain lions provide a rare opportunity to examine the potential to restore diversity through genetic rescue, and to observe the long-term effects of translocation. Our methods and results provide a framework for genome-wide analyses that can be applied to the management of small and isolated populations.



Citations (9)


... Merged reads from the shotgun libraries were mapped to the spectacled bear (Tremarctos ornatus) (GCA_028551375; Saremi et al. 2021) using PALEOMIX v.1.2.2 as described above. SAMTOOLS was used to index and generate mapping statistics for the bam files of each sample. ...

Reference:

Genetic diversity, phylogeography, and sexual dimorphism in the extinct giant short-faced bear (Arctodus simus)
An Annotated Draft Genome for the Andean Bear, Tremarctos ornatus

Journal of Heredity

... Beyond the ability to prove the presence of animals without any previous record in the cave, sedaDNA studies allowed the study of the genetic variability of the recovered animals, as previously demonstrated 24,26,80 . Specifically, sedaDNA enables two unique types of analyses that are not (or only very rarely) possible through the morphological study of remains: 1) The determination of the phenotypic/ genotypic affinities of the data in comparison with other previously published specimens, 2) The identification of population or species replacements that are not visible in the osseous remains. ...

Environmental Genomics of Late Pleistocene Black Bears and Giant Short-Faced Bears

Current Biology

... (a) A composite phylogeny showing the phylogenetic relationship of the fossil taxa included in this study to the extant Carnivora used for phylogenetic analysis. The phylogeny was derived using Hassanin et al. (2021), Perri et al. (2021), Tedford et al. (2009), Werdelin et al. 2010, Lyras (2009), and Radinsky (1973, 1975; (b) Phylogeny used in the implementation of phylogenetic generalized least squares (PGLS). PGLS was performed used the caper package (Orme et al. 2018). ...

Dire wolves were the last of an ancient New World canid lineage

Nature

... Here, we generated full-length cDNA data sets for 12 major mouse tissues from the BALB/c mouse strain. To generate over 60 million accurate full-length cDNA reads across these 12 tissues, we used the nanopore-based R2C2 long-read sequencing method (Volden et al. 2018;Byrne et al. 2019b;Adams et al. 2020;Cole et al. 2020;Vollmers et al. 2021;Volden and Vollmers 2022) which increases read accuracy and decreases length biases of ONT sequencers. We then analyzed these full-length cDNA reads with the Mandalorion isoform identification pipeline. ...

One fly-one genome: Chromosome-scale genome assembly of a single outbred Drosophila melanogaster

Nucleic Acids Research

... Alternatively, this low diversity could simply be a function of the ecological niche of A. simus. Indeed, wide-ranging, solitary carnivorans often possess low genetic diversity, e.g. the cougar (Mcrae et al. 2005, Caragiulo et al. 2014, Saremi et al. 2019, cape vulture (Kleinhans and Willows-Munro 2019), snow leopard ( Janecka et al. 2008, Aruge et al. 2019, and cheetah (Dobrynin et al. 2015, Schmidt-Küntzel et al. 2018) all have relatively low diversity, although many probably had higher diversity in the past. Notably, brown hyenas and striped hyenas-wide-ranging scavengers-also lack clear phylogeographic signals and have lower mitochondrial diversity (Rohland et al. 2005, Westbury et al. 2018, as do scavenging bird species with high dispersal capabilities, such as vultures (Kretzmann et al. 2003, Le Gouar et al. 2008, Arshad et al. 2009, Kleinhans and Willows-Munro 2019. ...

Author Correction: Puma genomes from North and South America provide insights into the genomic consequences of inbreeding

... We obtained PRNP gene sequences in silico from 21 P. concolor whole genomes following bioinformatic procedures described previously (Table 1; Ochoa et al. 2019;Saremi et al. 2019). Variable sites in the PRNP gene (accession NW_020340008.1 and region 30816895-30817651) were identified using BCFtools 1.11 (Danecek et al. 2021). ...

Puma genomes from North and South America provide insights into the genomic consequences of inbreeding

... The horses were genotyped for four previously described missenses variants [8]: rs1152296272; rs68621348; rs68621347; and rs782872967. The variant nomenclatures were updated from the original report to align with the current reference and nomenclature according to the EquCab3.0 genome [19]. Polymerase chain reactions (PCR) analyses were performed using DNA purified from the collected blood samples with specific primers designed from the transcript sequences for ENTPD1 (XM_001500628.6) and ENTPD2 (XM_023629424.1) using an online tool (BLAST, http:// blast.ncbi.nlm.nih.gov/Blast.cgi) ...

Author Correction: Improved reference genome for the domestic horse increases assembly contiguity and composition

Communications Biology

... Small population sizes and reduced connectivity place these species at risk of inbreeding and accumulating deleterious alleles. Recent studies have highlighted the presence of long runs of homozygosity in individuals from specific populations, for instance in wolves [83] and mountain lions [84]. They also highlight strategies for mitigation, including identifying source populations for assisted translocation based on sharing of homozygous tracts. ...

Mountain lion genomes provide insights into genetic rescue of inbred populations:

... The CENP-B gene sequence of horse, donkey, Grevy's zebra, and Burchell's zebra was identified in their respective genome assemblies [51,52] (Additional file 1: Table S1) and validated using both Sanger sequencing and NGS data obtained in our laboratory (Accession Bioproject: PRJNA1054998). Comparative analysis of the DNA sequences and of the deduced protein sequences revealed that CENP-B is highly conserved in the four species with only a few minor differences (Additional file 1: Table S1 and Fig. S1). ...

Improved reference genome for the domestic horse increases assembly contiguity and composition

Communications Biology