Life Sciences Commons^™

Ultracontinuous Single Haplotype Genome Assemblies For The Domestic Cat (Felis Catus) And Asian Leopard Cat (Prionailurus Bengalensis), Kevin R. Bredemeyer, Andrew J. Harris, Gang Li, Le Zhao, Nicole M. Foley, Melody E. Roelke-Parker, Stephen James O'Brien, Leslie A. Lyons, Wesley C. Warren, William J. Murphy

Biology Faculty Articles

In addition to including one of the most popular companion animals, species from the cat family Felidae serve as a powerful system for genetic analysis of inherited and infectious disease, as well as for the study of phenotypic evolution and speciation. Previous diploid-based genome assemblies for the domestic cat have served as the primary reference for genomic studies within the cat family. However, these versions suffered from poor resolution of complex and highly repetitive regions, with substantial amounts of unplaced sequence that is polymorphic or copy number variable. We sequenced the genome of a female F1 Bengal hybrid cat, the …

Urine As A High-Quality Source Of Host Genomic Dna From Wild Populations, Andrew T. Ozga, Timothy H. Webster, Ian C. Gilby, Melissa A. Wilson, Rebecca Nockerts, Michael L. Wilson, Anne Pusey, Yingying Li, Beatrice H. Hahn, Anne C. Stone

Biology Faculty Articles

The ability to generate genomic data from wild animal populations has the potential to give unprecedented insight into the population history and dynamics of species in their natural habitats. However, in the case of many species, it is impossible legally, ethically, or logistically to obtain tissues samples of high-quality necessary for genomic analyses. In this study we evaluate the success of multiple sources of genetic material (feces, urine, dentin, and dental calculus) and several capture methods (shotgun, whole-genome, exome) in generating genome-scale data in wild eastern chimpanzees (Pan troglodytes schweinfurthii) from Gombe National Park, Tanzania. We found that …

Oral Microbiome Diversity In Chimpanzees From Gombe National Park, Andrew T. Ozga, Ian C. Gilby, Rebecca Nockerts, Michael L. Wilson, Anne Pusey, Anne C. Stone

Biology Faculty Articles

Historic calcified dental plaque (dental calculus) can provide a unique perspective into the health status of past human populations but currently no studies have focused on the oral microbial ecosystem of other primates, including our closest relatives, within the hominids. Here we use ancient DNA extraction methods, shotgun library preparation, and next generation Illumina sequencing to examine oral microbiota from 19 dental calculus samples recovered from wild chimpanzees (Pan troglodytes schweinfurthii) who died in Gombe National Park, Tanzania. The resulting sequences were trimmed for quality, analyzed using MALT, MEGAN, and alignment scripts, and integrated with previously published dental …

Positive Selection Linked With Generation Of Novel Mammalian Dentition Patterns, Joao P. Machado, Siby Philip, Emanuel Maldonado, Stephen J. O'Brien, Warren E. Johnson

Biology Faculty Articles

A diverse group of genes are involved in the tooth development of mammals. Several studies, focused mainly on mice and rats, have provided a detailed depiction of the processes coordinating tooth formation and shape. Here we surveyed 236 tooth-associated genes in 39 mammalian genomes and tested for signatures of selection to assess patterns of molecular adaptation in genes regulating mammalian dentition. Of the 236 genes, 31 (∼13.1%) showed strong signatures of positive selection that may be responsible for the phenotypic diversity observed in mammalian dentition. Mammalian-specific tooth-associated genes had accelerated mutation rates compared with older genes found across all vertebrates. …

Genomic Legacy Of The African Cheetah, Acinonyx Jubatus, Pavel Dobrynin, Shiping Liu, Gaik Tamazian, Zijun Xiong, Andrey A. Yurchenko, Ksenia Krasheninnikova, Sergey Kliver, A. Schmidt-Kunzel, Klaus-Peter Koepfli, Warren E. Johnson, Lukas F. K. Kuderna, Raquel Garcia-Perez, Marc De Manuel, Ricardo Godinez, Aleksey Komissarov, Alexey Makunin, Vladimir Brukhin, Weilin Qiu, Long Zhou, Fang Li, Jian Yi, Carlos A. Driscoll, Agostinho Antunes, T. K. Oleksyk, Eduardo Eizirik, Polina Perelman, Melody E. Roelke, David E. Wildt, Mark Diekhans, Tomas Marques-Bonet, Laurie Marker, Jong Bhak, Jun Wang, Guojie Zhang, Stephen J. O'Brien

Biology Faculty Articles

Background

Patterns of genetic and genomic variance are informative in inferring population history for human, model species and endangered populations.

Results

Here the genome sequence of wild-born African cheetahs reveals extreme genomic depletion in SNV incidence, SNV density, SNVs of coding genes, MHC class I and II genes, and mitochondrial DNA SNVs. Cheetah genomes are on average 95 % homozygous compared to the genomes of the outbred domestic cat (24.08 % homozygous), Virunga Mountain Gorilla (78.12 %), inbred Abyssinian cat (62.63 %), Tasmanian devil, domestic dog and other mammalian species. Demographic estimators impute two ancestral population bottlenecks: one >100,000 years …

Intrinsic Challenges In Ancient Microbiome Reconstruction Using 16s Rrna Gene Amplification, Kirsten Ziesemer, Allison Mann, Krithivasan Sankaranarayanan, Hannes Schroeder, Andrew T. Ozga, Bernd W. Brandt, Egija Zaura, Andrea Waters-Rist, Menno Hoogland, Domingo C. Salazar-Garcia, Mark Aldenderfer, Camilla Speller, Jessica Hendy, Darlene A. Weston, Sandy J. Macdonald, Gavin H. Thomas, Matthew J. Collins, Cecil M. Lewis Jr., Corinne Hofman, Christina Warinner

Biology Faculty Articles

To date, characterization of ancient oral (dental calculus) and gut (coprolite) microbiota has been primarily accomplished through a metataxonomic approach involving targeted amplification of one or more variable regions in the 16S rRNA gene. Specifically, the V3 region (E. coli341–534) of this gene has been suggested as an excellent candidate for ancient DNA amplification and microbial community reconstruction. However, in practice this metataxonomic approach often produces highly skewed taxonomic frequency data. In this study, we use non-targeted (shotgun metagenomics) sequencing methods to better understand skewed microbial profiles observed in four ancient dental calculus specimens previously analyzed by amplicon …

Recurrent Evolution Of Melanism In South American Felids, Alexsandra Schneider, Corneliu Henegar, Kenneth Day, Devin Absher, Constanza Napolitano, Leandro Silveira, Victor A. David, Stephen J. O'Brien, Marilyn Menotti-Raymond, Gregory S. Barsh, Eduardo Eizirik

Biology Faculty Articles

Morphological variation in natural populations is a genomic test bed for studying the interface between molecular evolution and population genetics, but some of the most interesting questions involve non-model organisms that lack well annotated reference genomes. Many felid species exhibit polymorphism for melanism but the relative roles played by genetic drift, natural selection, and interspecies hybridization remain uncertain. We identify mutations of Agouti signaling protein (ASIP) or the Melanocortin 1 receptor (MC1R) as independent causes of melanism in three closely related South American species: the pampas cat (Leopardus colocolo), the kodkod (Leopardus guigna), and Geoffroy’s cat …

The Dynamic Proliferation Of Cansines Mirrors The Complex Evolution Of Feliforms, Kathryn B. Walters-Conte, Diana L. E. Johnson, Warren E. Johnson, Stephen J. O'Brien, Jill Pecon-Slattery

Biology Faculty Articles

Background: Repetitive short interspersed elements (SINEs) are retrotransposons ubiquitous in mammalian genomes and are highly informative markers to identify species and phylogenetic associations. Of these, SINEs unique to the order Carnivora (CanSINEs) yield novel insights on genome evolution in domestic dogs and cats, but less is known about their role in related carnivores. In particular, genome-wide assessment of CanSINE evolution has yet to be completed across the Feliformia (cat-like) suborder of Carnivora. Within Feliformia, the cat family Felidae is composed of 37 species and numerous subspecies organized into eight monophyletic lineages that likely arose 10 million years ago. Using …

Synthesizing Larval Competence Dynamics And Reef-Scale Retention Reveals A High Potential For Self-Recruitment In Corals, Joana Figueiredo, Andrew H. Baird, Sean R. Connolly

Marine & Environmental Sciences Faculty Articles

Many organisms have a complex life-cycle in which dispersal occurs at the propagule stage. For marine environments, there is growing evidence that high levels of recruitment back to the natal population (self-recruitment) are common in many marine organisms. For fish, swimming behavior is frequently invoked as a key mechanism allowing high self-recruitment. For organisms with weak-swimming larvae, such as many marine invertebrates, the mechanisms behind self-recruitment are less clear. Here, we assessed whether the combination of passive retention of larvae due to re-circulation processes near reefs, and the dynamics of settlement competence, can produce the high levels of self-recruitment previously …

The Role Of Gene Duplication And Unconstrained Selective Pressures In The Melanopsin Gene Family Evolution And Vertebrate Circadian Rhythm Regulation, Rui Borges, Warren E. Johnson, Stephen J. O'Brien, Vitor Vasconcelos, Agostinho Antunes

Biology Faculty Articles

Melanopsin is a photosensitive cell protein involved in regulating circadian rhythms and other non-visual responses to light. The melanopsin gene family is represented by two paralogs,OPN4x and OPN4m, which originated through gene duplication early in the emergence of vertebrates. Here we studied the melanopsin gene family using an integrated gene/protein evolutionary approach, which revealed that the rhabdomeric urbilaterian ancestor had the same amino acid patterns (DRY motif and the Y and E conterions) as extant vertebrate species, suggesting that the mechanism for light detection and regulation is similar to rhabdomeric rhodopsins. Both OPN4m and OPN4x paralogs are found …

Evolution Of A Major Drug Metabolizing Enzyme Defect In The Domestic Cat And Other Felidae: Phylogenetic Timing And The Role Of Hypercarnivory, Binu Shrestha, J. Michael Reed, Philip T. Starks, Gretchen E. Kaufman, Jared V. Goldstone, Melody E. Roelke, Stephen J. O'Brien, Klaus-Peter Koepfli, Laurence Frank, Michael H. Court

Biology Faculty Articles

The domestic cat (Felis catus) shows remarkable sensitivity to the adverse effects of phenolic drugs, including acetaminophen and aspirin, as well as structurally-related toxicants found in the diet and environment. This idiosyncrasy results from pseudogenization of the gene encoding UDP-glucuronosyltransferase (UGT) 1A6, the major species-conserved phenol detoxification enzyme. Here, we established the phylogenetic timing of disruptive UGT1A6 mutations and explored the hypothesis that gene inactivation in cats was enabled by minimal exposure to plant-derived toxicants. Fixation of the UGT1A6 pseudogene was estimated to have occurred between 35 and 11 million years ago with all extant Felidae having dysfunctional …

A Molecular Phylogeny Of Living Primates, Polina L. Perelman, Warren E. Johnson, Christian Roos, Hector Seuanez, Julie E. Horvath, Miguel A. M. Moreira, Bailey Kessing, J. U. Pontius, Melody E. Roelke, Yves Rumpler, Maria P. C. Schneider, Artur Silva, Stephen J. O'Brien, Jill Pecon-Slattery

Biology Faculty Articles

Comparative genomic analyses of primates offer considerable potential to define and understand the processes that mold, shape, and transform the human genome. However, primate taxonomy is both complex and controversial, with marginal unifying consensus of the evolutionary hierarchy of extant primate species. Here we provide new genomic sequence (~8 Mb) from 186 primates representing 61 (~90%) of the described genera, and we include outgroup species from Dermoptera, Scandentia, and Lagomorpha. The resultant phylogeny is exceptionally robust and illuminates events in primate evolution from ancient to recent, clarifying numerous taxonomic controversies and providing new data on human evolution. Ongoing speciation, reticulate …

Genome-Wide Characterization Of Centromeric Satellites From Multiple Mammalian Genomes, Can Alkan, Maria Francesca Cardone, Claudia Rita Catacchio, Francesca Antonacci, Stephen J. O'Brien, Oliver A. Ryder, Stefania Purgato, Monica Zoli, Evan E. Eichler, Mario Ventura

Biology Faculty Articles

Despite its importance in cell biology and evolution, the centromere has remained the final frontier in genome assembly and annotation due to its complex repeat structure. However, isolation and characterization of the centromeric repeats from newly sequenced species are necessary for a complete understanding of genome evolution and function. In recent years, various genomes have been sequenced, but the characterization of the corresponding centromeric DNA has lagged behind. Here, we present a computational method (RepeatNet) to systematically identify higher-order repeat structures from unassembled whole-genome shotgun sequence and test whether these sequence elements correspond to functional centromeric sequences. We analyzed genome …

Every Genome Sequence Needs A Good Map, Harris A. Lewin, Denis M. Larkin, J. U. Pontius, Stephen J. O'Brien

Biology Faculty Articles

No abstract provided.

Reticulate Evolution And Marine Organisms: The Final Frontier?, Michael L. Arnold, Nicole D. Fogarty

Marine & Environmental Sciences Faculty Articles

The role that reticulate evolution (i.e., via lateral transfer, viral recombination and/or introgressive hybridization) has played in the origin and adaptation of individual taxa and even entire clades continues to be tested for all domains of life. Though falsified for some groups, the hypothesis of divergence in the face of gene flow is becoming accepted as a major facilitator of evolutionary change for many microorganisms, plants and animals. Yet, the effect of reticulate evolutionary change in certain assemblages has been doubted, either due to an actual dearth of genetic exchange among the lineages belonging to these clades or …

Mitochondrial Genomes Reveal An Explosive Radiation Of Extinct And Extant Bears Near The Miocene-Pliocene Boundary, Johannes Krause, Tina Unger, Aline Nocon, Anna-Sapfo Malaspinas, Sergios-Orestis Kolokotronis, Mathias Stiller, Leopoldo Soibelzon, Helen Spriggs, Paul H. Dear, Adrian W. Briggs, Sarah C. E. Bray, Stephen J. O'Brien, Gernot Rabeder, Paul Matheus, Alan Cooper, Montgomery Slatkin, Svante Paabo, Michael Hofreiter

Biology Faculty Articles

Background: Despite being one of the most studied families within the Carnivora, the phylogenetic relationships among the members of the bear family (Ursidae) have long remained unclear. Widely divergent topologies have been suggested based on various data sets and methods.

Results: We present a fully resolved phylogeny for ursids based on ten complete mitochondrial genome sequences from all eight living and two recently extinct bear species, the European cave bear (Ursus spelaeus) and the American giant short-faced bear (Arctodus simus). The mitogenomic data yield a well-resolved topology for ursids, with the sloth bear at the basal …

Sequences, Annotation And Single Nucleotide Polymorphism Of The Major Histocompatibility Complex In The Domestic Cat, Naoya Yuhki, James C. Mullikin, Thomas W. Beck, Robert M. Stephens, Stephen J. O'Brien

Biology Faculty Articles

Two sequences of major histocompatibility complex (MHC) regions in the domestic cat, 2.976 and 0.362 Mbps, which were separated by an ancient chromosome break (55–80 MYA) and followed by a chromosomal inversion were annotated in detail. Gene annotation of this MHC was completed and identified 183 possible coding regions, 147 human homologues, possible functional genes and 36 pseudo/unidentified genes) by GENSCAN and BLASTN, BLASTP RepeatMasker programs. The first region spans 2.976 Mbp sequence, which encodes six classical class II antigens (three DRA and three DRB antigens) lacking the functional DP, DQ regions, nine antigen processing molecules (DOA/DOB, DMA/DMB, TAPASIN, and …

Genomic Organization, Sequence Divergence, And Recombination Of Feline Immunodeficiency Virus From Lions In The Wild, Jill Pecon-Slattery, Carrie L. Mccracken, Jennifer L. Troyer, Sue Vandewoude, Melody E. Roelke, Kerry Sondgeroth, Christiaan Winterbach, Stephen J. O'Brien

Biology Faculty Articles

Background

Feline immunodeficiency virus (FIV) naturally infects multiple species of cat and is related to human immunodeficiency virus in humans. FIV infection causes AIDS-like disease and mortality in the domestic cat (Felis catus) and serves as a natural model for HIV infection in humans. In African lions (Panthera leo) and other exotic felid species, disease etiology introduced by FIV infection are less clear, but recent studies indicate that FIV causes moderate to severe CD4 depletion.

Results

In this study, comparative genomic methods are used to evaluate the full proviral genome of two geographically distinct FIV subtypes …

Clouded Leopard Phylogeny Revisited: Support For Species Recognition And Population Division Between Borneo And Sumatra, Andreas Wilting, Valerie A. Buckley-Beason, Heike Feldhaar, Jurgen Gadau, Stephen J. O'Brien, K. Eduard Linsenmair

Biology Faculty Articles

Background

The clouded leopard (Neofelis nebulosa) is one of the least known cat species and depletion of their forested habitats puts it under heavy pressure. Recently reclassification of Bornean clouded leopards (N. nebulosa diardi) to species level (N.diardi) was suggested based on molecular and morphological evidence. Since the genetic results were based solely on three Bornean samples we re-evaluated this partition using additional samples of Bornean clouded leopards (N = 7) and we were also able to include specimens from Sumatra (N = 3), which were lacking in previous analysis.

Results

We found strong …

Genomically Intact Endogenous Feline Leukemia Viruses Of Recent Origin, Alfred L. Roca, Jill Pecon-Slattery, Stephen J. O'Brien

Biology Faculty Articles

We isolated and sequenced two complete endogenous feline leukemia viruses (enFeLVs), designated enFeLV-AGTT and enFeLV-GGAG. In enFeLV-AGTT, the open reading frames are reminiscent of a functioning FeLV genome, and the 5′ and 3′ long terminal repeat sequences are identical. Neither endogenous provirus is genetically fixed in cats but polymorphic, with 8.9 and 15.2% prevalence for enFeLV-AGTT and enFeLV-GGAG, respectively, among a survey of domestic cats. Neither provirus was found in the genomes of related species of the Felis genus, previously shown to harbor enFeLVs. The absence of mutational divergence, polymorphic incidence in cats, and absence in related species suggest that …

A Radiation Hybrid Map Of The Cat Genome: Implications For Comparative Mapping, William J. Murphy, Shan Sun, Zhang-Qun Chen, Naoya Yuhki, Deborah Hirschmann, Marilyn Menotti-Raymond, Stephen J. O'Brien

Biology Faculty Articles

Ordered gene maps of mammalian species are becoming increasingly valued in assigning gene variants to function in human and animal models, as well as recapitulating the natural history of genome organization. To extend this power to the domestic cat, a radiation hybrid (RH) map of the cat was constructed integrating 424 Type I-coding genes with 176 microsatellite markers, providing coverage over all 20 feline chromosomes. Alignment of parallel RH maps of human and cat reveal 100 conserved segments ordered (CSOs) between the species, nearly three times the number observed with reciprocal chromosome painting analyses. The observed number is equivalent to …

Extensive Conservation Of Sex Chromosome Organization Between Cat And Human Revealed By Parallel Radiation Hybrid Mapping, William J. Murphy, Shan Sun, Zhang-Qun Chen, Jill Pecon-Slattery, Stephen J. O'Brien

Biology Faculty Articles

A radiation hybrid (RH)-derived physical map of 25 markers on the feline X chromosome (including 19 Type I coding loci and 6 Type II microsatellite markers) was compared to homologous marker order on the human and mouse X chromosome maps. Complete conservation of synteny and marker order was observed between feline and human X chromosomes, whereas the same markers identified a minimum of seven rearranged syntenic segments between mouse and cat/human X chromosome marker order. Within the blocks, the feline, human, and mouse marker order was strongly conserved. Similarly, Y chromosome locus order was remarkably conserved between cat and human …

A Lion Lentivirus Related To Feline Immunodeficiency Virus: Epidemiologic And Phylogenetic Aspects, Eric W. Brown, Naoya Yuhki, Craig Packer, Stephen J. O'Brien

Biology Faculty Articles

Feline immunodeficiency virus (FIV) is a novel lentivirus that is genetically homologous and functionally analogous to the human AIDS viruses, human immunodeficiency virus types 1 and 2. FIV causes immunosuppression in domestic cats by destroying the CD4 T-lymphocyte subsets in infected hosts. A serological survey of over 400 free-ranging African and Asian lions (Panthera leo) for antibodies to FIV revealed endemic lentivirus prevalence with an incidence of seropositivity as high as 90%o. A lion lentivirus (FIV-Ple) was isolated by infection of lion lymphocytes in vitro. Seroconversion was documented in two Serengeti lions, and discordance of mother-cub serological status …

Phylogenetic Associations Of Human And Simian T-Cell Leukemia/Lymphotropic Virus Type I Strains: Evidence For Interspecies Transmission, Igor J. Koralnik, Enzo Boeri, W. Carl Saxinger, Anita Lo Monico, Jake Fullen, Antoine Gessain, Hong-Guang Guo, Robert C. Gallo, Phillip Markham, Vaniambadi Kalyanaraman, Vanessa Hirsch, Jonathan Allan, Krishna Murthy, Patricia Alford, Jill Pecon-Slattery, Stephen J. O'Brien, Genoveffa Ranchini

Biology Faculty Articles

Homologous env sequences from 17 human T-leukemia/lymphotropic virus type I (HTLV-I) strains from throughout the world and from 25 simian T-leukemia/lymphotropic virus type I (STLV-I) strains from 12 simian species in Asia and Africa were analyzed in a phylogenetic context as an approach to resolving the natural history of these related retroviruses. STLV-I exhibited greater overall sequence variation between strains (1 to 18% compared with 0 to 9% for HTLV-I), supporting the simian origin of the modern viruses in all species. Three HTLV-I phylogenetic clusters or clades (cosmopolitan, Zaire, and Melanesia) were resolved with phenetic, parsimony, and likelihood analytical procedures. …

Worldwide Prevalence Of Lentivirus Infection In Wild Feline Species: Epidemiologic And Phylogenetic Aspects, Robert A. Olmstead, Raymond Langley, Melody E. Roelke, Robert M. Goeken, Diane Adger-Johnson, Julie P. Goff, John P. Albert, Craig Packer, M. Karen Laurenson, Tim M. Caro, Lue Scheepers, David E. Wildt, Mitchell Bush, Janice S. Martenson, Stephen J. O'Brien

Biology Faculty Articles

The natural occurrence of lentiviruses closely related to feline immunodeficiency virus (FIV) in nondomestic felid species is shown here to be worldwide. Cross-reactive antibodies to FIV were common in several free-ranging populations of large cats, including East African lions and cheetahs of the Serengeti ecosystem and in puma (also called cougar or mountain lion) populations throughout North America. Infectious puma lentivirus (PLV) was isolated from several Florida panthers, a severely endangered relict puma subspecies inhabiting the Big Cypress Swamp and Everglades ecosystems in southern Florida. Phylogenetic analysis of PLV genomic sequences from disparate geographic isolates revealed appreciable divergence from domestic …