Paternal influences on offspring development: Behavioural and epigenetic pathways

Journal of Neuroendocrinology

Volumn 26, Issue 10, 2014, Pages 697-706

  Braun, K ^a   Champagne, F A ^b  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b Department of Psychology Columbia University ^*  (United States)

Author keywords

Biparental; Epigenetic; Maternal; Neurodevelopment; Paternal care

Indexed keywords

BRAIN DEVELOPMENT; CHILD DEVELOPMENT; EPIGENETICS; FATHER CHILD RELATION; HUMAN; LOCOMOTION; LONG TERMINAL REPEAT; MATERNAL DEPRIVATION; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PAIR BONDING; PARENTAL BEHAVIOR; PARENTAL DEPRIVATION; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROGENY; REVIEW; SOCIAL ENVIRONMENT; SURVIVAL; ANIMAL; ANIMAL BEHAVIOR; FATHER; FEMALE; GENETIC EPIGENESIS; MALE; MOTHER; NUTRITIONAL STATUS; SOCIAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; EPIGENESIS, GENETIC; FATHERS; FEMALE; MALE; MOTHERS; NUTRITIONAL STATUS; PHENOTYPE; SOCIAL BEHAVIOR;

EID: 84927522353     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12174     Document Type: Review

References (114)

1. Maccari S, Krugers HJ, Morley-Fletcher S, Szyf M, Brunton PJ. The consequences of early life adversity: neurobiological, behavioural and epigenetic adaptations. J Neuroendocrinol 2014; 26: 707-723.
2. Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 2008; 32: 1073-1086.
3. Susser E, Hoek HW, Brown A. Neurodevelopmental disorders after prenatal famine: the story of the Dutch Famine Study. Am J Epidemiol 1998; 147: 213-216.
4. Olegard R, Sabel KG, Aronsson M, Sandin B, Johansson PR, Carlsson C, Kyllerman M, Iversen K, Hrbek A. Effects on the child of alcohol abuse during pregnancy. Retrospective and prospective studies. Acta Paediatr Scand Suppl 1979; 275: 112-121.
5. Williams JH, Ross L. Consequences of prenatal toxin exposure for mental health in children and adolescents: a systematic review. Eur Child Adolesc Psychiatry 2007; 16: 243-253.
6. Sanchez MM, Ladd CO, Plotsky PM. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol 2001; 13: 419-449.
7. Gonzalez A, Lovic V, Ward GR, Wainwright PE, Fleming AS. Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Dev Psychobiol 2001; 38: 11-32.
8. Hane AA, Fox NA. Ordinary variations in maternal caregiving influence human infants' stress reactivity. Psychol Sci 2006; 17: 550-556.
9. Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001; 24: 1161-1192.
10. Marsiglio W, Amato P, Day RD, Lamb ME. Scholarship on fatherhood in the 1990s and beyond. J Marriage Fam 2000; 62: 18.
11. Bamshad M, Novak MA, de Vries GJ. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster). Physiol Behav 1994; 56: 751-758.
12. Becker K, Abraham A, Kindler J, Helmeke C, Braun K. Exposure to neonatal separation stress alters exploratory behavior and corticotropin releasing factor expression in neurons in the amygdala and hippocampus. Dev Neurobiol 2007; 67: 617-629.
13. Bock J, Gruss M, Becker S, Braun K. Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows. Cereb Cortex 2005; 15: 802-808.
14. Gos T, Bock J, Poeggel G, Braun K. Stress-induced synaptic changes in the rat anterior cingulate cortex are dependent on endocrine developmental time windows. Synapse 2008; 62: 229-232.
15. Saltzman W, Ziegler TE. Functional significance of hormonal changes in mammalian fathers. J Neuroendocrinol 2014; 26: 685-696.
16. Woodroffe R, Vincent A. Mother's little helpers: patterns of male care in mammals. Trends Ecol Evol 1994; 9: 294-297.
17. Svare B, Kinsley CH, Mann MA, Broida J. Infanticide: accounting for genetic variation in mice. Physiol Behav 1984; 33: 137-152.
18. Cantoni D, Brown RE. Paternal investment and reproductive success in the California mouse, Peromyscus californicus. Anim Behav 1997; 54: 377-386.
19. Ebensperger LA, Ramirez-Otarola N, Leon C, Ortiz ME, Croxatto HB. Early fitness consequences and hormonal correlates of parental behaviour in the social rodent, Octodon degus. Physiol Behav 2010; 101: 509-517.
20. Vieira ML, Brown RE. Effects of the presence of the father on pup development in California mice (Peromyscus californicus). Dev Psychobiol 2003; 42: 246-251.
21. Alter MD, Gilani AI, Champagne FA, Curley JP, Turner JB, Hen R. Paternal transmission of complex phenotypes in inbred mice. Biol Psychiatry 2009; 66: 1061-1066.
22. Saavedra-Rodriguez L, Feig LA. Chronic social instability induces anxiety and defective social interactions across generations. Biol Psychiatry 2013; 73: 44-53.
23. Anway MD, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 2006; 147(6 Suppl): S43-S49.
24. Ledig M, Misslin R, Vogel E, Holownia A, Copin JC, Tholey G. Paternal alcohol exposure: developmental and behavioral effects on the offspring of rats. Neuropharmacology 1998; 37: 57-66.
25. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 2010; 467: 963-966.
26. Curley JP, Mashoodh R, Champagne FA. Epigenetics and the origins of paternal effects. Horm Behav 2011; 59: 306-314.
27. Burley N. The differential-allocation hypothesis - an experimental test. Am Nat 1988; 132: 611-628.
28. Gowaty PA, Anderson WW, Bluhm CK, Drickamer LC, Kim YK, Moore AJ. The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proc Natl Acad Sci USA 2007; 104: 15023-15027.
29. Crews D, Gore AC, Hsu TS, Dangleben NL, Spinetta M, Schallert T, Anway MD, Skinner MK. Transgenerational epigenetic imprints on mate preference. Proc Natl Acad Sci USA 2007; 104: 5942-5946.
30. Yamazaki K, Beauchamp GK. Genetic basis for MHC-dependent mate choice. Adv Genet 2007; 59: 129-145.
31. Amato PR. Father-child relations, mother-child relations, and offspring psychological well-being in early adulthood. J Marriage Fam 1994; 56: 1031-1042.
32. Grossmann K, Grossmann KE, Fremmer-Bombik E, Kindler H, Scheuerer-Englisch H, Zimmermann P. The uniqueness of the child-father attachment relationship: fathers' sensitive and challenging play as a pivotal variable in a 16-year longitudinal study. Soc Dev 2002; 11: 301-337.
33. Ember C, Ember M. War, socialization, and interpersonal violence. J Conflict Resolut 1994; 38: 26.
34. Flinn MV, England BG. Social economics of childhood glucocorticoid stress response and health. Am J Phys Anthropol 1997; 102: 33-53.
35. Phares V, Compas BE. The role of fathers in child and adolescent psychopathology: make room for daddy. Psychol Bull 1992; 111: 387-412.
36. Kentner AC, Abizaid A, Bielajew C. Modeling dad: animal models of paternal behavior. Neurosci Biobehav Rev 2010; 34: 438-451.
37. Kleiman DG, Malcolm JR. The evolution of male parental investment in mammals, In Parental Care in Mammals, Gubernick DJ, Klopfer PH eds. New York, NY: Plenum Press, 1981.
38. Wilson KR, Prior MR. Father involvement and child well-being. J Paediatr Child Health 2011; 47: 405-407.
39. Bredy TW, Brown RE, Meaney MJ. Effect of resource availability on biparental care, and offspring neural and behavioral development in the California mouse (Peromyscus californicus). Eur J Neurosci 2007; 25: 567-575.
40. Lambert KG, Franssen CL, Hampton JE, Rzucidlo AM, Hyer MM, True M, Kaufman C, Bardi M. Modeling paternal attentiveness: distressed pups evoke differential neurobiological and behavioral responses in paternal and nonpaternal mice. Neuroscience 2013; 234: 1-12.
41. Feldman R. Oxytocin and social affiliation in humans. Horm Behav 2012; 61: 380-391.
42. Rosenfeld CS, Johnson SA, Ellersieck MR, Roberts RM. Interactions between parents and parents and pups in the monogamous California mouse (Peromyscus californicus). PLoS One 2013; 8: e75725.
43. Ziegler TE. Hormones associated with non-maternal infant care: a review of mammalian and avian studies. Folia Primatol (Basel) 2000; 71: 6-21.
44. Libhaber N, Eilam D. Social vole parents force their mates to baby-sit. Dev Psychobiol 2002; 41: 236-240.
45. Liu HX, Lopatina O, Higashida C, Fujimoto H, Akther S, Inzhutova A, Liang M, Zhong J, Tsuji T, Yoshihara T, Sumi K, Ishiyama M, Ma WJ, Ozaki M, Yagitani S, Yokoyama S, Mukaida N, Sakurai T, Hori O, Yoshioka K, Hirao A, Kato Y, Ishihara K, Kato I, Okamoto H, Cherepanov SM, Salmina AB, Hirai H, Asano M, Brown DA, Nagano I, Higashida H. Displays of paternal mouse pup retrieval following communicative interaction with maternal mates. Nat Commun 2013; 4: 1346.
46. Piovanotti MR, Vieira ML. Presence of the father and parental experience have differentiated effects on pup development in Mongolian gerbils (Meriones unguiculatus). Behav Processes 2004; 66: 107-117.
47. Helmeke C, Seidel K, Poeggel G, Bredy TW, Abraham A, Braun K. Paternal deprivation during infancy results in dendrite- and time-specific changes of dendritic development and spine formation in the orbitofrontal cortex of the biparental rodent Octodon degus. Neuroscience 2009; 163: 790-798.
48. Pinkernelle J, Abraham A, Seidel K, Braun K. Paternal deprivation induces dendritic and synaptic changes and hemispheric asymmetry of pyramidal neurons in the somatosensory cortex. Dev Neurobiol 2009; 69: 663-673.
49. McGraw LA, Young LJ. The prairie vole: an emerging model organism for understanding the social brain. Trends Neurosci 2010; 33: 103-109.
50. Ahern TH, Hammock EA, Young LJ. Parental division of labor, coordination, and the effects of family structure on parenting in monogamous prairie voles (Microtus ochrogaster). Dev Psychobiol 2011; 53: 118-131.
51. Wang Z, Young LJ, De Vries GJ, Insel TR. Voles and vasopressin: a review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog Brain Res 1998; 119: 483-499.
52. Gubernick DJ, Teferi T. Adaptive significance of male parental care in a monogamous mammal. Proc Biol Sci 2000; 267: 147-150.
53. Bester-Meredith JK, Marler CA. Vasopressin and the transmission of paternal behavior across generations in mated, cross-fostered Peromyscus mice. Behav Neurosci 2003; 117: 455-463.
54. Frazier CR, Trainor BC, Cravens CJ, Whitney TK, Marler CA. Paternal behavior influences development of aggression and vasopressin expression in male California mouse offspring. Horm Behav 2006; 50: 699-707.
55. Cao Y, Wu R, Tai F, Zhang X, Yu P, An X, Qiao X, Hao P. Neonatal paternal deprivation impairs social recognition and alters levels of oxytocin and estrogen receptor alpha mRNA expression in the MeA and NAcc, and serum oxytocin in mandarin voles. Horm Behav 2014; 65: 57-65.
56. Bambico FR, Lacoste B, Hattan PR, Gobbi G. Father absence in the monogamous california mouse impairs social behavior and modifies dopamine and glutamate synapses in the medial prefrontal cortex. Cereb Cortex in press.
57. Birnie AK, Taylor JH, Cavanaugh J, French JA. Quality of maternal and paternal care predicts later stress reactivity in the cooperatively-breeding marmoset (Callithrix geoffroyi). Psychoneuroendocrinology 2013; 38: 3003-3014.
58. Ahern TH, Young LJ. The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster). Front Behav Neurosci 2009; 3: 17.
59. Gromov VS. [Interactions of partners in family pairs, care of the offspring, and the role of tactile stimulation in formation of parental behavior of the Mongolian gerbil (Meriones unguiculatus) under laboratory conditions]. Izv Akad Nauk Ser Biol 2009; 5: 569-579.
60. Gleason ED, Marler CA. Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse. Proc Biol Sci 2013; 280: 20130824.
61. Ovtscharoff W Jr, Helmeke C, Braun K. Lack of paternal care affects synaptic development in the anterior cingulate cortex. Brain Res 2006; 1116: 58-63.
62. Vitureira N, Letellier M, Goda Y. Homeostatic synaptic plasticity: from single synapses to neural circuits. Curr Opin Neurobiol 2012; 22: 516-521.
63. Braun K, Seidel K, Weigel S, Roski C, Poeggel G. Paternal deprivation alters region- and age-specific interneuron expression patterns in the biparental rodent, Octodon degus. Cereb Cortex 2011; 21: 1532-1546.
64. Seidel K, Poeggel G, Holetschka R, Helmeke C, Braun K. Paternal deprivation affects the development of corticotrophin-releasing factor-expressing neurones in prefrontal cortex, amygdala and hippocampus of the biparental Octodon degus. J Neuroendocrinol 2011; 23: 1166-1176.
65. Braun K, Seidel K, Holetschka R, Groeger N, Poeggel G. Paternal deprivation alters the development of catecholaminergic innervation in the prefrontal cortex and related limbic brain regions. Brain Struct Funct 2013; 218: 859-872.
66. Ikemoto S, Panksepp J. The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev 1999; 31: 6-41.
67. Robbins TW, Everitt BJ. Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol 1996; 6: 228-236.
68. Yu P, An S, Tai F, Zhang X, He F, Wang J, An X, Wu R. The effects of neonatal paternal deprivation on pair bonding, NAcc dopamine receptor mRNA expression and serum corticosterone in mandarin voles. Horm Behav 2012; 61: 669-677.
69. Weinshenker D, Schroeder JP. There and back again: a tale of norepinephrine and drug addiction. Neuropsychopharmacology 2007; 32: 1433-1451.
70. Gos T, Schulkin J, Gos A, Bock J, Poeggel G, Braun K. Paternal deprivation affects the functional maturation of corticotropin-releasing hormone (CRH)- and calbindin-D28k-expressing neurons in the bed nucleus of the stria terminalis (BNST) of the biparental Octodon degus. Brain Struct Funct in press.
71. Jia R, Tai F, An S, Zhang X. Neonatal paternal deprivation or early deprivation reduces adult parental behavior and central estrogen receptor alpha expression in mandarin voles (Microtus mandarinus). Behav Brain Res 2011; 224: 279-289.
72. Santos F, Hendrich B, Reik W, Dean W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 2002; 241: 172-182.
73. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J, Reik W. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 2003; 35: 88-93.
74. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 1999; 23: 314-318.
75. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KV, Whitelaw E. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci USA 2003; 100: 2538-2543.
76. Ashe A, Sapetschnig A, Weick EM, Mitchell J, Bagijn MP, Cording AC, Doebley AL, Goldstein LD, Lehrbach NJ, Le Pen J, Pintacuda G, Sakaguchi A, Sarkies P, Ahmed S, Miska EA. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 2012; 150: 88-99.
77. Morgan CP, Bale TL. Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J Neurosci 2011; 31: 11748-11755.
78. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 2008; 105: 17046-17049.
79. Kaati G, Bygren LO, Pembrey M, Sjostrom M. Transgenerational response to nutrition, early life circumstances and longevity. Eur J Hum Genet 2007; 15: 784-790.
80. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjostrom M, Golding J, Team AS. Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 2006; 14: 159-166.
81. Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, Lillycrop KA. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr 2007; 97: 435-439.
82. Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, Burdge GC. Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr 2008; 100: 278-282.
83. Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, Burdge GC. Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 2007; 97: 1064-1073.
84. Dunn GA, Bale TL. Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 2009; 150: 4999-5009.
85. Dunn GA, Bale TL. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 2011; 152: 2228-2236.
86. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R, Bock C, Li C, Gu H, Zamore PD, Meissner A, Weng Z, Hofmann HA, Friedman N, Rando OJ. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 2010; 143: 1084-1096.
87. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005; 308: 1466-1469.
88. Skinner MK, Anway MD, Savenkova MI, Gore AC, Crews D. Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior. PLoS One 2008; 3: e3745.
89. Guerrero-Bosagna C, Settles M, Lucker B, Skinner MK. Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One 2010; 5: E13100.
90. Bielawski DM, Zaher FM, Svinarich DM, Abel EL. Paternal alcohol exposure affects sperm cytosine methyltransferase messenger RNA levels. Alcohol Clin Exp Res 2002; 26: 347-351.
91. Govorko D, Bekdash RA, Zhang C, Sarkar DK. Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations. Biol Psychiatry 2012; 72: 378-388.
92. Abel EL, Moore C, Waselewsky D, Zajac C, Russell LD. Effects of cocaine hydrochloride on reproductive function and sexual behavior of male rats and on the behavior of their offspring. J Androl 1989; 10: 17-27.
93. He F, Lidow IA, Lidow MS. Consequences of paternal cocaine exposure in mice. Neurotoxicol Teratol 2006; 28: 198-209.
94. Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC. Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 2013; 16: 42-47.
95. Brevik A, Lindeman B, Brunborg G, Duale N. Paternal benzo[a]pyrene exposure modulates microRNA expression patterns in the developing mouse embryo. Int J Cell Biol 2012; 2012: 407431.
96. Filkowski JN, Ilnytskyy Y, Tamminga J, Koturbash I, Golubov A, Bagnyukova T, Pogribny IP, Kovalchuk O. Hypomethylation and genome instability in the germline of exposed parents and their progeny is associated with altered miRNA expression. Carcinogenesis 2010; 31: 1110-1115.
97. Marczylo EL, Amoako AA, Konje JC, Gant TW, Marczylo TH. Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics 2012; 7: 432-439.
98. Champagne FA. Epigenetic influence of social experiences across the lifespan. Dev Psychobiol 2010; 52: 299-311.
99. Haller J, Harold G, Sandi C, Neumann ID. Effects of adverse early-life events on aggression and anti-social behaviours in animals and humans. J Neuroendocrinol 2014; 26: 724-738.
100. Franklin TB, Linder N, Russig H, Thony B, Mansuy IM. Influence of early stress on social abilities and serotonergic functions across generations in mice. PLoS One 2011; 6: e21842.
101. Franklin TB, Russig H, Weiss IC, Graff J, Linder N, Michalon A, Vizi S, Mansuy IM. Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry 2010; 68: 408-415.
102. Dietz DM, Laplant Q, Watts EL, Hodes GE, Russo SJ, Feng J, Oosting RS, Vialou V, Nestler EJ. Paternal transmission of stress-induced pathologies. Biol Psychiatry 2011; 70: 408-414.
103. Harold GT, Rice F, Hay DF, Boivin J, van den Bree M, Thapar A. Familial transmission of depression and antisocial behavior symptoms: disentangling the contribution of inherited and environmental factors and testing the mediating role of parenting. Psychol Med 2011; 41: 1175-1185.
104. Rice F, Harold GT, Boivin J, Hay DF, van den Bree M, Thapar A. Disentangling prenatal and inherited influences in humans with an experimental design. Proc Natl Acad Sci USA 2009; 106: 2464-2467.
105. Katari S, Turan N, Bibikova M, Erinle O, Chalian R, Foster M, Gaughan JP, Coutifaris C, Sapienza C. DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum Mol Genet 2009; 18: 3769-3778.
106. Weinraub M, Wolf BM. Effects of stress and social supports on mother-child interactions in single- and two-parent families. Child Dev 1983; 54: 1297-1311.
107. Osborne C, Berger LM, Magnuson K. Family structure transitions and changes in maternal resources and well-being. Demography 2012; 49: 23-47.
108. Horvathova T, Nakagawa S, Uller T. Strategic female reproductive investment in response to male attractiveness in birds. Proc Biol Sci 2012; 279: 163-170.
109. Bluhm CK, Gowaty PA. Reproductive compensation for offspring viability deficits by female mallards, Anas platyrhynchos. Anim Behav 2004; 68: 985-992.
110. Cunningham EJ, Russell AF. Egg investment is influenced by male attractiveness in the mallard. Nature 2000; 404: 74-77.
111. Mashoodh R, Franks B, Curley JP, Champagne FA. Paternal social enrichment effects on maternal behavior and offspring growth. Proc Natl Acad Sci USA 2012; 109(Suppl 2): 17232-17238.
112. Gilbert L, Williamson KA, Graves JA. Male attractiveness regulates daughter fecundity non-genetically via maternal investment. Proc Biol Sci 2012; 279: 523-528.
113. Gilbert L, Williamson KA, Hazon N, Graves JA. Maternal effects due to male attractiveness affect offspring development in the zebra finch. Proc Biol Sci 2006; 273: 1765-1771.
114. Meikle DB. Adult male house mice born to undernourished mothers are unattractive to oestrous females. Anim Behav 1995; 50: 753-758.