• A comparative genomics multitool for scientific discovery and conservation

      Genereux, Diane P.; Serres, Aitor; Armstrong, Joel; Johnson, Jeremy; Marinescu, Voichita D.; Murén, Eva; Juan, David; Bejerano, Gill; Casewell, Nicholas R.; Chemnick, Leona G.; et al. (2020)
      The Zoonomia Project is investigating the genomics of shared and specialized traits in eutherian mammals. Here we provide genome assemblies for 131 species, of which all but 9 are previously uncharacterized, and describe a whole-genome alignment of 240 species of considerable phylogenetic diversity, comprising representatives from more than 80% of mammalian families. We find that regions of reduced genetic diversity are more abundant in species at a high risk of extinction, discern signals of evolutionary selection at high resolution and provide insights from individual reference genomes. By prioritizing phylogenetic diversity and making data available quickly and without restriction, the Zoonomia Project aims to support biological discovery, medical research and the conservation of biodiversity.
    • A comprehensive genomic history of extinct and living elephants

      Palkopoulou, Eleftheria; Lipson, Mark; Mallick, Swapan; Nielsen, Svend; Rohland, Nadin; Baleka, Sina; Karpinski, Emil; Ivancevic, Atma M.; To, Thu-Hien; Kortschak, R. Daniel; et al. (2018)
      Elephantids are the world’s most iconic megafaunal family, yet there is no comprehensive genomic assessment of their relationships. We report a total of 14 genomes, including 2 from the American mastodon, which is an extinct elephantid relative, and 12 spanning all three extant and three extinct elephantid species including an ~120,000-y-old straight-tusked elephant, a Columbian mammoth, and woolly mammoths....
    • A massively parallel sequencing approach uncovers ancient origins and high genetic variability of endangered Przewalski's horses

      Goto, Hiroki; Ryder, Oliver A.; Fisher, Allison R.; Schultz, Bryant; Kosakovsky Pond, Sergei L.; Nekrutenko, Anton; Makova, Kateryna D. (2011)
      The endangered Przewalski's horse is the closest relative of the domestic horse and is the only true wild horse species surviving today. The question of whether Przewalski's horse is the direct progenitor of domestic horse has been hotly debated. Studies of DNA diversity within Przewalski's horses have been sparse but are urgently needed to ensure their successful reintroduction to the wild. In an attempt to resolve the controversy surrounding the phylogenetic position and genetic diversity of Przewalski's horses, we used massively parallel sequencing technology to decipher the complete mitochondrial and partial nuclear genomes for all four surviving maternal lineages of Przewalski's horses. Unlike single-nucleotide polymorphism (SNP) typing usually affected by ascertainment bias, the present method is expected to be largely unbiased. Three mitochondrial haplotypes were discovered—two similar ones, haplotypes I/II, and one substantially divergent from the other two, haplotype III. Haplotypes I/II versus III did not cluster together on a phylogenetic tree, rejecting the monophyly of Przewalski's horse maternal lineages, and were estimated to split 0.117–0.186 Ma, significantly preceding horse domestication. In the phylogeny based on autosomal sequences, Przewalski's horses formed a monophyletic clade, separate from the Thoroughbred domestic horse lineage. Our results suggest that Przewalski's horses have ancient origins and are not the direct progenitors of domestic horses. The analysis of the vast amount of sequence data presented here suggests that Przewalski's and domestic horse lineages diverged at least 0.117 Ma but since then have retained ancestral genetic polymorphism and/or experienced gene flow.
    • An ancient icon reveals new mysteries: mummy DNA resurrects a cryptic species within the Nile crocodile

      Hekkala, Evon; Shirley, Matthew H.; Amato, George; Austin, James D.; Charter, Suellen J.; Thorbjarnarson, John; Vliet, Kent A.; Houck, Marlys L.; Desalle, Rob; Blum, Michael J. (2011)
      ...Our analyses reveal a cryptic evolutionary lineage within the Nile crocodile that elucidates the biogeographic history of the genus and clarifies long‐standing arguments over the species’ taxonomic identity and conservation status. An examination of crocodile mummy haplotypes indicates that the cryptic lineage corresponds to an earlier description of C. suchus and suggests that both African Crocodylus lineages historically inhabited the Nile River....
    • An interdisciplinary systems approach to study sperm physiology and evolution

      Shi, L.Z.; Nascimento, J.; Botvinick, E.; Durrant, Barbara S.; Berns, M.W. (2011)
      Optical trapping is a noninvasive biophotonic tool that has been developed to study the physiological and biomechanical properties of cells…. A real‐time automated tracking and trapping system (RATTS) is described that provides a remote user‐friendly robotic interface…. This combination of photonic physical and engineering tools has been used to examine the evolutionary effect of sperm competition in primates….
    • Assessing evolutionary processes over time in a conservation breeding program: A combined approach using molecular data, simulations and pedigree analysis

      Wright, Belinda R.; Hogg, Carolyn J.; McLennan, Elspeth A.; Belov, Katherine; Grueber, Catherine E. (2021)
      …We have quantified the effects of selection, drift and gene flow in 503 individuals across five generations from the Tasmanian devil insurance population. To determine whether different processes were acting in different settings, we separately analysed animals housed under individual-based management, versus those that were released to an island site. We found that a greater proportion of alleles were lost over time in the smaller island population than in captivity and propose that genetic drift is the most likely process influencing this result….
    • Broad host range of SARS-CoV-2 predicted by comparative and structural analysis of ACE2 in vertebrates

      Damas, Joana; Hughes, Graham M.; Keough, Kathleen C.; Painter, Corrie A.; Persky, Nicole S.; Corbo, Marco; Hiller, Michael; Koepfli, Klaus-Peter; Pfenning, Andreas R.; Zhao, Huabin; et al. (2020)
      The novel coronavirus severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the cause of COVID-19. The main receptor of SARS-CoV-2, angiotensin I converting enzyme 2 (ACE2), is now undergoing extensive scrutiny to understand the routes of transmission and sensitivity in different species. Here, we utilized a unique dataset of ACE2 sequences from 410 vertebrate species, including 252 mammals, to study the conservation of ACE2 and its potential to be used as a receptor by SARS-CoV-2. We designed a five-category binding score based on the conservation properties of 25 amino acids important for the binding between ACE2 and the SARS-CoV-2 spike protein. Only mammals fell into the medium to very high categories and only catarrhine primates into the very high category, suggesting that they are at high risk for SARS-CoV-2 infection. We employed a protein structural analysis to qualitatively assess whether amino acid changes at variable residues would be likely to disrupt ACE2/SARS-CoV-2 spike protein binding and found the number of predicted unfavorable changes significantly correlated with the binding score. Extending this analysis to human population data, we found only rare (frequency <0.001) variants in 10/25 binding sites. In addition, we found significant signals of selection and accelerated evolution in the ACE2 coding sequence across all mammals, and specific to the bat lineage. Our results, if confirmed by additional experimental data, may lead to the identification of intermediate host species for SARS-CoV-2, guide the selection of animal models of COVID-19, and assist the conservation of animals both in native habitats and in human care.
    • Comparative and demographic analysis of orang-utan genomes

      Locke, Devin P.; Hillier, LaDeana W.; Warren, Wesley C.; Worley, Kim C.; Nazareth, Lynne V.; Muzny, Donna M.; Yang, Shiaw-Pyng; Wang, Zhengyuan; Chinwalla, Asif T.; Minx, Pat; et al. (2011)
      ‘Orang-utan’ is derived from a Malay term meaning ‘man of the forest’ and aptly describes the southeast Asian great apes native to Sumatra and Borneo. The orang-utan species, Pongo abelii (Sumatran) and Pongo pygmaeus (Bornean), are the most phylogenetically distant great apes from humans, thereby providing an informative perspective on hominid evolution. Here we present a Sumatran orang-utan draft genome assembly and short read sequence data from five Sumatran and five Bornean orang-utan genomes. Our analyses reveal that, compared to other primates, the orang-utan genome has many unique features. Structural evolution of the orang-utan genome has proceeded much more slowly than other great apes, evidenced by fewer rearrangements, less segmental duplication, a lower rate of gene family turnover and surprisingly quiescent Alu repeats, which have played a major role in restructuring other primate genomes. We also describe a primate polymorphic neocentromere, found in both Pongo species, emphasizing the gradual evolution of orang-utan genome structure. Orang-utans have extremely low energy usage for a eutherian mammal1, far lower than their hominid relatives. Adding their genome to the repertoire of sequenced primates illuminates new signals of positive selection in several pathways including glycolipid metabolism. From the population perspective, both Pongo species are deeply diverse; however, Sumatran individuals possess greater diversity than their Bornean counterparts, and more species-specific variation. Our estimate of Bornean/Sumatran speciation time, 400,000 years ago, is more recent than most previous studies and underscores the complexity of the orang-utan speciation process. Despite a smaller modern census population size, the Sumatran effective population size (Ne) expanded exponentially relative to the ancestral Ne after the split, while Bornean Ne declined over the same period. Overall, the resources and analyses presented here offer new opportunities in evolutionary genomics, insights into hominid biology, and an extensive database of variation for conservation efforts.
    • Contemporary demographic reconstruction methods are robust to genome assembly quality: A case study in Tasmanian devils

      Patton, Austin H; Margres, Mark J; Stahlke, Amanda R; Hendricks, Sarah; Lewallen, Kevin; Hamede, Rodrigo K; Ruiz-Aravena, Manuel; Ryder, Oliver A.; McCallum, Hamish I; Jones, Menna E; et al. (2019)
      Reconstructing species’ demographic histories is a central focus of molecular ecology and evolution. Recently, an expanding suite of methods leveraging either the sequentially Markovian coalescent (SMC) or the site-frequency spectrum has been developed to reconstruct population size histories from genomic sequence data. However, few studies have investigated the robustness of these methods to genome assemblies of varying quality. In this study, we first present an improved genome assembly for the Tasmanian devil using the Chicago library method. Compared with the original reference genome, our new assembly reduces the number of scaffolds (from 35,975 to 10,010) and increases the scaffold N90 (from 0.101 to 2.164 Mb). Second, we assess the performance of four contemporary genomic methods for inferring population size history (PSMC, MSMC, SMC++, Stairway Plot), using the two devil genome assemblies as well as simulated, artificially fragmented genomes that approximate the hypothesized demographic history of Tasmanian devils. We demonstrate that each method is robust to assembly quality, producing similar estimates of Ne when simulated genomes were fragmented into up to 5,000 scaffolds. Overall, methods reliant on the SMC are most reliable between ?300 generations before present (gbp) and 100 kgbp, whereas methods exclusively reliant on the site-frequency spectrum are most reliable between the present and 30 gbp. Our results suggest that when used in concert, genomic methods for reconstructing species’ effective population size histories 1) can be applied to nonmodel organisms without highly contiguous reference genomes, and 2) are capable of detecting independently documented effects of historical geological events.
    • Cross-cultural consensus for waist–hip ratio and women's attractiveness

      Singh, Devendra; Dixson, B. J.; Jessop, T. S.; Morgan, Bethan J.; Dixson, Alan F.; (2010)
      In women of reproductive age, a gynoid body fat distribution as measured by the size of waist–hip ratio (WHR) is a reliable indicator of their sex hormone profile, greater success in pregnancy and less risk for major diseases. According to evolutionary mate selection theory, such indicators of health and fertility should be judged as attractive….
    • Genetic connectivity across marginal habitats: the elephants of the Namib Desert

      Ishida Yasuko; Van Coeverden de Groot Peter J.; Leggett Keith E. A.; Putnam, Andrea S.; Fox Virginia E.; Lai Jesse; Boag Peter T.; Georgiadis Nicholas J.; Roca Alfred L. (2016)
      Locally isolated populations in marginal habitats may be genetically distinctive and of heightened conservation concern. Elephants inhabiting the Namib Desert have been reported to show distinctive behavioral and phenotypic adaptations in that severely arid environment. The genetic distinctiveness of Namibian desert elephants relative to other African savanna elephant (Loxodonta africana ) populations has not been established. To investigate the genetic structure of elephants in Namibia, we determined the mitochondrial (mt) DNA control region sequences and genotyped 17 microsatellite loci in desert elephants (n = 8) from the Hoanib River catchment and the Hoarusib River catchment. We compared these to the genotypes of elephants (n = 77) from other localities in Namibia. The mtDNA haplotype sequences and frequencies among desert elephants were similar to those of elephants in Etosha National Park, the Huab River catchment, the Ugab River catchment, and central Kunene, although the geographically distant Caprivi Strip had different mtDNA haplotypes. Likewise, analysis of the microsatellite genotypes of desert‐dwelling elephants revealed that they were not genetically distinctive from Etosha elephants, and there was no evidence for isolation by distance across the Etosha region. These results, and a review of the historical record, suggest that a high learning capacity and long‐distance migrations allowed Namibian elephants to regularly shift their ranges to survive in the face of high variability in climate and in hunting pressure.
    • Genetic signatures of a demographic collapse in a large-bodied forest dwelling primate (Mandrillus leucophaeus)

      Ting, Nelson; Astaras, Christos; Hearn, Gail; Honarvar, Shaya; Corush, Joel; Burrell, Andrew S.; Phillips, Naomi; Morgan, Bethan J.; Gadsby, Elizabeth L.; Raaum, Ryan; et al. (2012)
      It is difficult to predict how current climate change will affect wildlife species adapted to a tropical rainforest environment. Understanding how population dynamics fluctuated in such species throughout periods of past climatic change can provide insight into this issue. The drill (Mandrillus leucophaeus) is a large-bodied rainforest adapted mammal found in West Central Africa. In the middle of this endangered monkey's geographic range is Lake Barombi Mbo, which has a well-documented palynological record of environmental change that dates to the Late Pleistocene. We used a Bayesian coalescent-based framework to analyze 2,076 base pairs of mitochondrial DNA across wild drill populations to infer past changes in female effective population size since the Late Pleistocene. Our results suggest that the drill underwent a nearly 15-fold demographic collapse in female effective population size that was most prominent during the Mid Holocene (approximately 3-5 Ka). This time period coincides with a period of increased dryness and seasonality across Africa and a dramatic reduction in forest coverage at Lake Barombi Mbo. We believe that these changes in climate and forest coverage were the driving forces behind the drill population decline. Furthermore, the warm temperatures and increased aridity of the Mid Holocene are potentially analogous to current and future conditions faced by many tropical rainforest communities. In order to prevent future declines in population size in rainforest-adapted species such as the drill, large tracts of forest should be protected to both preserve habitat and prevent forest loss through aridification.
    • Heterogeneity in ecological and evolutionary meta-analyses: its magnitude and implications

      Senior Alistair M.; Grueber, Catherine E.; Kamiya Tsukushi; Lagisz Malgorzata; O'Dwyer Katie; Santos, Eduardo S. A.; Nakagawa Shinichi (2016)
      ...We reviewed 700 studies, finding 325 that used formal meta‐analysis, of which total heterogeneity was reported in fewer than 40%. We used second‐order meta‐analysis to collate heterogeneity statistics from 86 studies. Our analysis revealed that the median and mean heterogeneity, expressed as I 2, are 84.67% and 91.69%, respectively....
    • Highly accurate long-read HiFi sequencing data for five complex genomes

      Hon, Ting; Mars, Kristin; Young, Greg; Tsai, Yu-Chih; Karalius, Joseph W.; Landolin, Jane M.; Maurer, Nicholas; Kudrna, David; Hardigan, Michael A.; Steiner, Cynthia C.; et al. (2020)
      The PacBio® HiFi sequencing method yields highly accurate long-read sequencing datasets with read lengths averaging 10–25?kb and accuracies greater than 99.5%. These accurate long reads can be used to improve results for complex applications such as single nucleotide and structural variant detection, genome assembly, assembly of difficult polyploid or highly repetitive genomes, and assembly of metagenomes. Currently, there is a need for sample data sets to both evaluate the benefits of these long accurate reads as well as for development of bioinformatic tools including genome assemblers, variant callers, and haplotyping algorithms. We present deep coverage HiFi datasets for five complex samples including the two inbred model genomes Mus musculus and Zea mays, as well as two complex genomes, octoploid Fragaria?×?ananassa and the diploid anuran Rana muscosa. Additionally, we release sequence data from a mock metagenome community. The datasets reported here can be used without restriction to develop new algorithms and explore complex genome structure and evolution. Data were generated on the PacBio Sequel II System.
    • Insights into hominid evolution from the gorilla genome sequence

      Scally, Aylwyn; Dutheil, Julien Y.; Hillier, LaDeana W.; Jordan, Gregory E.; Goodhead, Ian; Herrero, Javier; Hobolth, Asger; Lappalainen, Tuuli; Mailund, Thomas; Marques-Bonet, Tomas; et al. (2012)
      Gorillas are humans’ closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera....
    • Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix

      Springer, Mark S.; Meredith, Robert W.; Gatesy, John; Emerling, Christopher A.; Park, Jong; Rabosky, Daniel L.; Stadler, Tanja; Steiner, Cynthia C.; Ryder, Oliver A.; Janečka, Jan E.; et al. (2012)
      Phylogenetic relationships, divergence times, and patterns of biogeographic descent among primate species are both complex and contentious. Here, we generate a robust molecular phylogeny for 70 primate genera and 367 primate species based on a concatenation of 69 nuclear gene segments and ten mitochondrial gene sequences, most of which were extracted from GenBank. Relaxed clock analyses of divergence times with 14 fossil-calibrated nodes suggest that living Primates last shared a common ancestor 71–63 Ma, and that divergences within both Strepsirrhini and Haplorhini are entirely post-Cretaceous. These results are consistent with the hypothesis that the Cretaceous-Paleogene mass extinction of non-avian dinosaurs played an important role in the diversification of placental mammals. Previous queries into primate historical biogeography have suggested Africa, Asia, Europe, or North America as the ancestral area of crown primates, but were based on methods that were coopted from phylogeny reconstruction. By contrast, we analyzed our molecular phylogeny with two methods that were developed explicitly for ancestral area reconstruction, and find support for the hypothesis that the most recent common ancestor of living Primates resided in Asia. Analyses of primate macroevolutionary dynamics provide support for a diversification rate increase in the late Miocene, possibly in response to elevated global mean temperatures, and are consistent with the fossil record. By contrast, diversification analyses failed to detect evidence for rate-shift changes near the Eocene-Oligocene boundary even though the fossil record provides clear evidence for a major turnover event (“Grande Coupure”) at this time. Our results highlight the power and limitations of inferring diversification dynamics from molecular phylogenies, as well as the sensitivity of diversification analyses to different species concepts.
    • Molecular phylogeny and evolution of the Perissodactyla

      Steiner, Cynthia C.; Ryder, Oliver A. (2011)
      The evolution of perissodactyls (rhinoceroses, tapirs, and horses) has been well studied primarily because of their extensive fossil record. Nevertheless, controversy persists regarding relationships of some of the extant taxa, reflecting inconsistencies between molecular and morphological studies. Here we examine the phylogenetic relationships of 16 living perissodactyl species by concatenating two mitochondrial and nine nuclear genes, and we estimate their divergence times using a relaxed Bayesian molecular clock approach....
    • Molecular systematics of eastern North American Phalangodidae (Arachnida: Opiliones: Laniatores), demonstrating convergent morphological evolution in caves

      Hedin, Marshal; Thomas, Steven M.; (2010)
      The phalangodid harvestmen (Opiliones: Laniatores) fauna of the southeastern United States has remained obscure since original descriptions of many genera and species over 60 years ago. The obscurity of this interesting group is pervasive, with uncertainty regarding basic systematic information such as generic limits, species limits, and geographic distributions....
    • On the phylogeny of Mustelidae subfamilies: analysis of seventeen nuclear non-coding loci and mitochondrial complete genomes

      Yu, Li; Peng, Dan; Liu, Jiang; Luan, Pengtao; Liang, Lu; Lee, Hang; Lee, Muyeong; Ryder, Oliver A.; Zhang, Yaping (2011)
      Background Mustelidae, as the largest and most-diverse family of order Carnivora, comprises eight subfamilies. Phylogenetic relationships among these Mustelidae subfamilies remain argumentative subjects in recent years. One of the main reasons is that the mustelids represent a typical example of rapid evolutionary radiation and recent speciation event. Prior investigation has been concentrated on the application of different mitochondrial (mt) sequence and nuclear protein-coding data, herein we employ 17 nuclear non-coding loci (>15 kb), in conjunction with mt complete genome data (>16 kb), to clarify these enigmatic problems. Results The combined nuclear intron and mt genome analyses both robustly support that Taxidiinae diverged first, followed by Melinae. Lutrinae and Mustelinae are grouped together in all analyses with strong supports. The position of Helictidinae, however, is enigmatic because the mt genome analysis places it to the clade uniting Lutrinae and Mustelinae, whereas the nuclear intron analysis favores a novel view supporting a closer relationship of Helictidinae to Martinae. This finding emphasizes a need to add more data and include more taxa to resolve this problem. In addition, the molecular dating provides insights into the time scale of the origin and diversification of the Mustelidae subfamilies. Finally, the phylogenetic performances and limits of nuclear introns and mt genes are discussed in the context of Mustelidae phylogeny. Conclusion Our study not only brings new perspectives on the previously obscured phylogenetic relationships among Mustelidae subfamilies, but also provides another example demonstrating the effectiveness of nuclear non-coding loci for reconstructing evolutionary histories in a group that has undergone rapid bursts of speciation.
    • Orangutan Alu quiescence reveals possible source element: support for ancient backseat drivers

      Walker, Jerilyn A.; Konkel, Miriam K.; Ullmer, Brygg; Monceaux, Christopher P.; Ryder, Oliver A.; Hubley, Robert; Smit, Arian FA; Batzer, Mark A. (2012)
      Sequence analysis of the orangutan genome revealed that recent proliferative activity of Alu elements has been uncharacteristically quiescent in the Pongo (orangutan) lineage, compared with all previously studied primate genomes. With relatively few young polymorphic insertions, the genomic landscape of the orangutan seemed like the ideal place to search for a driver, or source element, of Alu retrotransposition.