• Nanopore sequencing of long ribosomal DNA amplicons enables portable and simple biodiversity assessments with high phylogenetic resolution across broad taxonomic scale

      Krehenwinkel, Henrik; Pomerantz, Aaron; Henderson, James B.; Kennedy, Susan R.; Lim, Jun Y.; Swamy, Varun; Shoobridge, Juan D.; Patel, Nipam H.; Gillespie, Rosemary G.; Prost, Stefan (2019)
      Background: In light of the current biodiversity crisis, DNA barcoding is developing into an essential tool to quantify state shifts in global ecosystems. Current barcoding protocols often rely on short amplicon sequences, which yield accurate identification of biological entities in a community, but provide limited phylogenetic resolution across broad taxonomic scales. However, the phylogenetic structure of communities is an essential component of biodiversity. Consequently, a barcoding approach is required that unites robust taxonomic assignment power and high phylogenetic utility. A possible solution is offered by sequencing long ribosomal DNA (rDNA) amplicons on the MinION platform (Oxford Nanopore Technologies). Results: Using a dataset of various animal and plant species, with a focus on arthropods, we assemble a pipeline for long rDNA barcode analysis and introduce a new software (MiniBar) to demultiplex dual indexed nanopore reads. We find excellent phylogenetic and taxonomic resolution offered by long rDNA sequences across broad taxonomic scales. We highlight the simplicity of our approach by field barcoding with a miniaturized, mobile laboratory in a remote rainforest. We also test the utility of long rDNA amplicons for analysis of community diversity through metabarcoding and find that they recover highly skewed diversity estimates. Conclusions: Sequencing dual indexed, long rDNA amplicons on the MinION platform is a straightforward, cost effective, portable and universal approach for eukaryote DNA barcoding. Long rDNA amplicons scale up DNA barcoding by enabling the accurate recovery of taxonomic and phylogenetic diversity. However, bulk community analyses using long-read approaches may introduce biases and will require further exploration.
    • No evidence of inbreeding depression in a Tasmanian devil insurance population despite significant variation in inbreeding

      Gooley, Rebecca M.; Hogg, Carolyn J.; Belov, Katherine; Grueber, Catherine E. (2017)
      Inbreeding depression occurs when inbred individuals experience reduced fitness as a result of reduced genome-wide heterozygosity. The Tasmanian devil faces extinction due to a contagious cancer, devil facial tumour disease (DFTD). An insurance metapopulation was established in 2006 to ensure the survival of the species and to be used as a source population for re-wilding and genetic rescue. The emergence of DFTD and the rapid decline of wild devil populations have rendered the species at risk of inbreeding depression. We used 33 microsatellite loci to (1) reconstruct a pedigree for the insurance population and (2) estimate genome-wide heterozygosity for 200 individuals. Using heterozygosity-fitness correlations, we investigated the effect of heterozygosity on six diverse fitness measures (ulna length, asymmetry, weight-at-weaning, testes volume, reproductive success and survival). Despite statistically significant evidence of variation in individual inbreeding in this population, we found no associations between inbreeding and any of our six fitness measurements. We propose that the benign environment in captivity may decrease the intensity of inbreeding depression, relative to the stressful conditions in the wild. Future work will need to measure fitness of released animals to facilitate translation of this data to the broader conservation management of the species in its native range.
    • Noninvasive sampling for detection of elephant endotheliotropic herpesvirus and genomic DNA in Asian (Elephas maximus) and African (Loxodonta africana) elephants

      Jeffrey, Alison; Evans, Tierra Smiley; Molter, Christine M.; Howard, Lauren L.; Ling, Paul; Goldstein, Tracey; Gilardi, Kirsten (2020)
      Elephant endotheliotropic herpesvirus (EEHV) hemorrhagic disease (EEHV-HD) threatens Asian elephant (Elephas maximus) population sustainability in North America…. To evaluate noninvasive sample collection options, paired invasively collected (blood, trunk wash and oral swabs), and noninvasively collected (chewed plant and fecal) samples were compared over 6 wk from 9 Asian elephants and 12 African elephants….
    • Notes from the field: A primatologist's point of view

      Morgan, Bethan J. (2012)
      What's a regular day in the life of a field primatologist? Working in the tropics is perceived as difficult and dangerous, with scientific discoveries only part of the everyday drama of studying primates....
    • Nutrition and health in amphibian husbandry: Ex situ amphibian health and nutrition

      Ferrie, Gina M.; Alford, Vance C.; Atkinson, Jim; Baitchman, Eric; Barber, Diane; Blaner, William S.; Crawshaw, Graham; Daneault, Andy; Dierenfeld, Ellen; Finke, Mark; et al. (2014)
      Amphibian biology is intricate, and there are many inter‐related factors that need to be understood before establishing successful Conservation Breeding Programs (CBPs). Nutritional needs of amphibians are highly integrated with disease and their husbandry needs, and the diversity of developmental stages, natural habitats, and feeding strategies result in many different recommendations for proper care and feeding….
    • Obituary to Kupe Cowboy

      Morgan, Bethan J. (2020)
      Simon ‘Kupe’ Ngwese, better known as ‘Kupe Cowboy’, lived a full life. Born in around 1940, to a poor family in Kupe village, near Tombel, Kupe-Muanenguba division of South West Region, Cameroon, like many around him he grew up as a farmer and opportunistic hunter. Later in life, he worked as a research assistant to the then San Diego Zoo Global project at Mount Kupe in Bakossiland....
    • Old-growth forest is what giant pandas really need

      Zhang, Zejun; Swaisgood, Ronald R.; Zhang, S.; Nordstrom, Lisa A.; Wang, H.; Gu, X.; Hu, J.; Wei, F. (2011)
      …Here, we use an information-theoretic approach to analyse the largest, landscape-level dataset on panda habitat use to date, and challenge the prevailing wisdom about panda habitat needs. We show that pandas are associated with old-growth forest more than with any ecological variable other than bamboo….
    • 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.
    • On the timing of an epidemic of amphibian chytridiomycosis in the highlands of Guatemala

      Mendelson, Joseph R.; Jones, Megan E. B.; Pessier, Allan P.; Toledo, Gabriela; Kabay, Edward H.; Campbell, Jonathan A. (2014)
      We analyzed museum specimens from two regions of Guatemala for the presence of the pathogenic amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) using both histological and PCR-based assays. We determined that the pathogen was present at one site at low prevalence in 1980 and 1981, immediately preceding drastic declines of amphibian in the region by 1983….
    • On the trail of primate scent signals: A field analysis of callitrichid scent-gland secretions by portable gas chromatography-mass spectrometry

      Poirier, Alice C.; Waterhouse, John S.; Watsa, Mrinalini; Erkenswick, Gideon A.; Moreira, Laís A. A.; Tang, Jia; Dunn, Jacob C.; Melin, Amanda D.; Smith, Andrew C. (2021)
      …We present the first use of the Torion® portable gas chromatography-mass spectrometry (GC-MS) instrument for in situ chemical analysis of primate scents. We collected and analyzed swab samples from the scent glands and skin from 13 groups (57 individuals) of two sympatric species of wild emperor tamarins, Saguinus imperator, and Weddell's saddleback tamarins, Leontocebus weddelli (Callitrichidae). In total, 11 compounds of interest (i.e., probably derived from the animals) could be detected in the samples, with 31 of 215 samples containing at least one compound of interest….
    • Opportunities and challenges for conserving small populations: An emerging role for zoos in genetic rescue

      Ryder, Oliver A.; Minteer, Ben A.; Maienschein, Jane; Collins, James P. (University of Chicago PressChicago, IL, 2018)
      The growing commitment of zoos to address accelerated rates of extinction and losses of biodiversity utilizing the populations they manage has led to the exploration of options to rescue species from extinction, including advanced genetic and reproductive technologies. The availability of banked viable cell cultures, such as those held in collections like San Diego Zoo Global’s Frozen Zoo® and other facilities, may ultimately provide resources to reduce extinction risk of species for which appropriate samples have been collected....
    • 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.
    • Ovarian control and monitoring in amphibians

      Calatayud, Natalie E.; Stoops, M.; Durrant, Barbara S. (2018)
      Amphibian evolution spans over 350 million years ago, consequently this taxonomic group displays a wide, complex array of physiological adaptations and their diverse modes of reproduction are a prime example. Reproduction can be affected by taxonomy, geographic and altitudinal distribution, and environmental factors....
    • Ovulation induction in anovulatory southern white rhinoceros (Ceratotherium simum simum) without altrenogest

      Pennington, Parker M.; Marshall, Kira L.; Capiro, Jonnie M.; Felton, Rachel G.; Durrant, Barbara S. (2019)
      Lack of ovulation is common in captive southern white rhino females and contributes to poor reproductive success. We show that ovulation can be induced efficien
    • Oxytocin and vasopressin receptor gene variation as a proximate base for inter- and intraspecific behavioral differences in bonobos and chimpanzees

      Staes, Nicky; Stevens, Jeroen M. G.; Helsen, Philippe; Hillyer, Mia; Korody, Marisa L.; Eens, Marcel (2014)
      Recent literature has revealed the importance of variation in neuropeptide receptor gene sequences in the regulation of behavioral phenotypic variation. Here we focus on polymorphisms in the oxytocin receptor gene (OXTR) and vasopressin receptor gene 1a (Avpr1a) in chimpanzees and bonobos. In humans, a single nucleotide polymorphism (SNP) in the third intron of OXTR (rs53576 SNP (A/G)) is linked with social behavior, with the risk allele (A) carriers showing reduced levels of empathy and prosociality. Bonobos and chimpanzees differ in these same traits, therefore we hypothesized that these differences might be reflected in variation at the rs53576 position. We sequenced a 320 bp region surrounding rs53576 but found no indications of this SNP in the genus Pan. However, we identified previously unreported SNP variation in the chimpanzee OXTR sequence that differs from both humans and bonobos. Humans and bonobos have previously been shown to have a more similar 5' promoter region of Avpr1a when compared to chimpanzees, who are polymorphic for the deletion of ~360 bp in this region (+/- DupB) which includes a microsatellite (RS3). RS3 has been linked with variation in levels of social bonding, potentially explaining part of the interspecies behavioral differences found in bonobos, chimpanzees and humans. To date, results for bonobos have been based on small sample sizes. Our results confirmed that there is no DupB deletion in bonobos with a sample size comprising approximately 90% of the captive founder population, whereas in chimpanzees the deletion of DupB had the highest frequency. Because of the higher frequency of DupB alleles in our bonobo population, we suggest that the presence of this microsatellite may partly reflect documented differences in levels of sociability found in bonobos and chimpanzees.
    • Panda downlisted but not out of the woods

      Swaisgood, Ronald R.; Wang, Dajun; Wei, Fuwen (2018)
      The giant panda (Ailuropoda melanoleuca) is no longer Endangered on the International Union for the Conservation of Nature's (IUCN) storied Red List. The decision to downlist the panda to Vulnerable has its foundation in a systematic assessment of population parameters as determined by China State Forestry Administration's circa decadal national survey and other scientific outputs, compared to standardized criteria used by IUCN to determine the status of all species. This decision has not been without controversy and disagreement, perhaps reflecting disparities between how people view the term “Endangered” and the criteria established by the IUCN. Here, we explore the architecture of recovery of this iconic “Endangered” species, make transparent the process of the IUCN downlisting decision, evaluate emerging threats to pandas on the horizon, and contemplate the meaning of this milestone for endangered species conservation. Through this revelation, we find profound reasons for hope for species conservation everywhere, and a useful example of success in the making. However, this positive message comes with measured caution. The Chinese government and conservation community must maintain its focus and investment on panda conservation, and contend with strategies to address new threats. If they do not, the panda will return to “Endangered” status once again.
    • Pandemic (H1N1) 2009 virus in 3 wildlife species, San Diego, California, USA

      Schrenzel, Mark D.; Tucker, Tammy A.; Stalis, Ilse H.; Kagan, Rebecca A.; Burns, Russell P.; Denison, Amy M.; Drew, Clifton P.; Paddock, Christopher D.; Rideout, Bruce (2011)
      The influenza A pandemic (H1N1) 2009 virus rapidly created a global pandemic among humans and also appears to have strong infectivity for a broad range of animal species (1–3). The virus has been found repeatedly in swine and has been detected in a dog, cats, turkeys, and domestic ferrets and in nondomestic animals, including skunks, cheetahs, and giant anteaters (2–4). In some cases, animal-to-animal transmission may have occurred, raising concern about the development of new wildlife reservoirs. In 2009, the first recognized occurrence of pandemic (H1N1) 2009 in southern California in April was followed by a surge of cases during October through November (4). During this time, respiratory illness developed in a 12-year-old male American badger (Taxidea taxus taxus), a 19-year-old female Bornean binturong (Arctictis binturong penicillatus), and a 7-year-old black-footed ferret (Mustela nigripes) housed in a San Diego zoological garden....
    • Past experiences and future expectations generate context-dependent costs of foraging

      Berger-Tal, Oded; Embar, Keren; Kotler, Burt P.; Saltz, David (2014)
      We released Allenby’s gerbils (Gerbillus andersoni allenbyi) into an enclosure containing rich patches with equal amounts of food and manipulated the quality of the environment over time by reducing the amount of food in most (but not all) food patches and then increasing it again…. Specifically, in the second rich period, the gerbils spent more time foraging and harvested more food from the patches. Thus, seemingly identical environments can be treated as strikingly different by foragers as a function of their past experiences and future expectations.