• A high density snp array for the domestic horse and extant Perissodactyla: Utility for association mapping, genetic diversity, and phylogeny studies

      McCue, Molly E.; Bannasch, Danika L.; Petersen, Jessica L.; Gurr, Jessica; Bailey, Ernie; Binns, Matthew M.; Distl, Ottmar; Guérin, Gérard; Hasegawa, Telhisa; Hill, Emmeline W.; et al. (2012)
      An equine SNP genotyping array was developed and evaluated on a panel of samples representing 14 domestic horse breeds and 18 evolutionarily related species. More than 54,000 polymorphic SNPs provided an average inter-SNP spacing of ?43 kb. The mean minor allele frequency across domestic horse breeds was 0.23, and the number of polymorphic SNPs within breeds ranged from 43,287 to 52,085. Genome-wide linkage disequilibrium (LD) in most breeds declined rapidly over the first 50–100 kb and reached background levels within 1–2 Mb. The extent of LD and the level of inbreeding were highest in the Thoroughbred and lowest in the Mongolian and Quarter Horse. Multidimensional scaling (MDS) analyses demonstrated the tight grouping of individuals within most breeds, close proximity of related breeds, and less tight grouping in admixed breeds. The close relationship between the Przewalski's Horse and the domestic horse was demonstrated by pair-wise genetic distance and MDS. Genotyping of other Perissodactyla (zebras, asses, tapirs, and rhinoceros) was variably successful, with call rates and the number of polymorphic loci varying across taxa. Parsimony analysis placed the modern horse as sister taxa to Equus przewalski. The utility of the SNP array in genome-wide association was confirmed by mapping the known recessive chestnut coat color locus (MC1R) and defining a conserved haplotype of -750 kb across all breeds. These results demonstrate the high quality of this SNP genotyping resource, its usefulness in diverse genome analyses of the horse, and potential use in related species.
    • 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.
    • Activation of southern white rhinoceros (Ceratotherium simum simum) estrogen receptors by phytoestrogens: Potential role in the reproductive failure of captive-born females?

      Tubbs, Christopher W.; Hartig, P.; Cardon, M.; Varga, Nicole; Milnes, Matthew R. (2012)
      The captive southern white rhinoceros (SWR; Ceratotherium simum simum) population serves as an important genetic reservoir critical to the conservation of this vulnerable species. Unfortunately, captive populations are declining due to the poor reproductive success of captive-born females....
    • Assessing California's Relocation Guidelines for Burrowing Owls Impacted by Renewable Energy Development.

      Hennessy, Sarah McCullough; Wisinski, Colleen; Ronan, Noelle; Gregory, Chris; Swaisgood, Ronald R.; Nordstrom, Lisa A. (California Energy Commission, 2020)
      Once common and widespread throughout the western United States and Canada, the western burrowing owl (Athene cunicularia hypugaea) population has declined to the point where the species is now designated as a Species of Special Concern in California. Their presence in development areas, including renewable energy facilities, necessitates an effective strategy for protecting them. This study is the first of its kind to test both passive and active relocation techniques with burrowing owls and evaluate their relative effectiveness with and without the addition of conspecific cues (such as acoustic playback of owl calls and imitation whitewash to attract the owls)....
    • Automated telemetry reveals post-reintroduction exploratory behavior and movement patterns of an endangered corvid, ʻAlalā (Corvus hawaiiensis) in Hawaiʻi, USA

      Smetzer, Jennifer R.; Greggor, Alison L.; Paxton, Kristina L.; Masuda, Bryce M.; Paxton, Eben H. (2021)
      Continuous movement monitoring is a powerful tool for evaluating reintroduction techniques and assessing how well reintroduced animals are adjusting to the wild. However, to date, continuous monitoring has only occurred for large-bodied species capable of carrying heavy tracking devices. In this study we used an automated VHF radio telemetry array to investigate the exploratory behavior and movement patterns of critically endangered ?Alal? (Corvus hawaiiensis), reintroduced to the Island of Hawai?i in 2017. The 11 juvenile ?Alal? we tracked exhibited high site fidelity and initial survival. Over time the birds showed decreased time spent at the supplemental feeders, and transitioned to more focused use of the landscape, suggesting increased foraging on wild food items. Birds with seemingly less spatial neophobia at release also made larger post-release exploratory movements. This study provides the first evidence that 1) supplemental feeding can support site fidelity for reintroduced ?Alal? without restricting a transition to independent foraging, and 2) that pre-release personality metrics may be useful predictors for predicting post-release movements of ?Alal?. Our work is the first to demonstrate the utility and power of automated telemetry for monitoring the reintroduction of small species.
    • Behavioral diversity as a potential indicator of positive animal welfare

      Miller, Lance J.; Vicino, Greg A.; Sheftel, Jessica; Lauderdale, Lisa K. (2020)
      Modern day zoos and aquariums continuously assess the welfare of their animals and use evidence to make informed management decisions. Historically, many of the indicators of animal welfare used to assess the collection are negative indicators of welfare, such as stereotypic behavior. However, a lack of negative indicators of animal welfare does not demonstrate that an individual animal is thriving. There is a need for validated measures of positive animal welfare and there is a growing body of evidence that supports the use of behavioral diversity as a positive indicator of welfare. This includes an inverse relationship with stereotypic behavior as well as fecal glucocorticoid metabolites and is typically higher in situations thought to promote positive welfare. This review article highlights previous research on behavioral diversity as a potential positive indicator of welfare. Details are provided on how to calculate behavioral diversity and how to use it when evaluating animal welfare. Finally, the review will indicate how behavioral diversity can be used to inform an evidence-based management approach to animal care and welfare.
    • Chromosome painting in Tragulidae facilitates the reconstruction of Ruminantia ancestral karyotype

      Kulemzina, Anastasia I.; Yang, Fengtang; Trifonov, Vladimir A.; Ryder, Oliver A.; Ferguson-Smith, Malcolm A.; Graphodatsky, Alexander S. (2011)
      ...Here, we present the first genome-wide comparative map of the Java mouse deer (Tragulus javanicus, Tragulidae) revealed by chromosome painting with human and dromedary probes. Together with the published comparative maps of major representative cetartiodactyl species established with the same set of probes, our results allowed us to reconstruct a 2n = 48 Ruminantia ancestral karyotype, which is similar to the cetartiodactyl ancestral karyotype....
    • Co-designing behavior change interventions to conserve biodiversity

      Bowie, Matthew J.; Dietrich, Timo; Cassey, Phillip; Veríssimo, Diogo (2020)
      Many threats to biodiversity are the result of human actions, which means that changing human behavior can positively alter the trajectory of our current biodiversity crisis. While there is an increasing number of behavior change interventions being implemented in biodiversity conservation, their design is rarely informed by the people they try to influence, thereby lowering the probability of success. Building successful interventions requires substantial audience research, but this can be challenging for conservation projects with perennially limited time and resources. Here, we critically discuss co-design as a useful and effective approach for gathering audience insights relatively quickly, allowing conservation practitioners to integrate end-user voices when they would otherwise be excluded from intervention design. Specifically, we present a seven-step co-design process, providing an outline and guidance for how to generate more user-centric intervention ideas and transform them into feasible prototype interventions. Further, we show how we applied this seven-step process with coffee consumers in a sustainable conservation context. This study outlines contributions that showcase the value of user-centered design approaches to behavior change interventions for biodiversity conservation.
    • Collecting and maintaining exceptional species in tissue culture and cryopreservation

      Pence, Valerie; Westwood, Murphy; Maschinski, Joyce; Powell, Christy; Sugii, Nellie; Fish, Diana; McGuinness, Julianne; Raven, Pat; Duval, Julian; Herrera-Mishler, Tomas; et al. (Center for Plant ConservationEscondido, California, 2019)
      Tissue culture and cryopreservation are alternative storage methods for exceptional species that produce few seeds or seed that are intolerant to drying or freezing. Adequately storing exceptional species requires specialized expertise, infrastructure, and greater resources than conventional seed storage....
    • 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.
    • Deciphering genetic mate choice: Not so simple in group-housed conservation breeding programs

      Farquharson, Katherine A.; Hogg, Carolyn J.; Belov, Katherine; Grueber, Catherine E. (2020)
      Incorporating mate choice into conservation breeding programs can improve reproduction and the retention of natural behaviors. However, different types of genetic-based mate choice can have varied consequences for genetic diversity management. As a result, it is important to examine mechanisms of mate choice in captivity to assess its costs and benefits. Most research in this area has focused on experimental pairing trials; however, this resource-intensive approach is not always feasible in captive settings and can interfere with other management constraints. We used generalized linear mixed models and permutation approaches to investigate overall breeding success in group-housed Tasmanian devils at three nonmutually exclusive mate choice hypotheses: (a) advantage of heterozygous individuals, (b) advantage of dissimilar mates, and (c) optimum genetic distance, using both 1,948 genome-wide SNPs and 12 MHC-linked microsatellites. The managed devil insurance population is the largest such breeding program in Australia and is known to have high variance in reproductive success. We found that nongenetic factors such as age were the best predictors of breeding success in a competitive breeding scenario, with younger females and older males being more successful. We found no evidence of mate choice under the hypotheses tested. Mate choice varies among species and across environments, so we advocate for more studies in realistic captive management contexts as experimental or wild studies may not apply. Conservation managers must weigh up the need to wait for adequate sample sizes to detect mate choice with the risk that genetic changes may occur during this time in captivity. Our study shows that examining and integrating mate choice into the captive management of species housed in realistic, semi-natural group-based contexts may be more difficult than previously considered.
    • Development of a SNP-based assay for measuring genetic diversity in the Tasmanian devil insurance population

      Wright, Belinda; Morris, Katrina; Grueber, Catherine E.; Willet, Cali E.; Gooley, Rebecca; Hogg, Carolyn J.; O’Meally, Denis; Hamede, Rodrigo; Jones, Menna; Wade, Claire; et al. (2015)
      The Tasmanian devil (Sarcophilus harrisii) has undergone a recent, drastic population decline due to the highly contagious devil facial tumor disease. The tumor is one of only two naturally occurring transmissible cancers and is almost inevitably fatal. In 2006 a disease-free insurance population was established to ensure that the Tasmanian devil is protected from extinction. The insurance program is dependent upon preserving as much wild genetic diversity as possible to maximize the success of subsequent reintroductions to the wild. Accurate genotypic data is vital to the success of the program to ensure that loss of genetic diversity does not occur in captivity. Until recently, microsatellite markers have been used to study devil population genetics, however as genetic diversity is low in the devil and potentially decreasing in the captive population, a more sensitive genotyping assay is required.
    • Effects of season and social interaction on fecal testosterone in wild male giant pandas: implications for energetics and mating strategies

      Nie, Y.; Zhang, Z.; Swaisgood, Ronald R.; Wei, F. (2012)
      In the first-ever study of reproductive endocrinology in wild male giant pandas (Ailuropoda melanoleuca), we provide new insights into the reproductive ecology of the species. We tracked and observed pandas in Foping Nature Reserve of the Qinling Mountains for 3 years, collecting fecal samples for testosterone metabolite analysis and data on reproductive activity....
    • Elaeophora in the meninges of a Malayan sambar (Rusa unicolor equina)

      Bernard, Jennifer; Grunenwald, Caroline; Stalis, Ilse H.; Varney, Megan; Zuba, Jeffery R.; Gerhold, Richard (2016)
      An adult nematode was grossly identified in the meninges of a Malayan sambar (Rusa unicolor equina), with numerous microfilariae associated with encephalitis and vasculitis on histopathology. The nematode was confirmed to be Elaeophora schneideri by sequencing a portion of the 18S rRNA gene. Our report highlights the potential for aberrant migration of E. schneideri in exotic deer species and the use of advanced testing to specifically identify this metazoan parasite, avoiding misidentification of Parelaphostrongylus tenuis.
    • Fat-soluble vitamin and mineral comparisons between zoo-based and free-ranging koalas (phascolarctos cinereus)

      Schmidt, Debra A.; Pye, Geoffrey W.; Hamlin-Andrus, Chris C.; Ellis, William A.; Ellersieck, Mark R.; Chen, Tai C.; Holick, Michael F. (2013)
      As part of a health investigation on koalas at San Diego Zoo, serum samples were analyzed from 18 free-ranging and 22 zoo-based koalas, Phascolarctos cinereus. Serum concentrations of calcium, chloride, cobalt, copper, iron, magnesium, manganese, molybdenum, phosphorus, potassium, selenium, sodium, zinc, and vitamins A, E, and 25(OH)D3 were quantified....
    • Funding should come to those who wait

      Swaisgood, Ronald R.; Terborgh, John W.; Blumstein, Daniel T.; (2010)
      ... If long-term research is to flourish, we must build a reward system for studies characterized by deferred gratification. A sea change in these values must precede attempts to address funding....
    • Genomic insights into a contagious cancer in Tasmanian devils

      Grueber, Catherine E.; Peel, Emma; Gooley, Rebecca; Belov, Katherine (2015)
      The Tasmanian devil faces extinction due to a contagious cancer…. From characterising immune genes and immune responses to studying tumour evolution, we have begun to uncover how a cancer can be ‘caught’ and are using genomic data to manage an insurance population of disease-free devils for the long-term survival of the species.
    • 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....
    • Immunomics of the koala (Phascolarctos cinereus)

      Abts, Kendra C.; Ivy, Jamie A.; DeWoody, J. Andrew (2015)
      The study of the koala transcriptome has the potential to advance our understanding of its immunome—immunological reaction of a given host to foreign antigens—and to help combat infectious diseases (e.g., chlamydiosis) that impede ongoing conservation efforts….. Our efforts have produced full-length sequences for potentially important immune genes in koala, which should serve as targets for future investigations that aim to conserve koala populations.
    • Inbreeding and selection shape genomic diversity in captive populations: Implications for the conservation of endangered species

      Willoughby, Janna R.; Ivy, Jamie A.; Lacy, Robert C.; Doyle, Jacqueline M.; DeWoody, J. Andrew (2017)
      Captive breeding programs are often initiated to prevent species extinction until reintroduction into the wild can occur. However, the evolution of captive populations via inbreeding, drift, and selection can impair fitness, compromising reintroduction programs. To better understand the evolutionary response of species bred in captivity, we used nearly 5500 single nucleotide polymorphisms (SNPs) in populations of white-footed mice (Peromyscus leucopus) to measure the impact of breeding regimes on genomic diversity. We bred mice in captivity for 20 generations using two replicates of three protocols: random mating (RAN), selection for docile behaviors (DOC), and minimizing mean kinship (MK). The MK protocol most effectively retained genomic diversity and reduced the effects of selection. Additionally, genomic diversity was significantly related to fitness, as assessed with pedigrees and SNPs supported with genomic sequence data. Because captive-born individuals are often less fit in wild settings compared to wild-born individuals, captive-estimated fitness correlations likely underestimate the effects in wild populations. Therefore, minimizing inbreeding and selection in captive populations is critical to increasing the probability of releasing fit individuals into the wild.