View Item 

Show simple item record

Early life social and ecological determinants of global DNA methylation in wild spotted hyenas
dc.contributor.authorLaubach, Zachary M.
dc.contributor.authorFaulk, Christopher D.
dc.contributor.authorDolinoy, Dana C.
dc.contributor.authorMontrose, Luke
dc.contributor.authorJones, Tamara R.
dc.contributor.authorRay, Donna
dc.contributor.authorPioon, Malit O.
dc.contributor.authorHolekamp, Kay E.
dc.date.accessioned2019-10-30T15:31:21Z
dc.date.availableWITHHELD_11_MONTHS
dc.date.available2019-10-30T15:31:21Z
dc.date.issued2019-08
dc.identifier.citationLaubach, Zachary M.; Faulk, Christopher D.; Dolinoy, Dana C.; Montrose, Luke; Jones, Tamara R.; Ray, Donna; Pioon, Malit O.; Holekamp, Kay E. (2019). "Early life social and ecological determinants of global DNA methylation in wild spotted hyenas." Molecular Ecology 28(16): 3799-3812.
dc.identifier.issn0962-1083
dc.identifier.issn1365-294X
dc.identifier.urihttps://hdl.handle.net/2027.42/151897
dc.description.abstractEnvironmental factors early in life can have lasting influence on the development and phenotypes of animals, but the underlying molecular modifications remain poorly understood. We examined cross‐sectional associations among early life socioecological factors and global DNA methylation in 293 wild spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya, grouped according to three age classes (cub, subadult and adult). Explanatory variables of interest included annual maternal rank based on outcomes of dyadic agonistic interactions, litter size, wild ungulate prey density and anthropogenic disturbance in the year each hyena was born based on counts of illegal livestock in the Reserve. The dependent variable of interest was global DNA methylation, assessed via the LUminometric Methylation Assay, which provides a percentage methylation value calculated at CCGG sites across the genome. Among cubs, we observed approximately 2.75% higher CCGG methylation in offspring born to high‐ than low‐ranking mothers. Among cubs and subadults, higher anthropogenic disturbance corresponded with greater %CCGG methylation. In both cubs and adults, we found an inverse association between prey density measured before a hyena was 3 months old and %CCGG methylation. Our results suggest that maternal rank, anthropogenic disturbance and prey availability early in life are associated with later life global DNA methylation. Future studies are required to understand the extent to which these DNA methylation patterns relate to adult phenotypes and fitness outcomes.
dc.publisherUniversity of Chicago Press
dc.publisherWiley Periodicals, Inc.
dc.subject.otherDevelopmental Origins of Health and Disease
dc.subject.othermammals
dc.subject.othersocial environment
dc.subject.otherDNA methylation
dc.titleEarly life social and ecological determinants of global DNA methylation in wild spotted hyenas
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelEcology and Evolutionary Biology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/151897/1/mec15174_am.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/151897/2/mec15174.pdf
dc.identifier.doi10.1111/mec.15174
dc.identifier.sourceMolecular Ecology
dc.identifier.citedreferenceObermann‐Borst, S. A., Heijmans, B. T., Eilers, P. H. C., Tobi, E. W., Steegers, E. A. P., Slagboom, P. E., & Steegers‐Theunissen, R. P. M. ( 2012 ). Periconception maternal smoking and low education are associated with methylation of INSIGF in children at the age of 17 months. Journal of Developmental Origins of Health and Disease, 3 ( 5 ), 315 – 320. https://doi.org/10.1017/S2040174412000293
dc.identifier.citedreferenceNeedham, B. L., Smith, J. A., Zhao, W., Wang, X. U., Mukherjee, B., Kardia, S. L. R., … Diez Roux, A. V. ( 2015 ). Life course socioeconomic status and DNA methylation in genes related to stress reactivity and inflammation: The multi‐ethnic study of atherosclerosis. Epigenetics, 10 ( 10 ), 958 – 969. https://doi.org/10.1080/15592294.2015.1085139
dc.identifier.citedreferenceOno, H., Iwasaki, M., Kuchiba, A., Kasuga, Y., Yokoyama, S., Onuma, H., … Tsugane, S. ( 2012 ). Association of dietary and genetic factors related to one‐carbon metabolism with global methylation level of leukocyte DNA. Cancer Science, 103 ( 12 ), 2159 – 2164. https://doi.org/10.1111/cas.12013
dc.identifier.citedreferencePainter, R. C., Roseboom, T. J., & Bleker, O. P. ( 2005 ). Prenatal exposure to the Dutch famine and disease in later life: An overview. Reproductive Toxicology, 20 ( 3 ), 345 – 352. https://doi.org/10.1016/j.reprotox.2005.04.005
dc.identifier.citedreferencePerng, W., Rozek, L. S., Mora‐Plazas, M., Duchin, O., Marin, C., Forero, Y., … Villamor, E. ( 2012 ). Micronutrient status and global DNA methylation in school‐age children. Epigenetics, 7 ( 10 ), 1133 – 1141. https://doi.org/10.4161/epi.21915
dc.identifier.citedreferenceProvencal, N., Suderman, M. J., Guillemin, C., Massart, R., Ruggiero, A., Wang, D., … Szyf, M. ( 2012 ). The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells. Journal of Neuroscience, 32 ( 44 ), 15626 – 15642. https://doi.org/10.1523/JNEUROSCI.1470-12.2012
dc.identifier.citedreferenceRazin, A., & Riggs, A. D. ( 1980 ). DNA methylation and gene function. Science, 210, 604 – 610. https://doi.org/10.1126/science.6254144
dc.identifier.citedreferenceRothman, K. J. ( 1990 ). No adjustments are needed for multiple comparisons. Epidemiology, 1 ( 1 ), 43 – 46. https://doi.org/10.1097/00001648-199001000-00010
dc.identifier.citedreferenceSapolsky, R. M. ( 2005 ). The influence of social hierarchy on primate health. Science, 308 ( 5722 ), 648 – 652. https://doi.org/10.1126/science.1106477
dc.identifier.citedreferenceSchübeler, D. ( 2015 ). Function and information content of DNA methylation. Nature, 517 ( 7534 ), 321 – 326. https://doi.org/10.1038/nature14192
dc.identifier.citedreferenceSchulz, W. A. ( 2006 ). L1 retrotransposons in human cancers. Journal of Biomedicine and Biotechnology, 2006 ( 1 ), 83672. https://doi.org/10.1155/JBB/2006/83672
dc.identifier.citedreferenceSlotkin, R. K., & Martienssen, R. ( 2007 ). Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics, 8 ( 4 ), 272 – 285. https://doi.org/10.1038/nrg2072
dc.identifier.citedreferenceSmale, L., Frank, L. G., & Holekamp, K. E. ( 1993 ). Ontogeny of dominance in free‐living spotted hyaenas: Juvenile rank relations with adult females and immigrant males. Animal Behaviour, 46 ( 3 ), 467 – 477. https://doi.org/10.1006/anbe.1993.1215
dc.identifier.citedreferenceSmith, J. E., Memenis, S. K., & Holekamp, K. E. ( 2007 ). Rank‐related partner choice in the fission‐fusion society of the spotted hyena ( Crocuta crocuta ). Behavioral Ecology and Sociobiology, 61 ( 5 ), 753 – 765. https://doi.org/10.1007/s00265-006-0305-y
dc.identifier.citedreferenceSubramanyam, M. A., Diez‐Roux, A. V., Pilsner, J. R., Villamor, E., Donohue, K. M., Liu, Y., & Jenny, N. S. ( 2013 ). Social factors and leukocyte DNA methylation of repetitive sequences: The Multi‐Ethnic Study of Atherosclerosis. PLoS ONE, 8 ( 1 ), e54018. https://doi.org/10.1371/journal.pone.0054018
dc.identifier.citedreferenceSwanson, E. M., Dworkin, I., & Holekamp, K. E. ( 2011 ). Lifetime selection on a hypoallometric size trait in the spotted hyena. Proceedings of the Royal Society B: Biological Sciences, 278, 3277 – 3285. https://doi.org/10.1098/rspb.2010.2512
dc.identifier.citedreferenceTilson, R. L., & Hamilton, W. J. ( 1984 ). Social dominance and feeding patterns of spotted hyaenas. Animal Behaviour, 32 ( 3 ), 715 – 724. https://doi.org/10.1016/S0003-3472(84)80147-5
dc.identifier.citedreferenceTobi, E. W., Lumey, L. H., Talens, R. P., Kremer, D., Putter, H., Stein, A. D., … Heijmans, B. T. ( 2009 ). DNA methylation differences after exposure to prenatal famine are common and timing‐ and sex‐specific. Human Molecular Genetics, 18 ( 21 ), 4046 – 4053. https://doi.org/10.1093/hmg/ddp353
dc.identifier.citedreferenceTuck‐Muller, C. M., Narayan, A., Tsien, F., Smeets, D., Sawyer, J., Fiala, E. S., … Ehrlich, M. ( 2000 ). DNA hypomethylation and unusual chromosome instability in cell lines from ICF syndrome patients. Cytogenetics and Cell Genetics, 89, 121 – 128. https://doi.org/10.1159/000015590
dc.identifier.citedreferenceTung, J., Barreiro, L. B., Johnson, Z. P., Hansen, K. D., Michopoulos, V., Toufexis, D., … Gilad, Y. ( 2012 ). Social environment is associated with gene regulatory variation in the rhesus macaque immune system. Proceedings of the National Academy of Sciences of the United States of America, 109 ( 17 ), 6490 – 6495. https://doi.org/10.1073/pnas.1202734109
dc.identifier.citedreferenceVirani, S., Dolinoy, D. C., Halubai, S., Jones, T. R., Domino, S. E., Rozek, L. S., … Padmanabhan, V. ( 2012 ). Delivery type not associated with global methylation at birth. Clinical Epigenetics, 4 ( 1 ), 8. https://doi.org/10.1186/1868-7083-4-8
dc.identifier.citedreferenceVryer, R., & Saffery, R. ( 2017 ). What’s in a name? Context‐dependent significance of ‘global’ methylation measures in human health and disease. Clinical Epigenetics, 9, 2. https://doi.org/10.1186/s13148-017-0311-0
dc.identifier.citedreferenceWaterland, R. A., Kellermayer, R., Laritsky, E., Rayco‐Solon, P., Harris, R. A., Travisano, M., … Prentice, A. M. ( 2010 ). Season of conception in rural gambia affects DNA methylation at putative human metastable epialleles. PLoS Genetics, 6 ( 12 ), e1001252. https://doi.org/10.1371/journal.pgen.1001252
dc.identifier.citedreferenceWaterland, R. A., & Michels, K. B. ( 2007 ). Epigenetic epidemiology of the developmental origins hypothesis. Annual Review of Nutrition, 27, 363 – 388. https://doi.org/10.1146/annurev.nutr.27.061406.093705
dc.identifier.citedreferenceWatts, H. E., Tanner, J. B., Lundrigan, B. L., & Holekamp, K. E. ( 2009 ). Post‐weaning maternal effects and the evolution of female dominance in the spotted hyena. Proceedings of the Royal Society B: Biological Sciences, 276 ( 1665 ), 2291 – 2298. https://doi.org/10.1098/rspb.2009.0268
dc.identifier.citedreferenceWeaver, I. C. G., Cervoni, N., Champagne, F. A., D’Alessio, A. C., Sharma, S., Seckl, J. R., … Meaney, M. J. ( 2004 ). Epigenetic programming by maternal behavior. Nature Neuroscience, 7 ( 8 ), 847 – 854. https://doi.org/10.1038/nn1276
dc.identifier.citedreferenceWoo, H. D., & Kim, J. ( 2012 ). Global DNA hypomethylation in peripheral blood leukocytes as a biomarker for cancer risk: A meta‐analysis. PLoS ONE, 7 ( 4 ), e34615. https://doi.org/10.1371/journal.pone.0034615
dc.identifier.citedreferenceAdalsteinsson, B. T., Gudnason, H., Aspelund, T., Harris, T. B., Launer, L. J., Eiriksdottir, G., … Gudnason, V. ( 2012 ). Heterogeneity in white blood cells has potential to confound DNA methylation measurements. PLoS ONE, 7 ( 10 ), 1 – 9. https://doi.org/10.1371/journal.pone.0046705
dc.identifier.citedreferenceAnderson, O. S., Sant, K. E., & Dolinoy, D. C. ( 2012 ). Nutrition and epigenetics: An interplay of dietary methyl donors, one‐carbon metabolism and DNA methylation. The Journal of Nutritional Biochemistry, 23 ( 8 ), 853 – 859. https://doi.org/10.1016/j.jnutbio.2012.03.003
dc.identifier.citedreferenceAppleton, A. A., Armstrong, D. A., Lesseur, C., Lee, J., Padbury, J. F., Lester, B. M., & Marsit, C. J. ( 2013 ). Patterning in placental 11‐B hydroxysteroid dehydrogenase methylation according to prenatal socioeconomic adversity. PLoS ONE, 8 ( 9 ), e74691. https://doi.org/10.1371/journal.pone.0074691
dc.identifier.citedreferenceBall, M. P., Li, J. B., Gao, Y., Lee, J.‐H., LeProust, E. M., Park, I.‐H., … Church, G. M. ( 2009 ). Targeted and genome‐scale strategies reveal gene‐body methylation signatures in human cells. Nature Biotechnology, 27 ( 4 ), 361 – 368. https://doi.org/10.1038/nbt.1533
dc.identifier.citedreferenceBarau, J., Teissandier, A., Zamudio, N., Roy, S., Nalesso, V., Hérault, Y., … Bourc’his, D. ( 2016 ). The DNA methyltransferase DNMT3C protects male germ cells from transposon activity. Science, 354 ( 6314 ), 909 – 912. https://doi.org/10.1126/science.aah5143
dc.identifier.citedreferenceBateson, P., Barker, D., Clutton‐Brock, T., Deb, D., D’Udine, B., Foley, R. A., … Sultan, S. E. ( 2004 ). Developmental plasticity and human health. Nature, 430 ( 6998 ), 419 – 421. https://doi.org/10.1038/nature02725
dc.identifier.citedreferenceBen‐Shlomo, Y., & Kuh, D. ( 2003 ). What is a life course approach to chronic disease epidemiology? Conceptual models in life course epidemiology. International Journal of Epidemiology, 31 ( 2 ), 285 – 293. https://doi.org/10.1093/ije/31.2.285
dc.identifier.citedreferenceBjornsson, T. H., Sigurdsson, M. I., Fallin, M. D., Irizarry, R. A., Aspelund, T., Cui, H., … Feinberg, A. P. ( 2008 ). Intra‐individual change over time in DNA methylation with familial clustering. Journal of American Medical Association, 299 ( 24 ), 2877 – 2883. https://doi.org/10.1001/jama.299.24.2877
dc.identifier.citedreferenceBoeke, C. E., Baccarelli, A., Kleinman, K. P., Burris, H. H., Litonjua, A. A., Rifas‐Shiman, S. L., … Gillman, M. ( 2012 ). Gestational intake of methyl donors and global LINE‐1 DNA methylation in maternal and cord blood: Prospective results from a folate‐replete population. Epigenetics, 7 ( 3 ), 253 – 260. https://doi.org/10.4161/epi.7.3.19082
dc.identifier.citedreferenceBush, N. R., Edgar, R. D., Park, M., MacIsaac, J. L., McEwen, L. M., Adler, N. E., … Boyce, W. T. ( 2018 ). The biological embedding of early‐life socioeconomic status and family adversity in children’s genome‐wide DNA methylation. Epigenomics, 10 ( 11 ), 1445 – 1461. https://doi.org/10.2217/epi-2018-0042
dc.identifier.citedreferenceChen, R. Z., Pettersson, U., Beard, C., Jackson‐Grusby, L., & Jaenisch, R. ( 1998 ). DNA hypomethylation leads to elevated mutation rates. Nature, 395 ( 6697 ), 89 – 93. https://doi.org/10.1038/25779
dc.identifier.citedreferenceColuccio, A., Ecco, G., Duc, J., Offner, S., Turelli, P., & Trono, D. ( 2018 ). Individual retrotransposon integrants are differentially controlled by KZFP/KAP1‐dependent histone methylation, DNA methylation and TET‐mediated hydroxymethylation in naïve embryonic stem cells. Epigenetics and Chromatin, 11 ( 1 ), 1 – 18. https://doi.org/10.1186/s13072-018-0177-1
dc.identifier.citedreferenceCooper, S. M., Holekamp, K. E., & Smale, L. ( 1999 ). A seasonal feast: Long‐term analysis of feeding behaviour in the spotted hyaena ( Crocuta crocuta ). African Journal of Ecology, 37, 149 – 160. https://doi.org/10.1046/j.1365-2028.1999.00161.x
dc.identifier.citedreferenceCrudo, A., Petropoulos, S., Moisiadis, V. G., Iqbal, M., Kostaki, A., Machnes, Z., … Matthews, S. G. ( 2012 ). Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: Multigenerational effects. Endocrinology, 153 ( 7 ), 3269 – 3283. https://doi.org/10.1210/en.2011-2160
dc.identifier.citedreferenceDoherty, T. S., Forster, A., & Roth, T. L. ( 2016 ). Global and gene‐specific DNA methylation alterations in the adolescent amygdala and hippocampus in an animal model of caregiver maltreatment. Behavioural Brain Research, 298, 55 – 61. https://doi.org/10.1016/j.bbr.2015.05.028
dc.identifier.citedreferenceEden, A., Gaudet, F., Waghmare, A., & Jaenisch, R. ( 2003 ). Chromosomal instability and tumors promoted by DNA hypomethylation. Science, 300 ( 5618 ), 455. https://doi.org/10.1126/science.1083557
dc.identifier.citedreferenceEngh, A. L., Esch, K., Smale, L., & Holekamp, K. E. ( 2000 ). Mechanisms of maternal rank “inheritance” in the spotted hyaena, Crocuta crocuta. Animal Behaviour, 60, 323 – 332. https://doi.org/10.1006/anbe.2000.1502
dc.identifier.citedreferenceEngler, H., Bailey, M. T., Engler, A., & Sheridan, J. F. ( 2004 ). Effects of repeated social stress on leukocyte distribution in bone marrow, peripheral blood and spleen. Journal of Neuroimmunology, 148 ( 1–2 ), 106 – 115. https://doi.org/10.1016/j.jneuroim.2003.11.011
dc.identifier.citedreferenceFeinberg, A. P., & Vogelstein, B. ( 1983 ). Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature, 301 ( 5895 ), 89 – 92. https://doi.org/10.1038/301089a0
dc.identifier.citedreferenceFrank, L. G. ( 1986 ). Social organization of the spotted hyaena Crocuta crocuta. II. Dominance and reproduction. Animal Behaviour, 34 ( 5 ), 1510 – 1527. https://doi.org/10.1016/S0003-3472(86)80221-4
dc.identifier.citedreferenceFrank, L. G., Glickman, S. E., & Licht, P. ( 1991 ). Fatal sibling aggression, precocial development, and androgens in neonatal spotted hyenas. Science, 252 ( 5006 ), 702 – 704. https://doi.org/10.1126/science.2024122
dc.identifier.citedreferenceFrank, L. G., Glickman, S. E., & Powch, I. ( 1990 ). Sexual dimorphism in the spotted hyaena ( Crocuta crocuta ). Journal of Zoology, 221 ( 2 ), 308 – 313. https://doi.org/10.1111/j.1469-7998.1990.tb04001.x
dc.identifier.citedreferenceGillman, M. W. ( 2005 ). Developmental origins of health and disease. New England Journal of Medicine, 353 ( 17 ), 1848 – 1850. https://doi.org/10.1056/NEJMe058187
dc.identifier.citedreferenceGluckman, P. D., Cutfield, W., Hofman, P., & Hanson, M. A. ( 2005 ). The fetal, neonatal, and infant environments – The long‐term consequences for disease risk. Early Human Development, 81 ( 1 ), 51 – 59. https://doi.org/10.1016/j.earlhumdev.2004.10.003
dc.identifier.citedreferenceGreally, J. M. ( 2018 ). A user’s guide to the ambiguous word “epigenetics”. Nature Reviews Molecular Cell Biology, 19 ( 4 ), 207 – 208. https://doi.org/10.1038/nrm.2017.135
dc.identifier.citedreferenceGreen, D. S., Johnson‐Ulrich, L., Couraud, H. E., & Holekamp, K. E. ( 2018 ). Anthropogenic disturbance induces opposing population trends in spotted hyenas and African lions. Biodiversity and Conservation, 27 ( 4 ), 871 – 889. https://doi.org/10.1007/s10531-017-1469-7
dc.identifier.citedreferenceGreenberg, J. R. ( 2017 ). Developmental flexibility in spotted hyneas ( Crocuta crocuta ): The role of maternal and anthropogenic effects. PhD thesis, Michigan State University.
dc.identifier.citedreferenceHannon, E., Knox, O., Sugden, K., Burrage, J., Wong, C. C. Y., Belsky, D. W., … Mill, J. ( 2018 ). Characterizing genetic and environmental influences on variable DNA methylation using monozygotic and dizygotic twins. PLoS Genetics, 14 ( 8 ), 1 – 27. https://doi.org/10.1371/journal.pgen.1007544
dc.identifier.citedreferenceHanson, M. A., & Gluckman, P. D. ( 2014 ). Early developmental conditioning of later health and disease: Physiology or pathophysiology? Physiological Reviews, 94 ( 4 ), 1027 – 1076. https://doi.org/10.1152/physrev.00029.2013
dc.identifier.citedreferenceHead, J., Mittal, K., & Basu, N. ( 2014 ). Application of the LUminometric Methylation Assay to ecological species: Tissue quality requirements and a survey of DNA methylation levels in animals. Molecular Ecology Resources, 14 ( 5 ), 943 – 952. https://doi.org/10.1111/1755-0998.12244
dc.identifier.citedreferenceHeijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., … Lumey, L. H. ( 2008 ). Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proceedings of the National Academy of Sciences of the United States of America, 105 ( 44 ), 17046 – 17049. https://doi.org/10.1073/pnas.0806560105
dc.identifier.citedreferenceHeindel, J. J., & Vandenberg, L. N. ( 2015 ). Developmental origins of health and disease: A paradigm for understanding disease etiology and prevention. Current Opinion in Pediatrics, 27 ( 2 ), 248 – 253. https://doi.org/10.1097/MOP.0000000000000191.Developmental
dc.identifier.citedreferenceHelmby, H., Jönsson, G., & Troye‐Blomberg, M. ( 2000 ). Cellular changes and apoptosis in the spleens and peripheral blood of mice infected with blood‐stage Plasmodium chabaudi chabaudi AS. Infection and Immunity, 68 ( 3 ), 1485 – 1490. https://doi.org/10.1128/IAI.68.3.1485-1490.2000
dc.identifier.citedreferenceHolekamp, K. E., & Smale, L. ( 1991 ). Dominance acquisition during mammalian social development: The “inheritance” of maternal rank. Integrative and Comparative Biology, 31, 306 – 317. https://doi.org/10.1093/icb/31.2.306
dc.identifier.citedreferenceHolekamp, K. E., & Smale, L. ( 1993 ). Ontogeny of dominance in free‐living spotted hyaenas: Juvenile rank relations with other immature individuals. Animal Behaviour, 46 ( 3 ), 451 – 466. https://doi.org/10.1006/anbe.1993.1214
dc.identifier.citedreferenceHolekamp, K. E., & Smale, L. ( 1998 ). Behavioral development in the spotted hyena. BioScience, 48 ( 12 ), 997 – 1005. https://doi.org/10.2307/1313456
dc.identifier.citedreferenceHolekamp, K. E., Smale, L., Berg, R., & Cooper, S. M. ( 1997 ). Hunting rates and hunting success in the spotted hyena ( Crocuta crocuta ). Journal of Zoology, 242, 1 – 15. https://doi.org/10.1111/j.1469-7998.1997.tb02925.x
dc.identifier.citedreferenceHolekamp, K. E., Smale, L., & Szykman, M. ( 1996 ). Rank and reproduction in the female spotted hyaena. Journal of Reproduction and Fertility, 108 ( 2 ), 229 – 237. https://doi.org/10.1530/jrf.0.1080229
dc.identifier.citedreferenceHolekamp, K. E., Smith, J. E., Strelioff, C. C., Van Horn, R. C., & Watts, H. E. ( 2012 ). Society, demography and genetic structure in the spotted hyena. Molecular Ecology, 21 ( 3 ), 613 – 632. https://doi.org/10.1111/j.1365-294X.2011.05240.x
dc.identifier.citedreferenceHöner, O. P., Wachter, B., Hofer, H., Wilhelm, K., Thierer, D., Trillmich, F., … East, M. L. ( 2010 ). The fitness of dispersing spotted hyaena sons is influenced by maternal social status. Nature Communications, 1, 1 – 7. https://doi.org/10.1038/ncomms1059
dc.identifier.citedreferenceJones, P. A. ( 2012 ). Functions of DNA methylation: Islands, start sites, gene bodies and beyond. Nature Reviews Genetics, 13 ( 7 ), 484 – 492. https://doi.org/10.1038/nrg3230
dc.identifier.citedreferenceKarimi, M., Johansson, S., & Ekström, T. J. ( 2006 ). Using LUMA. A luminometric‐based assay for global DNA methylation. Epigenetics, 1 ( 1 ), 45 – 48. https://doi.org/10.1098/rstb.2013.0501
dc.identifier.citedreferenceKarimi, M., Johansson, S., Stach, D., Corcoran, M., Grandér, D., Schalling, M., … Ekström, T. J. ( 2006 ). LUMA (LUminometric Methylation Assay)–a high throughput method to the analysis of genomic DNA methylation. Experimental Cell Research, 312 ( 11 ), 1989 – 1995. https://doi.org/10.1016/j.yexcr.2006.03.006
dc.identifier.citedreferenceKing, K., Murphy, S., & Hoyo, C. ( 2015 ). Epigenetic regulation of newborns’ imprinted genes related to gestational growth: Patterning by parental race/ethnicity and maternal socioeconomic status. Journal of Epidemiology and Community Health, 69 ( 7 ), 639 – 647. https://doi.org/10.1136/jech-2014-204781
dc.identifier.citedreferenceKinney, S. M., Chin, H. G., Vaisvila, R., Bitinaite, J., Zheng, Y. U., Estève, P.‐O., … Pradhan, S. ( 2011 ). Tissue‐specific distribution and dynamic changes of 5‐hydroxymethylcytosine in mammalian genomes. Journal of Biological Chemistry, 286 ( 28 ), 24685 – 24693. https://doi.org/10.1074/jbc.M110.217083
dc.identifier.citedreferenceKlose, R. J., & Bird, A. P. ( 2006 ). Genomic DNA methylation: The mark and its mediators. Trends in Biochemical Sciences, 31 ( 2 ), 89 – 97. https://doi.org/10.1016/j.tibs.2005.12.008
dc.identifier.citedreferenceKolowski, J. M., & Holekamp, K. E. ( 2006 ). Spatial, temporal, and physical characteristics of livestock depredations by large carnivores along a Kenyan reserve border. Biological Conservation, 128, 529 – 541. https://doi.org/10.1016/j.biocon.2005.10.021
dc.identifier.citedreferenceKovacheva, V. P., Mellott, T. J., Davison, J. M., Wagner, N., Lopez‐Coviella, I., Schnitzler, A. C., & Blusztajn, J. K. ( 2007 ). Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up‐regulation of Dnmt1 expression. Journal of Biological Chemistry, 282 ( 43 ), 31777 – 31788. https://doi.org/10.1074/jbc.M705539200
dc.identifier.citedreferenceKruuk, H. ( 1972 ). The spotted hyena: A study of predation and social behavior. Chicago, IL: University of Chicago Press.
dc.identifier.citedreferenceKulkarni, A., Dangat, K., Kale, A., Sable, P., Chavan‐Gautam, P., & Joshi, S. ( 2011 ). Effects of altered maternal folic acid, vitamin B 12 and docosahexaenoic acid on placental global DNA methylation patterns in wistar rats. PLoS ONE, 6 ( 3 ), 1 – 7. https://doi.org/10.1080/03069888808253558
dc.identifier.citedreferenceLander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., & Baldwin, J., … International Human Genome Sequencing Consortium ( 2001 ). Initial sequencing and analysis of the human genome. Nature, 409 ( 6822 ), 860 – 921. https://doi.org/10.1038/35057062
dc.identifier.citedreferenceLappalainen, T., & Greally, J. M. ( 2017 ). Associating cellular epigenetic models with human phenotypes. Nature Reviews Genetics, 18 ( 7 ), 441 – 451. https://doi.org/10.1038/nrg.2017.32
dc.identifier.citedreferenceLaubach, Z. M., Faulk, C. D., Cardenas, A., & Perng, W. ( 2017 ). Nutrition, DNA methylation, and developmental origins of cardiometabolic disease: A signal systems approach. In V. R. Preedy & V. B. Patel (Eds.), Handbook of nutrition, diet, and epigenetics (pp. 1 – 18 ). Berlin, Germany: Springer International Publishing.
dc.identifier.citedreferenceLaubach, Z. M., Perng, W., Dolinoy, D. C., Faulk, C. D., Holekamp, K. E., & Getty, T. ( 2018 ). Epigenetics and the maintenance of developmental plasticity: Extending the signalling theory framework. Biological Reviews, 93 ( 3 ), 1323 – 1338. https://doi.org/10.1111/brv.12396
dc.identifier.citedreferenceLea, A. J., Tung, J., Archie, E. A., & Alberts, S. C. ( 2017 ). Developmental plasticity: Bridging research in evolution and human health. Evolution, Medicine, and Public Health, 2017 ( 1 ), 162 – 175. https://doi.org/10.1093/emph/eox019
dc.identifier.citedreferenceLev Maor, G., Yearim, A., & Ast, G. ( 2015 ). The alternative role of DNA methylation in splicing regulation. Trends in Genetics, 31 ( 5 ), 274 – 280. https://doi.org/10.1016/j.tig.2015.03.002
dc.identifier.citedreferenceLi, E., & Bird, A. ( 2007 ). DNA methylation in mammals. In C. D. Allis, T. Jenuwein, D. Reinberg, & M.‐L. Caparros (Eds.), Epigenetics (pp. 343 – 356 ). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
dc.identifier.citedreferenceLi, S., Zhang, J., Huang, S., & He, X. ( 2018 ). Genome‐wide analysis reveals that exon methylation facilitates its selective usage in the human transcriptome. Briefings in Bioinformatics, 19 ( 5 ), 754 – 764. https://doi.org/10.1093/bib/bbx019
dc.identifier.citedreferenceLi, Y., Pan, X., Roberts, M. L., Liu, P., Kotchen, T. A., Cowley, A. W., … Kidambi, S. ( 2018 ). Stability of global methylation profiles of whole blood and extracted DNA under different storage durations and conditions. Epigenomics, 10 ( 6 ), 797 – 811. https://doi.org/10.2217/epi-2018-0025
dc.identifier.citedreferenceLindblad‐Toh, K., Garber, M., Zuk, O. R., Lin, M. F., Parker, B. J., Washietl, S., … Kellis, M. ( 2011 ). A high‐resolution map of human evolutionary constraint using 29 mammals. Nature, 478 ( 7370 ), 476 – 482. https://doi.org/10.1038/nature10530
dc.identifier.citedreferenceLindblad‐Toh, K., Wade, C. M., Mikkelsen, T. S., Karlsson, E. K., Jaffe, D. B., Kamal, M., … Lander, E. S. ( 2005 ). Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature, 438 ( 7069 ), 803 – 819. https://doi.org/10.1038/nature04338
dc.identifier.citedreferenceLoi, M., Del Savio, L., & Stupka, E. ( 2013 ). Social epigenetics and equality of opportunity. Public Health Ethics, 6 ( 2 ), 142 – 153. https://doi.org/10.1093/phe/pht019
dc.identifier.citedreferenceMansournia, M. A., Etminan, M., Danaei, G., Kaufman, J. S., & Collins, G. ( 2017 ). Handling time varying confounding in observational research. BMJ, 359, j4587. https://doi.org/10.1136/bmj.j4587
dc.identifier.citedreferenceMassart, R., Suderman, M. J., Nemoda, Z., Sutti, S., Ruggiero, A. M., Dettmer, A. M., … Szyf, M. ( 2017 ). The signature of maternal social rank in placenta deoxyribonucleic acid methylation profiles in rhesus monkeys. Child Development, 88 ( 3 ), 900 – 918. https://doi.org/10.1111/cdev.12640
dc.identifier.citedreferenceMcGuinness, D., McGlynn, L. M., Johnson, P. C. D., MacIntyre, A., Batty, G. D., Burns, H., … Shiels, P. G. ( 2012 ). Socio‐economic status is associated with epigenetic differences in the pSoBid cohort. International Journal of Epidemiology, 41 ( 1 ), 151 – 160. https://doi.org/10.1093/ije/dyr215
dc.identifier.citedreferenceMeissner, A., Gnirke, A., Bell, G. W., Ramsahoye, B., Lander, E. S., & Jaenisch, R. ( 2005 ). Reduced representation bisulfite sequencing for comparative high‐resolution DNA methylation analysis. Nucleic Acids Research, 33 ( 18 ), 5868 – 5877. https://doi.org/10.1093/nar/gki901
dc.identifier.citedreferenceVajargah, K., & Masoomehnikbakht, K. ( 2015 ). Application REML model and determining cut off of ICC by multi‐level model based on Markov chains simulation in health. Indian Journal of Fundamental and Applied Life Sciences, 5, 2231 – 6345.
dc.identifier.citedreferenceMontrose, L., Noonan, C. W., Cho, Y. H., Lee, J., Harley, J., O’Hara, T., … Ward, T. J. ( 2015 ). Evaluating the effect of ambient particulate pollution on DNA methylation in Alaskan sled dogs: Potential applications for a sentinel model of human health. Science of the Total Environment, 512–513, 489 – 494. https://doi.org/10.1016/j.scitotenv.2014.12.046
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
mec15174_am.pdf
Size:
636.3KB
Format:
PDF
View/Open
Name:
mec15174.pdf
Size:
707.6KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.