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      Parental habituation to human disturbance over time reduces fear of humans in coyote offspring

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          Abstract

          A fundamental tenet of maternal effects assumes that maternal variance over time should have discordant consequences for offspring traits across litters. Yet, seldom are parents observed across multiple reproductive bouts, with few studies considering anthropogenic disturbances as an ecological driver of maternal effects. We observed captive coyote ( Canis latrans) pairs over two successive litters to determine whether among‐litter differences in behavior (i.e., risk‐taking) and hormones (i.e., cortisol and testosterone) corresponded with parental plasticity in habituation. Thus, we explicitly test the hypothesis that accumulating experiences of anthropogenic disturbance reduces parental fear across reproductive bouts, which should have disparate phenotypic consequences for first‐ and second‐litter offspring. To quantify risk‐taking behavior, we used foraging assays from 5–15 weeks of age with a human observer present as a proxy for human disturbance. At 5, 10, and 15 weeks of age, we collected shaved hair to quantify pup hormone levels. We then used a quantitative genetic approach to estimate heritability, repeatability, and between‐trait correlations. We found that parents were riskier (i.e., foraged more frequently) with their second versus first litters, supporting our prediction that parents become increasingly habituated over time. Second‐litter pups were also less risk‐averse than their first‐litter siblings. Heritability for all traits did not differ from zero (0.001–0.018); however, we found moderate support for repeatability in all observed traits ( r = 0.085–0.421). Lastly, we found evidence of positive phenotypic and cohort correlations among pup traits, implying that cohort identity (i.e., common environment) contributes to the development of phenotypic syndromes in coyote pups. Our results suggest that parental habituation may be an ecological cue for offspring to reduce their fear response, thus emphasizing the role of parental plasticity in shaping their pups’ behavioral and hormonal responses toward humans.

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          Epigenetic programming by maternal behavior.

          Here we report that increased pup licking and grooming (LG) and arched-back nursing (ABN) by rat mothers altered the offspring epigenome at a glucocorticoid receptor (GR) gene promoter in the hippocampus. Offspring of mothers that showed high levels of LG and ABN were found to have differences in DNA methylation, as compared to offspring of 'low-LG-ABN' mothers. These differences emerged over the first week of life, were reversed with cross-fostering, persisted into adulthood and were associated with altered histone acetylation and transcription factor (NGFI-A) binding to the GR promoter. Central infusion of a histone deacetylase inhibitor removed the group differences in histone acetylation, DNA methylation, NGFI-A binding, GR expression and hypothalamic-pituitary-adrenal (HPA) responses to stress, suggesting a causal relation among epigenomic state, GR expression and the maternal effect on stress responses in the offspring. Thus we show that an epigenomic state of a gene can be established through behavioral programming, and it is potentially reversible.
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            The adaptive significance of maternal effects

            T Mousseau (1998)
            Recently, the adaptive significance of maternal effects has been increasingly recognized. No longer are maternal effects relegated as simple `troublesome sources of environmental resemblance' that confound our ability to estimate accurately the genetic basis of traits of interest. Rather, it has become evident that many maternal effects have been shaped by the action of natural selection to act as a mechanism for adaptive phenotypic response to environmental heterogeneity. Consequently, maternal experience is translated into variation in offspring fitness.
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              An ecologist's guide to the animal model.

              1. Efforts to understand the links between evolutionary and ecological dynamics hinge on our ability to measure and understand how genes influence phenotypes, fitness and population dynamics. Quantitative genetics provides a range of theoretical and empirical tools with which to achieve this when the relatedness between individuals within a population is known. 2. A number of recent studies have used a type of mixed-effects model, known as the animal model, to estimate the genetic component of phenotypic variation using data collected in the field. Here, we provide a practical guide for ecologists interested in exploring the potential to apply this quantitative genetic method in their research. 3. We begin by outlining, in simple terms, key concepts in quantitative genetics and how an animal model estimates relevant quantitative genetic parameters, such as heritabilities or genetic correlations. 4. We then provide three detailed example tutorials, for implementation in a variety of software packages, for some basic applications of the animal model. We discuss several important statistical issues relating to best practice when fitting different kinds of mixed models. 5. We conclude by briefly summarizing more complex applications of the animal model, and by highlighting key pitfalls and dangers for the researcher wanting to begin using quantitative genetic tools to address ecological and evolutionary questions.
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                Author and article information

                Contributors
                cjschell@uw.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                11 December 2018
                December 2018
                : 8
                : 24 ( doiID: 10.1002/ece3.2018.8.issue-24 )
                : 12965-12980
                Affiliations
                [ 1 ] Committee on Evolutionary Biology University of Chicago Chicago Illinois
                [ 2 ] School of Interdisciplinary Arts and Sciences University of Washington Tacoma Tacoma Washington
                [ 3 ] USDA‐WS‐NWRC Predator Research Facility, Department of Wildland Resources Utah State University Logan Utah
                [ 4 ] Department of Psychology Franklin and Marshall College Lancaster Pennsylvania
                [ 5 ] Conservation and Science Department Lincoln Park Zoo Chicago Illinois
                Author notes
                [*] [* ] Correspondence

                Christopher J. Schell, Committee on Evolutionary Biology, University of Chicago, Chicago, IL.

                Email: cjschell@ 123456uw.edu

                Author information
                http://orcid.org/0000-0002-2073-9852
                http://orcid.org/0000-0003-4522-0157
                http://orcid.org/0000-0001-8057-401X
                http://orcid.org/0000-0003-4102-9144
                Article
                ECE34741
                10.1002/ece3.4741
                6308887
                30619597
                58cf9859-80f2-4e64-b12c-05f37ce547e3
                © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 22 August 2018
                : 10 October 2018
                : 24 October 2018
                Page count
                Figures: 5, Tables: 4, Pages: 16, Words: 40690
                Funding
                Funded by: Pritzker School of Medicine
                Award ID: Hinds Fellowship (2011, 2013)
                Funded by: Animal and Plant Health Inspection Service
                Award ID: NWRC Predator Research Facility Fellowship
                Funded by: United Negro College Fund Special Programs Corporation
                Award ID: MERCK Fellowship
                Funded by: Directorate for Biological Sciences
                Award ID: NSF Graduate Research Fellowship Program (GRFP)
                Funded by: Merck
                Funded by: U.S. Department of Agriculture
                Award ID: 72184
                Funded by: University of Chicago
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece34741
                December 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.5.4 mode:remove_FC converted:28.12.2018

                Evolutionary Biology
                canis latrans,hormones,human disturbance,parental effects,repeatability,risk‐taking

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