The biology of paternal care in human and nonhuman primates

Fernandez-Duque, Eduardo; Valeggia, Claudia R.; Mendoza, Sally P.

doi:10.1146/annurev-anthro-091908-164334

Cited by 232Primate Behavior and EcologyNeuroendocrine regulation and behaviorAnimal Behavior and Reproduction

The biology of paternal care in human and nonhuman primates

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Fernandez-Duque, Eduardo, Valeggia, Claudia R., Mendoza, Sally P.·2009·Annual Review of Anthropology

DOI 10.1146/annurev-anthro-091908-164334

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Abstract

Among primates, intense paternal care is manifested in only a few distantly related species, including humans. Thus, neither purely phylogenetic nor socioecological hypotheses can explain its presence or the variability in the expression of paternal behaviors. Traditional theoretical models for the evolution of paternal care can now be reexamined, focusing on male-female interactions as a possible key to understanding parental strategies. At a proximate level, the existing evidence implies a common physiological substrate for both paternal behavior and pair-bonds. Vasopressin, and perhaps prolactin and testosterone, apparently underlies the endocrinological bases of paternal care, and neuroanatomical reward pathways may be involved in the formation of attachment bonds. Understanding of the genetic structure of primate populations and the neurogenetics of social behavior is also emerging. A multidisciplinary approach that also considers epigenetic and transgenerational effects promises to open new avenues to explain the flexible nature of paternal care in primates.

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Callithrix and Callicebus have relatively similar social structures, characterized by high levels of sociality, selective breeding, maintenance of long-term male-female relationships, and biparental care.
“Callithrix and Callicebus have relatively similar social structures, characterized by high levels of sociality, selective breeding, maintenance of long-term male-female relationships, and biparental care (Digby, 1995; Fernandez-Duque et al., 2009; Spence-Aizenberg et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Fernandez-Duque et al., 2009

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Social Behavior, Reproductive Strategies, and Population Genetic Structure of Lagothrix poeppigii
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Paternity assessment in wild groups of toque macaques Macaca sinica at Polonnaruwa, Sri Lanka using molecular markers
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Prolactin and paternal care: Comparison of three species of monogamous new world monkeys (Callicebus cupreus, Callithrix jacchus, and Callimico goeldii).
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Mating, Parenting, and the Evolution of Human Pair Bonds
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Sociophysiology of squirrel monkeys
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Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can
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Adult male replacement and subsequent infant care by male and siblings in socially monogamous owl monkeys (Aotus azarai)
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A Prisoner’s Dilemma Model of the Evolution of Paternal Care
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Mating system and avpr1a promoter variation in primates
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Can knowledge of developmental processes illuminate the evolution of parental care?
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WOLF–BISON INTERACTIONS IN YELLOWSTONE NATIONAL PARK
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Impending extinction crisis of the world’s primates: Why primates matter
Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., Di Fiore, A., Nekaris, K. A.-I., Nijman, V., Heymann, E. W., Lambert, J. E., et al. (2017) · Science Advances · doi:10.1126/sciadv.1600946 · Cited by 1,466 · see citing works
Empathy: Gender effects in brain and behavior
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The Neurobiology of Human Attachments
Feldman, R. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.11.007 · Cited by 839 · see citing works
Beyond sexual orientation: integrating gender/sex and diverse sexualities via sexual configurations theory
van Anders, S. M. (2015) · Archives of Sexual Behavior · doi:10.1007/s10508-015-0490-8 · Cited by 651 · see citing works
The Evolutionary Origins of Friendship
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The Steroid/Peptide Theory of Social Bonds: Integrating testosterone and peptide responses for classifying social behavioral contexts
van Anders, S. M., Goldey, K. L., & Kuo, P. X. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.06.001 · Cited by 321 · see citing works
Children's Parents
Bornstein, M. H. (2015) · Wiley eBooks · doi:10.1002/9781118963418.childpsy403 · Cited by 227 · see citing works
Beyond masculinity: Testosterone, gender/sex, and human social behavior in a comparative context
van Anders, S. M. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.07.001 · Cited by 174 · see citing works
Testosterone and reproductive effort in male primates
Muller, M. N. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.09.001 · Cited by 174 · see citing works
The neural mechanisms and consequences of paternal caregiving
Feldman, R., Braun, K., & Champagne, F. A. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0124-6 · Cited by 168 · see citing works
Parenting and plasticity
Leuner, B., Glasper, E. R., & Gould, E. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.07.003 · Cited by 159 · see citing works
Baby cries and nurturance affect testosterone in men
van Anders, S. M., Tolman, R. M., & Volling, B. L. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.09.012 · Cited by 156 · see citing works
The neuroendocrinology of primate maternal behavior
Wendy Saltzman, A., & Dario Maestripieri, A. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.09.017 · Cited by 150 · see citing works
Morphological and population genomic evidence that human faces have evolved to signal individual identity
Sheehan, M. J., & Nachman, M. W. (2014) · Nature Communications · doi:10.1038/ncomms5800 · Cited by 145 · see citing works
Neural control of parental behaviors
Kohl, J., & Dulac, C. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.002 · Cited by 136 · see citing works
The neurobiology of fatherhood
Rilling, J. K., & Mascaro, J. S. (2017) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2017.02.013 · Cited by 135 · see citing works
The neurobiology of parenting: A neural circuit perspective
Kohl, J., Autry, A. E., & Dulac, C. G. (2016) · BioEssays · doi:10.1002/bies.201600159 · Cited by 131 · see citing works
Patterns of MHC ‐dependent mate selection in humans and nonhuman primates: a meta‐analysis
Winternitz, J. C., Abbate, J. L., Huchard, É., Havlı́ček, J., & Garamszegi, L. Z. (2016) · Molecular Ecology · doi:10.1111/mec.13920 · Cited by 118 · see citing works
Pair-bonding, fatherhood, and the role of testosterone: a meta-analytic review
Grebe, N. M., Sarafin, R. E., Strenth, C. R., & Zilioli, S. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.01.010 · Cited by 116 · see citing works
Functional Significance of Hormonal Changes in Mammalian Fathers
Saltzman, W., & Ziegler, T. E. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12176 · Cited by 114 · see citing works
Human Social Evolution: Self-Domestication or Self-Control?
Shilton, D., Breski, M., Dor, D., & Jablonka, E. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.00134 · Cited by 116 · see citing works
Variation in grouping patterns, mating systems and social structure: what socio-ecological models attempt to explain
Koenig, A., Scarry, C. J., Wheeler, B. C., & Borries, C. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0348 · Cited by 112 · see citing works
Primate paternal care: Interactions between biology and social experience
Storey, A. E., & Ziegler, T. E. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.07.024 · Cited by 111 · see citing works
The birth of new neurons in the maternal brain: Hormonal regulation and functional implications
Leuner, B., & Sabihi, S. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.02.004 · Cited by 110 · see citing works
Dendritic Growth in Medial Prefrontal Cortex and Cognitive Flexibility Are Enhanced during the Postpartum Period
Leuner, B., & Gould, E. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3388-10.2010 · Cited by 105 · see citing works
Prosocial behaviour emerges independent of reciprocity in cottontop tamarins
Cronin, K. A., Schroeder, K. K. E., & Snowdon, C. T. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2010.0879 · Cited by 103 · see citing works
Determinants of Parenting
Bornstein, M. H. (2016) · Wiley eBooks · doi:10.1002/9781119125556.devpsy405 · Cited by 107 · see citing works
Variable postpartum responsiveness among humans and other primates with “cooperative breeding”: A comparative and evolutionary perspective
Hrdy, S. B. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.10.016 · Cited by 101 · see citing works
The Heteronormativity Theory of Low Sexual Desire in Women Partnered with Men
van Anders, S. M., Herbenick, D., Brotto, L. A., Harris, E. A., & Chadwick, S. B. (2021) · Archives of Sexual Behavior · doi:10.1007/s10508-021-02100-x · Cited by 105 · see citing works
Applying socioendocrinology to evolutionary models: Fatherhood and physiology
Gettler, L. T. (2014) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.21412 · Cited by 99 · see citing works
Tamarins: Insights into monogamous and non‐monogamous single female social and breeding systems
Garber, P. A., Porter, L. M., Spross, J., & Fiore, A. D. (2015) · American Journal of Primatology · doi:10.1002/ajp.22370 · Cited by 84 · see citing works
Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys
Huck, M., Fernández‐Duque, E., Babb, P. L., & Schurr, T. G. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.0195 · Cited by 86 · see citing works
Evolution of Parental Care
Gilbert, J. (2013) · doi:10.1093/obo/9780199830060-0131 · Cited by 84 · see citing works
Fathers' decline in testosterone and synchrony with partner testosterone during pregnancy predicts greater postpartum relationship investment
Saxbe, D., Edelstein, R. S., Lyden, H. M., Wardecker, B. M., Chopik, W. J., & Moors, A. C. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.07.005 · Cited by 82 · see citing works
Growth and Development in Wild Owl Monkeys (Aotus azarai) of Argentina
Huck, M., Rotundo, M., & Fernández‐Duque, E. (2011) · International Journal of Primatology · doi:10.1007/s10764-011-9530-y · Cited by 79 · see citing works
Prenatal hormones in first‐time expectant parents: Longitudinal changes and within‐couple correlations
Edelstein, R. S., Wardecker, B. M., Chopik, W. J., Moors, A. C., Shipman, E. L., & Lin, N. J. (2014) · American Journal of Human Biology · doi:10.1002/ajhb.22670 · Cited by 79 · see citing works
Social Monogamy in Nonhuman Primates: Phylogeny, Phenotype, and Physiology
French, J. A., Cavanaugh, J., Mustoe, A. C., Carp, S. B., & Womack, S. L. (2017) · The Journal of Sex Research · doi:10.1080/00224499.2017.1339774 · Cited by 72 · see citing works
Paternal effects on access to resources in a promiscuous primate society
Huchard, É., Charpentier, M. J. E., Marshall, H. H., King, A. J., Knapp, L. A., & Cowlishaw, G. (2012) · Behavioral Ecology · doi:10.1093/beheco/ars158 · Cited by 75 · see citing works
The Parental Brain
Numan, M. (2020) · doi:10.1093/oso/9780190848675.001.0001 · Cited by 101 · see citing works
Neuropeptide diversity and the regulation of social behavior in New World primates
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.004 · Cited by 66 · see citing works
Attachment Theory and Fathers: Moving From “Being There” to “Being With”
Palm, G. F. (2014) · Journal of Family Theory & Review · doi:10.1111/jftr.12045 · Cited by 68 · see citing works
Becoming DADS
Gettler, L. T. (2016) · Current Anthropology · doi:10.1086/686149 · Cited by 66 · see citing works
Evolutionary pattern in the OXT-OXTR system in primates: Coevolution and positive selection footprints
Vargas-Pinilla, P., Paixão-Côrtes, V. R., Paré, P., Tovo-Rodrigues, L., Vieira, C. M. D. A. G., Xavier, A., Comas, D., Pissinatti, A., Sinigaglia, M., Rigo, M. M., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1419399112 · Cited by 59 · see citing works
The evolution of pair‐living, sexual monogamy, and cooperative infant care: Insights from research on wild owl monkeys, titis, sakis, and tamarins
Fernández‐Duque, E., Huck, M., Belle, S. V., & Fiore, A. D. (2020) · American Journal of Physical Anthropology · doi:10.1002/ajpa.24017 · Cited by 60 · see citing works
Descriptive Experiences and Sexual vs. Nurturant Aspects of Cuddling between Adult Romantic Partners
van Anders, S. M., Edelstein, R. S., Wade, R. M., & Samples-Steele, C. R. (2012) · Archives of Sexual Behavior · doi:10.1007/s10508-012-0014-8 · Cited by 60 · see citing works
Of Apples and Oranges? The Evolution of “Monogamy” in Non-human Primates
Huck, M., Fiore, A. D., & Fernández‐Duque, E. (2020) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2019.00472 · Cited by 58 · see citing works
Sexual conflict in primates
Stumpf, R. M., Martínez‐Mota, R., Milich, K. M., Righini, N., & Shattuck, M. R. (2011) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.20297 · Cited by 57 · see citing works
Owl monkeys A otusspp in the wild and in captivity
Fernández‐Duque, E. (2012) · International Zoo Yearbook · doi:10.1111/j.1748-1090.2011.00156.x · Cited by 55 · see citing works
The High Price of Success: Costs of Mating Effort in Male Primates
Thompson, M. E., & Georgiev, A. V. (2014) · International Journal of Primatology · doi:10.1007/s10764-014-9790-4 · Cited by 54 · see citing works
Personality Traits: A View From the Animal Kingdom
Weiß, A. (2017) · Journal of Personality · doi:10.1111/jopy.12310 · Cited by 52 · see citing works
The Association of Intergroup Encounters, Dominance Status, and Fecal Androgen and Glucocorticoid Profiles in Wild Male White‐Faced Capuchins (Cebus capucinus)
Schoof, V. A. M., & Jack, K. M. (2012) · American Journal of Primatology · doi:10.1002/ajp.22089 · Cited by 51 · see citing works
Explicit and implicit caregiving interests in expectant fathers: Do endogenous and exogenous oxytocin and vasopressin matter?
Cohen-Bendahan, C. C. C., Beijers, R., van Doornen, L. J. P., & de Weerth, C. (2015) · Infant Behavior and Development · doi:10.1016/j.infbeh.2015.06.007 · Cited by 50 · see citing works
Male and female robots
Rold, F. D., Petrosino, G., & Parisi, D. (2011) · Adaptive Behavior · doi:10.1177/1059712311417737 · Cited by 50 · see citing works
Evolving the neuroendocrine physiology of human and primate cooperation and collective action
Trumble, B. C., Jaeggi, A. V., & Gurven, M. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0014 · Cited by 50 · see citing works
How early maternal deprivation changes the brain and behavior?
Čater, M., & Majdič, G. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15238 · Cited by 51 · see citing works
Size, Site Fidelity, and Overlap of Home Ranges and Core Areas in the Socially Monogamous Owl Monkey (Aotus azarae) of Northern Argentina
Wartmann, F. M., Juárez, C. P., & Fernández‐Duque, E. (2014) · International Journal of Primatology · doi:10.1007/s10764-014-9771-7 · Cited by 48 · see citing works
Paternal care and the evolution of exaggerated sexual swellings in primates
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Authors: Fernandez-Duque, E., Valeggia, C. R., & Mendoza, S. P.
Affiliations: Department of Anthropology, University of Pennsylvania, Philadelphia, Pennsylvania 19104;
Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
University of California, Davis (US)
ORCID: Valeggia, Claudia R.
Venue: Annual Review of Anthropology
Publisher: Annual Reviews
Published: 2009-10-01
Volume: 38
Issue: 1
Pages: 115-130
ISSN: 0084-6570 (ISSN-L)
1545-4290
DOI: 10.1146/annurev-anthro-091908-164334
OpenAlex: W2170298557
Semantic Scholar: 301ca675e41e42d65c09f7cad571ad90a75c2d1f
Cited by: 232
References: 151
Citations by year: 2026: 3 · 2025: 9 · 2024: 11 · 2023: 7 · 2022: 7 · 2021: 16 · 2020: 30 · 2019: 14 · 2018: 11 · 2017: 16 · 2016: 23 · 2015: 22 · 2014: 18 · 2013: 11 · 2012: 13
FWCI: 1.46
Type: journal article
Language: en
Open access: green
hdl.handle.net
Licence: cc-by-nc-sa
Locations: Annual Review of Anthropology (publishedVersion)
Conicet (submittedVersion, cc-by-nc-sa)
Funders: National Science Foundation (0621020)
Wenner-Gren Foundation
Leakey Foundation
National Geographic Society
University of Pennsylvania
Consejo Nacional de Investigaciones Científicas y Técnicas
Topics: Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords: paternal care, primate social behavior, human evolution, pair bonding, vasopressin, prolactin, testosterone, reward pathways, attachment, neuroendocrinology, epigenetics, transgenerational effects, male-female interaction, parental strategies

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The biology of paternal care in human and nonhuman primates

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