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The expression of father-daughter bond behaviors influences adult partner attachment in titi monkeys

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Abstract

Coppery titi monkeys (Plecturocebus cupreus) are socially monogamous monkeys that display strong pair bonds similar to human romantic attachments, preceded by infant attachment to their fathers. To understand how father-daughter bonds impact adult relationship dynamics, we established a novel method for quantifying expression of bond-related behaviors. We assessed behavioral and neural correlates of preference, stress buffering, and separation distress to identify how females’ current and former attachment figures impact female attachment. Whereas all females (n = 9) shifted to preferring their partner over father six-months post-pairing, females that exhibited higher expression of juvenile parent preference maintained a relationship with their father six-months post-pairing, as evidenced by higher-than-expected father proximity. Higher expression of juvenile measures of proximity following a brief separation predicted slightly increased partner proximity in adulthood. Neural activity patterns in brain regions assessed pre- and post-pairing showed high similarity in glucose metabolism, despite overall activity being lower post-pairing. While there was some inconsistency in results, higher expression of juvenile proximity following a separation was associated with enhanced reduction in activity within social bonding brain regions (social salience network, periaqueductal gray, cerebellum), suggesting a potential stress buffering benefit via reduced threat-related brain activation, like that seen in high-quality human relationships. These findings advance current knowledge of how early relationships may shape adult bond-related behavior and neural activity.

Data availability

The datasets generated during and/or analyzed during the current study are available in the Zenodo repository, https://doi.org/10.5281/zenodo.15660221.

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Acknowledgements

We would like to thank the following for their invaluable assistance: Jaleh Janatpour, Kevin Theis, Charles Smith, the veterinary staff at California National Primate Research Center (CNPRC), and the Bales Laboratory undergraduate and international interns. We would also like to thank Alan Conley and Rebecca Cotterman for the work measuring plasma cortisol. This research was funded by the National Institute of Child Health and Human Development [grant number R01HD092055 to Karen L. Bales], by the National Institutes of Health base grant [grant number P51OD011107 to Prasant Mohapatra and the CNPRC], and the National Institutes of Health [grant number S10OD021715 to Simon Cherry].

Funding

This research was funded by the National Institute of Child Health and Human Development [grant number R01HD092055 to Karen L. Bales], by the National Institutes of Health base grant [grant number P51OD011107 to Prasant Mohapatra and the CNPRC], and the National Institutes of Health [grant number S10OD021715 to Simon Cherry].

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Authors and Affiliations

  1. Department of Psychology, University of California, Davis, Davis, CA, USA

    Lynea R. Witczak, Allison R. Lau, Emilio Ferrer & Karen L. Bales

  2. California National Primate Research Center, University of California, Davis, Davis, CA, USA

    Lynea R. Witczak, Allison R. Lau, Brad A. Hobson, Pauline B. Zablocki-Thomas, Madison Dufek, Abhijit J. Chaudhari & Karen L. Bales

  3. Graduate Program in Animal Behavior, University of California, Davis, Davis, CA, USA

    Allison R. Lau & Karen L. Bales

  4. Center for Molecular and Genomic Imaging, University of California, Davis, Davis, CA, USA

    Brad A. Hobson & Abhijit J. Chaudhari

  5. Department of Biology, Utah State University, Logan, UT, USA

    Sara M. Freeman

  6. Department of Radiology, University of California, Davis, Davis, CA, USA

    Abhijit J. Chaudhari

  7. Department of Neurobiology, Physiology, and Behavior, University of California, Davis, Davis, CA, USA

    Karen L. Bales

  8. Department of Biology, 100 Campus Drive, Elon, NC, 95616, USA

    Lynea R. Witczak

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  1. Lynea R. Witczak
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Contributions

L.R.W. lead study conceptualization, methodology, formal analysis, investigation, and visualization. L.R.W. and A.R.L. wrote the paper. M.D. and P.B.ZT. assisted with investigation and project administration. S.M.F., B.A.H., and A.J.C. assisted with methodology. E.F. provided guidance on formal analysis. K.L.B. acquired funding for the project, providing essential resources, and was the supervisor for L.R.W, guiding project conceptualization and methodology. All authors had access to the data, commented on the manuscript drafts, and approved the final submitted version.

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Lynea R. Witczak.

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Witczak, L.R., Lau, A.R., Hobson, B.A. et al. The expression of father-daughter bond behaviors influences adult partner attachment in titi monkeys.
Sci Rep (2025). https://doi.org/10.1038/s41598-025-31143-6

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  • DOI: https://doi.org/10.1038/s41598-025-31143-6

Keywords

  • Neuroimaging
  • Preference test
  • Pair bond
  • Filial bond
  • Social salience network
  • Stress buffering

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