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Using Gene Transcription to Assess Ecological and Anthropological Stressors in Brown Bears

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Abstract

Increasingly, population- and ecosystem-level health assessments are performed using sophisticated molecular tools. Advances in molecular technology enable the identification of synergistic effects of multiple stressors on the individual physiology of different species. Brown bears (Ursus arctos) are an apex predator; thus, they are ideal candidates for detecting potentially ecosystem-level systemic perturbations using molecular-based tools. We used gene transcription to analyze 130 brown bear samples from three National Parks and Preserves in Alaska. Although the populations we studied are apparently stable in abundance and exist within protected and intact environments, differences in transcript profiles were noted. The most prevalent differences were among locations. The transcript patterns among groups reflect the influence of environmental factors, such as nutritional status, disease, and xenobiotic exposure. However, these profiles also likely represent baselines for each unique environment by which future measures can be made to identify early indication of population-level changes due to, for example, increasing Arctic temperatures. Some of those environmental changes are predicted to be potentially positive for brown bears, but other effects such as the manifestation of disease or indirect effects of oceanic acidification may produce negative impacts.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215:403-410

    Article  PubMed  CAS  Google Scholar 

  • Bowen L, Aldridge B, Godinez C, Zavala A, Lowenstine L, Stott JL, Johnson ML (2006) MHC gene configuration variation in geographically disparate populations of California sea lion (Zalophus californianus): pathogen pressure or breeding biology? Molecular Ecology 15:529-533

    Article  PubMed  CAS  Google Scholar 

  • Bowen L, Riva F, Mohr C, Aldridge B, Schwartz J, Miles AK, Stott JL (2007) Differential gene expression induced by exposure of captive mink to fuel oil: a model for the sea otter. EcoHealth 4:298-309

    Article  Google Scholar 

  • Bowen L, Miles AK, Murray M, Haulena M, Tuttle J, Van Bonn W, Adams L, Bodkin JL, Ballachey B, Estes J, Tinker MT, Keister R, Stott JL (2012) Gene transcription in sea otters (Enhydra lutris); emerging diagnostics in marine mammal and ecosystem health. Molecular Ecology Resources 12:67-74

    Article  PubMed  CAS  Google Scholar 

  • Bowen L, Miles AK, Stott JL, Waters S, Atwood T (2015) Enhanced biological processes associated with alopecia in polar bears (Ursus maritimus). Science of the Total Environment 529:114-120

    Article  PubMed  CAS  Google Scholar 

  • Bowen L, Miles AK, Ballachey B, Waters S, Bodkin JL (2016) Gene transcript profiling in sea otters post-Exxon Valdez oil spill: A tool for marine ecosystem health assessment. Journal of Marine Science and Engineering 4:39-51

    Article  Google Scholar 

  • Burek KA, Gulland FMS, O’Hara TM (2008) Effects of climate change on Arctic marine mammal health. Ecological Applications 18:126-134

    Article  Google Scholar 

  • Chen Z, Wang H, Matsumura K, Qian P (2012) Expression of calmodulin and myosin light chain kinase during larval settlement of the barnacle Balanus Amphitrite. PLoS One 7:e31337

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Maio A (1999) Heat shock proteins: facts, thoughts, and dreams. Shock 11:1-12

    Article  PubMed  Google Scholar 

  • Dong L, Ma Q, Whitlock JP Jr (1997) Down-regulation of major histocompatibility complex Q1b gene expression by 2,3,7,8-tetrachlorodibenzo-p-dioxin. The Journal of Biological Chemistry 272:29614-29619

    Article  PubMed  CAS  Google Scholar 

  • Dubansky B, Whitehead A, Miller JT, Rice C, Galvez F (2013) Multi-tissue molecular, genomic, and developmental effects of the Deepwater Horizon oil spill on resident Gulf killifish (Fundulus grandis). Environmental Science & Technology 47:5074-5082

    Article  CAS  Google Scholar 

  • Elmendorf, SC, Henry GHR, Hollister RD, Björk RG, Boulanger-Lapointe N, Cooper EJ, Cornelissen JHC, Day TA, Dorrepaal E, Elumeeva TG, Gill M, Gould WA, Harte J, Hik DS, Hofgaard A, Johnson DR, Johnstone JF, Jónsdóttir IS, Jorgenson JC, Klanderud K, Klein JA, Koh S, Kudo G, Lara M, Lévesque E, Magnússon B, May JL, Mercado-Dı´az JA, Michelsen A, Molau U, Myers-Smith IH, Oberbauer SF, Onipchenko VG, Rixen C, Schmidt NM, Shaver GR, Spasojevic MJ, Þórhallsdóttir PE, Tolvanen A, Troxler T, Tweedie CE, Villareal S, Wahren CH, Walker X, Webber PJ, Welker JM, Wipf S (2012) Plot-scale evidence of tundra vegetation change and links to recent summer warming. Nature Climate Change 2:453-457

    Article  Google Scholar 

  • Goldsby RA, Kindt TJ, Osborne BA, Kuby J (2003) Immunology, 5th ed., New York: WH Freeman and Company

    Google Scholar 

  • Graham AL, Shuker DM, Pollitt LC, Auld SKJR, Wilson AJ, Little TJ (2010) Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Functional Ecology 25:1-13

    Google Scholar 

  • Gurish MF, Humbles A, Tao H, Finkelstein S, Boyce JA, Gerard C, Friend DS, Austen KF (2002) CCR3 is required for tissue eosinophilia and larval cytotoxicity after infection with Trichinella spiralis. Journal of Immunology 168:5730-5736

    Article  CAS  Google Scholar 

  • Harris SG, Padilla J, Koumas L, Ray D, Phipps RP (2002) Prostaglandins as modulators of immunity. Trends in Immunology 23:144-150

    Article  PubMed  CAS  Google Scholar 

  • Hilderbrand GV, Schwartz CC, Robbins CT, Hanley TA (2000) Effect of Hibernation and Reproductive Status on Body Mass and Condition of Coastal Brown Bears. Journal of Wildlife Management 64:176-183

    Article  Google Scholar 

  • Hilderbrand, GV, Joly, K, Rabinowitch SP, Shults B (2013) Wildlife stewardship in National Park Service areas in Alaska: A report to the Alaska Leadership Council Sub-group on Wildlife Harvest on Parklands, Natural Resource Report NPS/AKSO/NRR—2013/663, Fort Collins, Colorado: National Park Service

    Google Scholar 

  • Iwama GK, Mathilakath MV, Forsyth RB, Ackerman PA (1999) Heat shock proteins and physiological stress in fish. American Zoologist 39:901-909

    Article  CAS  Google Scholar 

  • Joly K, Duffy PA, Rupp TS (2012) Simulating the effects of climate change on fire regimes in Arctic biomes: implications for caribou and moose habitat. Ecosphere 3:1-18

    Article  Google Scholar 

  • Kibenge MJT, Munir K, Kibenge FSB (2005) Constitutive expression of Atlantic salmon Mx1 protein in CHSE-214 cells confers resistance to Infectious Salmon Anaemia virus. Virology Journal 2:75

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kringel H, Iburg T, Dawson H, Aasted B, Roepstorff A (2006) A time course study of immunological responses in Trichuris suis infected pigs demonstrates induction of a local type 2 response associated with worm burden. International Journal of Parasitology 36: 915-924

    Article  PubMed  CAS  Google Scholar 

  • Mangipane LS, Belant JL, Lafferty DJR, Gustine DD, Hiller TL, Colvin ME, Mangipane BA, Hilderbrand GV (in press) Dietary plasticity in a nutrient-rich system does not influence brown bear (Ursus arctos) body condition or denning Polar Biology

  • Martin LB, Hopkins WA, Mydlarz LD, Rohr JR (2010) The effects of anthropogenic global changes on immune functions and disease resistance. Annuals of the New York Academy of Sciences 1195:129-148

    Article  Google Scholar 

  • McLoughlin K, Turteltaub K, Bankaitis-Davis D, Gerren R, Siconolfi L, Storm K, Cheronis J, Trollinger D, Macejak D, Tryon V, Bevilacqua M (2006) Limited dynamic range of immune response gene expression observed in healthy blood donors using RT-PCR. Molecular Medicine 12:185-195

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miles AK, Bowen L, Ballachey BE, Bodkin JL, Murray M, Estes JL, Keister RA, Stott JL (2012) Variation in transcript profiles in sea otters (Enhydra lutris) from Prince William Sound, Alaska and clinically normal reference otters. Marine Ecology Progress Series 451:201-212

    Article  Google Scholar 

  • Moll HP, Maier T, Zommer A, Lavoie T, Brostjan C (2011) The differential activity of interferon-a subtypes is consistent among distinct target genes and cell types. Cytokine 53:52-59

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nielsen SE, Cattet MRL, Boulanger J, Cranston J, McDermid GJ, Shafer ABA, Stenhouse GB (2013) Environmental, biological and anthropogenic effects on grizzly bear body size: temporal and spatial considerations. BMC Ecology 13:13-31

    Article  Google Scholar 

  • Oesch-Bartlomowicz B, Oesch F (2005) Phosphorylation of cytochromes P450: first discovery of a posttranslational modification of a drug-metabolizing enzyme. Biochemical and Biophysical Research Communications 338:446-449

    Article  PubMed  CAS  Google Scholar 

  • Quintana FJ, Basso AS, Iglesias AH, Korn T, Farez, MF, Bettelli E, Caccamo M, Oukka M, Weiner HL (2008) Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453:6-7

    Article  CAS  Google Scholar 

  • Parham P (2015) The Immune System, 4th ed., New York: Garland Science, Taylor and Francis Group, LLC

    Google Scholar 

  • R Development Core Team (2012) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available: http://www.R-project.org/

  • Robinson J, Waller M, Parham P, Bodmer JG, Marsh SGE (2001) IMGT/HLA Database – a sequence database for the human major histocompatibility complex. Nucleic Acids Research 29:210-213

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saucillo DC, Gerriets VA, Sheng J, Rathmell JC, MacIver NJ (2014) Leptin metabolically licenses T cells for activation to link nutrition and immunity. The Journal of Immunology 192:136-144

    Article  PubMed  CAS  Google Scholar 

  • Sellers RA, Miller SD (1999) Population dynamics of brown bears after the Exxon Valdez oil spill. Ursus 11:73-78

    Google Scholar 

  • Stanek A, Wolf N, Hilderbrand G, Mangipane B, Causey D, Welker J (2017) Seasonal foraging strategies of Alaskan grey wolves (Canis lupus) in a salmon subsidized ecosystem. Canadian Journal of Zoology

  • Tabuchi M, Veldhoen N, Dangerfield N, Jeffries S, Helbing CC, Ross PS (2006) PCB related alteration of thyroid hormones and thyroid hormone receptor gene expression in free-ranging harbor seals (Phoca vitulina). Environmental Health Perspectives 114:1024-1031

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Taylor W., Reynolds H., Ballard W (1989) Immobilization of grizzly bears with tiletamine hydrochloride and zolazepam hydrochloride. Journal of Wildlife Management 53:978-981.

    Article  Google Scholar 

  • Tsai MJ, O’Malley BW (1994) Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annual Review of Biochemistry 63:451-486

    Article  PubMed  CAS  Google Scholar 

  • Tsan M, Gao B (2004) Cytokine function of heat shock proteins. American Journal of Physiology-Cell Physiology 286:C739-C744

    Article  PubMed  CAS  Google Scholar 

  • Tumpey TM, Szretter KJ, Van Hoeven N, Katz JM, Kochs G, Haller O, García-Sastre A, Staeheli P (2007) The Mx1 gene protects mice against the pandemic 1918 and highly lethal human H5N1 influenza viruses. Journal of Virology 81:10818-10821

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van der Wal R, Stien A (2014) High-arctic plants like it hot: a long-term investigation of between-year variability in plant biomass. Ecology 95:3414-3427

    Article  Google Scholar 

  • Veldhoen M, Hirota K, Westendorf AM, Buer J, Dumoutier L, Renauld JC, Stockinger B (2008) The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453:106-109

    Article  PubMed  CAS  Google Scholar 

  • Wegner KM, Kalbe M, Rauch G, Kurtz J, Schaschl H, Reusch TBH (2006) Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Molecular Ecology 15:1153-1164

    Article  PubMed  CAS  Google Scholar 

  • Welch DW, Ishida Y, Nagasawa K (1998) Thermal limits and ocean migrations of sockeye salmon (Onorhynchus nerka): long-term consequences of global warming. Canadian Journal of Fisheries and Aquatic Sciences 55:937-948

    Article  Google Scholar 

  • Wilson RR, Gustine DD, Joly K (2014) Evaluating potential effects of an industrial road on winter habitat of caribou in north-central Alaska. Arctic 67: 472-482

    Article  Google Scholar 

  • Xu S, Cao X (2010) Interleukin-17 and its expanding biological functions. Cellular & Molecular Immunology 7:164-174

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank the following for their help which has been critical to the project: Biologists—Buck Mangipane, Lindsey Mangipane, Joy Erlenbach, Mathew Sorum, Matthew Cameron, and Andrea Morehouse; Wildlife Veterinarian J. Powers; Pilots—T. Cambier, R. Richotte, A. Greenblatt, J. DeCreeft, C. Cebulski, M. Keller, and J. Cummings. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Correspondence to Lizabeth Bowen.

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Bowen, L., Miles, A.K., Waters, S. et al. Using Gene Transcription to Assess Ecological and Anthropological Stressors in Brown Bears. EcoHealth 15, 121–131 (2018). https://doi.org/10.1007/s10393-017-1287-0

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  • DOI: https://doi.org/10.1007/s10393-017-1287-0

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