• A High-Quality, Long-Read De Novo Genome Assembly to Aid Conservation of Hawaii's Last Remaining Crow Species

      Sutton, Jolene; Helmkampf, Martin; Steiner, Cynthia C.; Bellinger, M. Renee; Korlach, Jonas; Hall, Richard; Baybayan, Primo; Muehling, Jill; Gu, Jenny; Kingan, Sarah; et al. (2018)
      Genome-level data can provide researchers with unprecedented precision to examine the causes and genetic consequences of population declines, which can inform conservation management. Here, we present a high-quality, long-read, de novo genome assembly for one of the world’s most endangered bird species, the ʻAlalā (Corvus hawaiiensis; Hawaiian crow). As the only remaining native crow species in Hawaiʻi, the ʻAlalā survived solely in a captive-breeding program from 2002 until 2016, at which point a long-term reintroduction program was initiated. The high-quality genome assembly was generated to lay the foundation for both comparative genomics studies and the development of population-level genomic tools that will aid conservation and recovery efforts. We illustrate how the quality of this assembly places it amongst the very best avian genomes assembled to date, comparable to intensively studied model systems. We describe the genome architecture in terms of repetitive elements and runs of homozygosity, and we show that compared with more outbred species, the ʻAlalā genome is substantially more homozygous. We also provide annotations for a subset of immunity genes that are likely to be important in conservation management, and we discuss how this genome is currently being used as a roadmap for downstream conservation applications
    • A time- and cost-effective strategy to sequence mammalian Y Chromosomes: an application to the de novo assembly of gorilla Y

      Tomaszkiewicz, Marta; Rangavittal, Samarth; Cechova, Monika; Sanchez, Rebeca Campos; Fescemyer, Howard W.; Harris, Robert; Ye, Danling; O'Brien, Patricia C. M.; Chikhi, Rayan; Ryder, Oliver A.; et al. (2016)
      The mammalian Y Chromosome sequence, critical for studying male fertility and dispersal, is enriched in repeats and palindromes, and thus, is the most difficult component of the genome to assemble. Previously, expensive and labor-intensive BAC-based techniques were used to sequence the Y for a handful of mammalian species. Here, we present a much faster and more affordable strategy for sequencing and assembling mammalian Y Chromosomes of sufficient quality for most comparative genomics analyses and for conservation genetics applications. The strategy combines flow sorting, short- and long-read genome and transcriptome sequencing, and droplet digital PCR with novel and existing computational methods. It can be used to reconstruct sex chromosomes in a heterogametic sex of any species. We applied our strategy to produce a draft of the gorilla Y sequence. The resulting assembly allowed us to refine gene content, evaluate copy number of ampliconic gene families, locate species-specific palindromes, examine the repetitive element content, and produce sequence alignments with human and chimpanzee Y Chromosomes. Our results inform the evolution of the hominine (human, chimpanzee, and gorilla) Y Chromosomes. Surprisingly, we found the gorilla Y Chromosome to be similar to the human Y Chromosome, but not to the chimpanzee Y Chromosome. Moreover, we have utilized the assembled gorilla Y Chromosome sequence to design genetic markers for studying the male-specific dispersal of this endangered species.
    • Age-dependent, negative heterozygosity-fitness correlations and local effects in an endangered Caribbean reptile, Iguana delicatissima

      Judson, Jessica L Martin; Knapp, Charles R.; Welch, Mark E. (2018)
      Inbreeding depression can have alarming impacts on threatened species with small population sizes. Assessing inbreeding has therefore become an important focus of conservation research. In this study, heterozygosity-fitness correlations (HFCs) were measured by genotyping 7 loci in 83 adult and 184 hatchling Lesser Antillean Iguanas, Iguana delicatissima, at a communal nesting site in Dominica to assess the role of inbreeding depression on hatchling fitness and recruitment to the adult population in this endangered species. We found insignificant correlations between multilocus heterozygosity and multiple fitness proxies in hatchlings and adults. Further, multilocus heterozygosity did not differ significantly between hatchlings and adults, which suggests that the survivorship of homozygous hatchlings does not differ markedly from that of their heterozygous counterparts. However, genotypes at two individual loci were correlated with hatching date, a finding consistent with the linkage between specific marker loci and segregating deleterious recessive alleles. These results provide only modest evidence that inbreeding depression influences the population dynamics of I. delicatissima on Dominica.;
    • Applying SNP-derived molecular coancestry estimates to captive breeding programs

      Ivy, Jamie A.; Putnam, Andrea S.; Navarro, Asako Y.; Gurr, Jessica; Ryder, Oliver A. (2016)
      ...Although pedigree-based breeding strategies are quite effective at retaining long-term genetic variation, management of zoo-based breeding programs continues to be hampered when pedigrees are poorly known. The objective of this study was to evaluate 2 options for generating single nucleotide polymorphism (SNP) data to resolve unknown relationships within captive breeding programs...
    • Comparative genomics reveals insights into avian genome evolution and adaptation

      Zhang, Guojie; Li, Cai; Li, Qiye; Li, Bo; Larkin, Denis M.; Lee, Chul; Storz, Jay F.; Antunes, Agostinho; Greenwold, Matthew J.; Meredith, Robert W.; et al. (2014)
      Birds are the most species-rich class of tetrapod vertebrates and have wide relevance across many research fields. We explored bird macroevolution using full genomes from 48 avian species representing all major extant clades....
    • Conservation genomics of threatened animal species

      Steiner, Cynthia C.; Putnam, Andrea S.; Hoeck, Paquita E. A.; Ryder, Oliver A. (2013)
      The genomics era has opened up exciting possibilities in the field of conservation biology by enabling genomic analyses of threatened species that previously were limited to model organisms. Next-generation sequencing (NGS) and the collection of genome-wide data allow for more robust studies of the demographic history of populations and adaptive variation associated with fitness and local adaptation.…
    • Contrasting evolutionary history, anthropogenic declines and genetic contact in the northern and southern white rhinoceros (Ceratotherium simum)

      Moodley, Yoshan; Russo, Isa-Rita M.; Robovský, Jan; Dalton, Desiré L.; Kotzé, Antoinette; Smith, Steve; Stejskal, Jan; Ryder, Oliver A.; Hermes, Robert; Walzer, Chris; et al. (2018)
      The white rhinoceros (Ceratotherium simum) has a discontinuous African distribution, which is limited by the extent of sub-Saharan grasslands. The southern population (SWR) declined to its lowest number around the turn of the nineteenth century, but recovered to become the world's most numerous rhinoceros....
    • Contrasting genomic shifts underlie parallel phenotypic evolution in response to fishing

      Therkildsen, Nina O.; Wilder, Aryn P.; Conover, David O.; Munch, Stephan B.; Baumann, Hannes; Palumbi, Stephen R. (2019)
      Parallel and idiosyncratic fish adaptation Fish populations respond rapidly to fishing pressure. Within a handful of generations, marked phenotypic change can occur—often to smaller body sizes, because it is the big fish that are usually extracted....
    • Evaluating recovery potential of the northern white rhinoceros from cryopreserved somatic cells

      Tunstall, Tate S.; Kock, Richard; Vahala, Jiri; Diekhans, Mark; Fiddes, Ian; Armstrong, Joel; Paten, Benedikt; Ryder, Oliver A.; Steiner, Cynthia C. (2018)
      The critically endangered northern white rhinoceros is believed to be extinct in the wild, with the recent death of the last male leaving only two remaining individuals in captivity. Its extinction would appear inevitable, but the development of advanced cell and reproductive technologies such as cloning by nuclear transfer and the artificial production of gametes via stem cells differentiation offer a second chance for its survival. In this work, we analyzed genome-wide levels of genetic diversity, inbreeding, population history, and demography of the white rhinoceros sequenced from cryopreserved somatic cells, with the goal of informing how genetically valuable individuals could be used in future efforts toward the genetic rescue of the northern white rhinoceros. We present the first sequenced genomes of the northern white rhinoceros, which show relatively high levels of heterozygosity and an average genetic divergence of 0.1% compared with the southern subspecies. The two white rhinoceros subspecies appear to be closely related, with low genetic admixture and a divergent time <80,000 yr ago. Inbreeding, as measured by runs of homozygosity, appears slightly higher in the southern than the northern white rhinoceros. This work demonstrates the value of the northern white rhinoceros cryopreserved genetic material as a potential gene pool for saving this subspecies from extinction.
    • Evolutionary and functional novelty of pancreatic ribonuclease: a study of Musteloidea (order Carnivora)

      Liu, Jiang; Wang, Xiao-ping; Cho, Soochin; Lim, Burton K.; Irwin, David M.; Ryder, Oliver A.; Zhang, Ya-ping; Yu, Li (2014)
      Pancreatic ribonuclease (RNASE1) is a digestive enzyme that has been one of the key models in studies of evolutionary innovation and functional diversification. It has been believed that the RNASE1 gene duplications are correlated with the plant-feeding adaptation of foregut-fermenting herbivores. Here, we characterized RNASE1 genes from Caniformia, which has a simple digestive system and lacks microbial digestion typical of herbivores, in an unprecedented scope based on both gene sequence and tissue expression analyses. Remarkably, the results yielded new hypotheses regarding the evolution and the function of Caniformia RNASE1 genes. Four independent gene duplication events in the families of superfamily Musteloidea, including Procyonidae, Ailuridae, Mephitidae and Mustelidae, were recovered, rejecting previous Mustelidae-specific duplication hypothesis, but supporting Musteloidea duplication hypothesis. Moreover, our analyses revealed pronounced differences among the RNASE1 gene copies regarding their selection pressures, pI values and tissue expression patterns, suggesting the differences in their physiological functions. Notably, the expression analyses detected the transcription of a RNASE1 pseudogene in several tissues, raising the possibility that pseudogenes are also a potential source during the RNase functional diversification. In sum, the present work demonstrated a far more complex and intriguing evolutionary pattern and functional diversity of mammalian ribonuclease than previously thought.
    • Evolutionary genomics and conservation of the endangered Przewalski’s horse

      Der Sarkissian, Clio; Ermini, Luca; Schubert, Mikkel Heide; Yang, Melinda A.; Librado, Pablo; Fumagalli, Matteo; Jónsson, Hákon; Bar-Gal, Gila Kahila; Albrechtsen, Anders; Vieira, Filipe G.; et al. (2015)
      Przewalski’s horses (PHs, Equus ferus ssp. przewalskii) were discovered in the Asian steppes in the 1870s and represent the last remaining true wild horses. PHs became extinct in the wild in the 1960s but survived in captivity, thanks to major conservation efforts....
    • Exploring the limits of saving a subspecies: The ethics and social dynamics of restoring northern white rhinos (Ceratotherium simum cottoni)

      Ryder, Oliver A.; Friese, Carrie; Greely, Henry T.; Sandler, Ronald; Saragusty, Joseph; Durrant, Barbara S.; Redford, Kent H. (2020)
      The northern white rhino (Ceratotherium simum cottoni) is functionally extinct with only two females left alive. However, cryopreserved material from a number of individuals represents the potential to produce additional individuals using advanced reproductive and genetic rescue technologies and perhaps eventually a population to return to their native range. If this could and were done, how should it be done responsibly and thoughtfully. What issues and questions of a technical, bioethical, and societal nature will it raise that need to be anticipated and addressed? Such issues are explored in this article by an interdisciplinary team assembled to provide context to the northern white rhino project of the San Diego Zoo Global.
    • Extreme selective sweeps independently targeted the X chromosomes of the great apes

      Nam, Kiwoong; Munch, Kasper; Hobolth, Asger; Dutheil, Julien Yann; Veeramah, Krishna R.; Woerner, August E.; Hammer, Michael F.; Great Ape Genome Diversity Project; Mailund, Thomas; Schierup, Mikkel Heide; et al. (2015)
      …We perform a comparative analysis of X chromosome polymorphism in 10 great ape species, including humans. In most species, we identify striking megabase-wide regions, where nucleotide diversity is less than 20% of the chromosomal average....
    • Genetic structure and diversity among historic and modern populations of the Sumatran rhinoceros (Dicerorhinus sumatrensis)

      Brandt, Jessica R.; van Coeverden de Groot, Peter J.; Witt, Kelsey E.; Engelbrektsson, Paige K.; Helgen, Kristofer M.; Malhi, Ripan S.; Ryder, Oliver A.; Roca, Alfred L. (2018)
      The Sumatran rhinoceros (Dicerorhinus sumatrensis), once widespread across Southeast Asia, now consists of as few as 30 individuals within Sumatra and Borneo. To aid in conservation planning, we sequenced 218 bp of control region mitochondrial (mt) DNA, identifying 17 distinct mitochondrial haplotypes across modern (N = 13) and museum (N = 26) samples....
    • Genomic analysis of snub-nosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation

      Yu, Li; Wang, Guo-Dong; Ruan, Jue; Chen, Yong-Bin; Yang, Cui-Ping; Cao, Xue; Wu, Hong; Liu, Yan-Hu; Du, Zheng-Lin; Wang, Xiao-Ping; et al. (2016)
      The snub-nosed monkey genus Rhinopithecus includes five closely related species distributed across altitudinal gradients from 800 to 4,500 m. Rhinopithecus bieti, Rhinopithecus roxellana, and Rhinopithecus strykeri inhabit high-altitude habitats, whereas Rhinopithecus brelichi and Rhinopithecus avunculus inhabit lowland regions. We report the de novo whole-genome sequence of R. bieti and genomic sequences for the four other species. Eight shared substitutions were found in six genes related to lung function, DNA repair, and angiogenesis in the high-altitude snub-nosed monkeys. Functional assays showed that the high-altitude variant of CDT1 (Ala537Val) renders cells more resistant to UV irradiation, and the high-altitude variants of RNASE4 (Asn89Lys and Thr128Ile) confer enhanced ability to induce endothelial tube formation in vitro. Genomic scans in the R. bieti and R. roxellana populations identified signatures of selection between and within populations at genes involved in functions relevant to high-altitude adaptation. These results provide valuable insights into the adaptation to high altitude in the snub-nosed monkeys.
    • Great ape genetic diversity and population history

      Prado-Martinez, Javier; Sudmant, Peter H.; Kidd, Jeffrey M.; Li, Heng; Kelley, Joanna L.; Lorente-Galdos, Belen; Veeramah, Krishna R.; Woerner, August E.; O’Connor, Timothy D.; Santpere, Gabriel; et al. (2013)
      Most great ape genetic variation remains uncharacterized; however, its study is critical for understanding population history, recombination, selection and susceptibility to disease. Here we sequence to high coverage a total of 79 wild- and captive-born individuals representing all six great ape species and seven subspecies and report 88.8 million single nucleotide polymorphisms. Our analysis provides support for genetically distinct populations within each species, signals of gene flow, and the split of common chimpanzees into two distinct groups: Nigeria–Cameroon/western and central/eastern populations. We find extensive inbreeding in almost all wild populations, with eastern gorillas being the most extreme. Inferred effective population sizes have varied radically over time in different lineages and this appears to have a profound effect on the genetic diversity at, or close to, genes in almost all species. We discover and assign 1,982 loss-of-function variants throughout the human and great ape lineages, determining that the rate of gene loss has not been different in the human branch compared to other internal branches in the great ape phylogeny. This comprehensive catalogue of great ape genome diversity provides a framework for understanding evolution and a resource for more effective management of wild and captive great ape populations.
    • Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat

      Mendoza, M. Lisandra Zepeda; Xiong, Zijun; Escalera-Zamudio, Marina; Runge, Anne Kathrine; Thézé, Julien; Streicker, Daniel; Frank, Hannah K.; Loza-Rubio, Elizabeth; Liu, Shengmao; Ryder, Oliver A.; et al. (2018)
      The common vampire bat (Desmodus rotundus) is one of only three obligate blood-feeding mammals. By sequencing both its genome and gut metagenome, the authors provide a holistic view of the evolutionary adaptations that underlie this unusual diet.
    • Inference of gorilla demographic and selective history from whole-genome sequence data

      McManus, Kimberly F.; Kelley, Joanna L.; Song, Shiya; Veeramah, Krishna R.; Woerner, August E.; Stevison, Laurie S.; Ryder, Oliver A.; Great Ape Genome Project; Kidd, Jeffrey M.; Wall, Jeffrey D.; et al. (2015)
      Although population-level genomic sequence data have been gathered extensively for humans, similar data from our closest living relatives are just beginning to emerge. Examination of genomic variation within great apes offers many opportunities to increase our understanding of the forces that have differentially shaped the evolutionary history of hominid taxa. Here, we expand upon the work of the Great Ape Genome Project by analyzing medium to high coverage whole-genome sequences from 14 western lowland gorillas (Gorilla gorilla gorilla), 2 eastern lowland gorillas (G. beringei graueri), and a single Cross River individual (G. gorilla diehli). We infer that the ancestors of western and eastern lowland gorillas diverged from a common ancestor approximately 261 ka, and that the ancestors of the Cross River population diverged from the western lowland gorilla lineage approximately 68 ka. Using a diffusion approximation approach to model the genome-wide site frequency spectrum, we infer a history of western lowland gorillas that includes an ancestral population expansion of 1.4-fold around 970 ka and a recent 5.6-fold contraction in population size 23 ka. The latter may correspond to a major reduction in African equatorial forests around the Last Glacial Maximum. We also analyze patterns of variation among western lowland gorillas to identify several genomic regions with strong signatures of recent selective sweeps. We find that processes related to taste, pancreatic and saliva secretion, sodium ion transmembrane transport, and cardiac muscle function are overrepresented in genomic regions predicted to have experienced recent positive selection.
    • Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits

      Chen, Lei; Qiu, Qiang; Jiang, Yu; Wang, Kun; Lin, Zeshan; Li, Zhipeng; Bibi, Faysal; Yang, Yongzhi; Wang, Jinhuan; Nie, Wenhui; et al. (2019)
      The ruminants are one of the most successful mammalian lineages, exhibiting morphological and habitat diversity and containing several key livestock species. To better understand their evolution, we generated and analyzed de novo assembled genomes of 44 ruminant species, representing all six Ruminantia families....
    • Molecular phylogeny and chromosomal evolution of Alcelaphini (Antilopinae)

      Steiner, Cynthia C.; Charter, Suellen J.; Houck, Marlys L.; Ryder, Oliver A. (2014)
      Robertsonian (Rb) translocations, in particular centric fusions, are thought to play a primary role in evolution and speciation of the Bovidae family....This work studies chromosome variation in 72 captive individuals of 6 species of Alcelaphini (Antilopinae): The hartebeest (genus Alcelaphus), hirola (Beatragus), black and blue wildebeests (Connochaetes), and the topi and bontebok (Damaliscus)….