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The University of Chicago Differential and Long-Term THE UNIVERSITY OF CHICAGO DIFFERENTIAL AND LONG-TERM IMPACTS OF BIPARENTAL EFFECTS ON OFFSPRING PERSONALITY AND HORMONES IN COYOTES (CANIS LATRANS) A DISSERTATION SUBMITTED TO THE FACULTY OF THE DIVISION OF THE BIOLOGICAL SCIENCES AND THE PRITZKER SCHOOL OF MEDICINE IN CANDIDACY FOR THE DEGREE OF DOCTOR OF PHILOSOPHY COMMITTEE ON EVOLUTIONARY BIOLOGY BY CHRISTOPHER JOHN SCHELL CHICAGO, ILLINOIS DECEMBER 2015 I dedicate this to my parents and grandparents, my beautiful wife Danielle LaVeta Schell, and my future children. May they too be infected with the same curiosity, courage, and sense of adventure that my parents nurtured inside me. TABLE OF CONTENTS LIST OF TABLES ......................................................................................................................... iv LIST OF FIGURES ........................................................................................................................ v ACKNOWLEGMENTS ............................................................................................................... vii ABSTRACT .................................................................................................................................. xii CHAPTER 1: INTRODUCTION ................................................................................................... 1 CHAPTER 2: CONSPECIFIC ODOR CUES AND PARITY AFFECT PRENATAL ANDROGENS AND TERRITORIALITY OF COYOTE BREEDING PAIRS ......................... 24 CHAPTER 3: PRE-PARTUM ANDROGENS AND PARITY ARE PRINCIPAL DETERMINANTS OF COYOTE PARENTAL STYLES........................................................... 58 CHAPTER 4: COYOTE PARENTING EXPERIENCE AND PRENATAL ANDROGENS IMPACT BOLDNESS AND HORMONES IN PUPS ................................................................. 88 CHAPTER 5: DEVELOPMENTAL EXPERIENCES PREDICT YEARLING PERSONALITY TRAITS AND ANDROGENS IN COYOTES........................................................................... 120 CHAPTER 6: CONCLUSION ................................................................................................... 155 APPENDIX A: FECAL HORMONE VALIDATIONS ............................................................. 174 APPENDIX B: SPEARMAN RANK CORRELATIONS AMONG TERRITORIAL BEHAVIORS AND HORMONES OF EXPECTANT PARENTS ........................................... 184 APPENDIX C: DIFFERENCES IN HAIR HORMONES BY BODY REGION ...................... 186 APPENDIX D: YEARLING COMPONENTS AND HORMONAL RESPONSES TO HUMAN- ASSOCIATED OBJECTS .......................................................................................................... 187 REFERENCES ........................................................................................................................... 193 iii LIST OF TABLES Table 2.1: Behavioral ethogram used during foreign scent tests .................................................. 32 Table 2.2: Consistent individual differences in marking and investigative behaviors ................. 42 Table 2.3: Consistent individual differences in overall gestational hormones ............................. 48 Table 3.1: Behavioral ethogram used during the gestation and weaning periods ........................ 63 Table 3.2: Differences in parenting behaviors between mothers and fathers corresponding to litter age ........................................................................................................................................ 72 Table 3.3: Results of principal components analysis for parental care behaviors ........................ 73 Table 3.4: Consistent individual differences in parental care principal components ................... 74 Table 3.5: Consistent individual differences in general marking, social and vigilance behaviors 75 Table 3.6: Spearman rank relationships among mean (± S.E.) parenting components and general behaviors of parents ...................................................................................................................... 76 Table 4.1: The five different novel objects provided ................................................................... 93 Table 5.1: Behavioral ethogram used during the feeding and novel object tests ....................... 126 Table 5.2: The four objects presented to yearlings previously provided to them as pups ......... 127 Table 5.3: Results of principal components analysis (PCA) for feeding test measures ............. 138 Table 5.4: Results of principal components analysis (PCA) for object test measures ............... 139 Table 6.1: Summary of findings for chapters 2 through 5 .......................................................... 160 Table B1: Spearman rank correlations among scent-marking and investigative behaviors ....... 184 Table B2: Correlations among fecal glucocorticoids, fecal androgens, and behaviors .............. 185 Table D1: Change in fecal glucocorticoid and androgen metabolites post-object presentation . 190 Table D2: Fecal glucocorticoid metabolites (FGMs). pre-test and post-object presentation for each repeated object type ............................................................................................................ 191 Table D3: Fecal androgen metabolites (FAMs). pre-test and post-object presentation for each repeated object type .................................................................................................................... 192 iv LIST OF FIGURES Figure 2.1: Mean (± S.E.) instances of marking and investigative behaviors .............................. 40 Figure 2.2: Mean (± S.E.) time spent <1 meter within the odor- (treatment) or water-treated (control) test site ........................................................................................................................... 41 Figure 2.3: Fecal glucocorticoid and androgen metabolite concentrations across gestation before parturition ...................................................................................................................................... 46 Figure 2.4: Fecal glucocorticoid and androgen metabolite concentrations over the odor cue provisioning period ....................................................................................................................... 47 Figure 2.5: Correlations among best linear unbiased predictors (BLUPs) for fecal androgen metabolites and investigatory behaviors ....................................................................................... 49 Figure 3.1: Mean (± S.E.) parental care principal component scores of first-time and experienced mothers over pup development ..................................................................................................... 77 Figure 3.2: Mean (± S.E.) parental care principal component scores of first-time and experienced fathers over pup development ....................................................................................................... 78 Figure 3.3: Correlations among litter size, mean (± S.E.) contact, mean aggression/provisioning components, and androgen metabolites ........................................................................................ 79 Figure 3.4: Correlations among mean (± S.E.) urinations, ground scratches, howls, and fecal glucocorticoid metabolites ............................................................................................................ 80 Figure 4.1: Mean proportion that litters re-emerged from their dens and approached during novel objects tests ................................................................................................................................ 103 Figure 4.2: Mean proportion that litters re-emerged from their dens and ate independently from their parents during feeding tests ................................................................................................ 105 Figure 4.3: Hair cortisol and testosterone concentrations of litters over developmental time ... 107 Figure 4.4: Correlations among mean proportion each pup ate during feeding tests, their hair cortisol concentrations, and hair testosterone concentrations at 15 weeks of age ...................... 109 Figure 4.5: Correlations among mean proportion each litter ate during feeding tests, mean maternal androgen metabolites, and paternal androgen metabolites .......................................... 110 Figure 5.1: Correlations among the pup and yearling feeding test measures ............................. 140 Figure 5.2: Boldness principal components for yearling feeding and repeated object tests ....... 141 v Figure 5.3: Correlations among pup variables and repeated object principal component scores ..... ..................................................................................................................................................... 144 Figure 5.4: Mean (± S.E.) overall fecal glucocorticoid and androgen metabolites of male and female yearlings .......................................................................................................................... 145 Figure 5.5: Correlations among boldness and territoriality components across yearling feeding and object tests ............................................................................................................................ 146 Figure 6.1: Summary of findings from Chapters 2 through 5 ..................................................... 161 Figure C1: Mean (± S.E.) hair cortisol testosterone concentrations of 5-week old pups from six different shaved body regions ....................................................................................................
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