Transition to siblinghood causes a substantial and long-lasting increase in urinary cortisol levels in wild bonobos

  1. Verena Behringer
  2. Andreas Berghänel
  3. Tobias Deschner
  4. Sean M Lee
  5. Barbara Fruth
  6. Gottfried Hohmann

  • Curated by eLife

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    Evaluation Summary:

    This paper documents in wild bonobos significant physiological changes in response to becoming a sibling for the first time. The authors find that new siblings' cortisol increases dramatically, while their neopterin (a marker of immune function) decreases. This paper will be of interest to those who study development, life history transitions, and colleagues at the intersection of physiology and behavior, in particular in primates and other mammals with slow life histories.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #3 agreed to share their name with the authors.)

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Abstract

In animals with slow ontogeny and long-term maternal investment, immatures are likely to experience the birth of a younger sibling before reaching maturity. In these species, the birth of a sibling marks a major event in an offspring’s early life as the older siblings experience a decrease in maternal support. The transition to siblinghood (TTS) is often considered to be stressful for the older offspring, but physiological evidence is lacking. To explore the TTS in wild bonobos, we investigated physiological changes in urinary cortisol (stress response), neopterin (cell-mediated immunity), and total triiodothyronine (T3, metabolic rate), as well as changes in behaviors that reflect the mother–offspring relationship. Following a sibling’s birth, urinary cortisol levels of the older offspring increased fivefold, independent of their age, and remained elevated for 7 months. The cortisol level increase was associated with declining neopterin levels; however, T3 levels and behavioral measures did not change. Our results indicate that the TTS is accompanied by elevated cortisol levels and that this change does not coincide with nutritional weaning and attainment of physical independence. Our results suggest that bonobos and humans experience TTS in similar ways and that this developmental event may have emerged in the last common ancestor.

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  1. Version published to 10.7554/elife.77227 on eLife
  2. eLife

    Evaluation Summary:

    This paper documents in wild bonobos significant physiological changes in response to becoming a sibling for the first time. The authors find that new siblings' cortisol increases dramatically, while their neopterin (a marker of immune function) decreases. This paper will be of interest to those who study development, life history transitions, and colleagues at the intersection of physiology and behavior, in particular in primates and other mammals with slow life histories.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #3 agreed to share their name with the authors.)

  3. eLife

    Reviewer #1 (Public Review):

    This manuscript examines the behavioral and physiological responses of wild bonobos to the birth of a younger sibling. It contains some quite interesting findings that contribute to our understanding of the effects of a major life history transition in a primate species that is closely related to humans. There are many strengths of this paper, including a novel use of a fantastic longitudinal data set that incorporates both behavioral and physiological measures.

    I think there are several things that can be done to help improve the clarity and utility of the paper for readers. First, the very human-centric framing doesn't feel like it is setting up the findings as well as it could be. It repeatedly emphasizes that a study like this has not been done in humans. That would be interesting to do, and this study certainly helps provide justification for doing one, but studies that haven't been done in humans aren't a very good justification for doing this study in bonobos.

    The transition to siblinghood is not something that is unique to humans, and I think the framing would feel like a better fit for the topic if it was less concerned with humans and took a bigger-picture comparative approach. Becoming a sibling at or shortly after weaning is something that happens to the majority of individuals in species with slow life histories, and is a fairly significant life-history transition. Re-orienting towards that would help make the introduction feel less 'forced' than it does currently.

    Second, there are a couple of non-trivial results (or really interpretations of results) that require more explanation. The authors contend that their data show evidence of a precipitous drop in cort at around seven months post-TTS. However, the paper does not address why this might be. I would assume that the most biologically plausible scenario would be that cort would slowly return to baseline over the course of several months, as older siblings adjust to their new reality. If that's not what we find, then what potential explanation do we have both for the massive drop itself, and the timing of that drop?

    Somewhat relatedly, the paper connects the jump in cort to the observed decrease in neopterin around the birth of younger siblings. But, it does not address the fact that the return of cort to baseline levels does not correspond with an increase in neopterin. Instead, the data suggest that neopterin does not recover, at least not on the (non-trivial) timescales examined in this study. This is not currently talked about in the discussion, and it should be.

    Finally, in the discussion, the authors propose that a potential reason for the observed increase in cort levels is increases in male aggression. This paragraph is currently not well-integrated into the rest of the paper. If this phenomenon (i.e., the cort increase) is caused by male aggression, then this has important implications for the applicability of these findings to other species. This is a fundamentally different thing than animals being psychologically stressed by the arrival of a new sibling, which seems to me to be the primary take-away that is emphasized throughout the rest of the manuscript. Related to an earlier point, it would be useful to know if and how this explanation comports with the observed cort drop 7 months post-birth.

  4. eLife

    Reviewer #2 (Public Review):

    In this manuscript, Behringer et al. tackle the topic of transitions to siblinghood (TTS), a domain of research dominated by developmental psychology, using comparative evidence. Within psychological research, there is substantial heterogeneity, and controversy, concerning how becoming a sibling affects a child. Looking to address this question with a fresh approach, the authors compile a longitudinal dataset of urine biomarker measurements, as well as some indications of dependence on mothers, in a group of 26 bonobos before and after the birth of their first younger siblings. Urinary cortisol peaks around the time of a sibling's birth, and urinary neopterin drops, with the magnitude of these changes seemingly not moderated by the older sibling's age (within the range of ages observed in this study). While older siblings show relatively diminished interactions with mom when younger siblings are born, this appears to be the consequence of gradual independence that has either been partially or fully realized by the time of birth.

    In terms of strengths, the technical details of the assays and statistical models are largely clear and well-supported. The main findings are intriguing, particularly the large jump in cortisol, which has not been documented before in an ape. While the authors briefly discuss several interpretations of this result, they appear to favor the conclusion that 'a cortisol jump shows the transition to siblinghood is ubiquitously stressful in bonobos'-I see this as a fair paraphrase, given for instance manuscript lines 372-377. It is clear the authors see this cortisol effect as the most impactful part of their manuscript. Unfortunately, it is not at all clear whether this central finding constitutes solid evidence for their favored conclusion. Romero and Beattie (2021; https://doi.org/10.1002/jez.2459), in their paper about "myths of glucocorticoid function", provide a succinct summary of how equating elevated cortisol to stress is problematic: "Glucocorticoid concentrations provide no predictive value in determining whether a wild animal is or is not chronically stressed ... Not only will many wild animals suffering from chronic stress show no changes in glucocorticoid concentrations, but decreases may also reflect chronic stress. A diagnosis of chronic stress requires other corroborating evidence, such as weight loss, changes in fitness, etc." In other words, without accompanying behavioral and/or physical evidence of stress, it is equally plausible to interpret cortisol increases as evidence of TTS being stressful, or it being an occasion for ecological adjustment that does not manifest in stress. Either end of this interpretive axis has support in the developmental psych literature (e.g., Volling, 2012, which the authors cite).

    I was really hoping to see some of this corroborating evidence in the present manuscript-for instance, some behavioral measures from the sibling that would indicate distress-but this important element is missing. The existing behavioral measures, which concern dependency on the mother, are interesting, but on their own they are not nearly enough to support claims like "our results on wild bonobos support ... that the birth of a sibling is a highly stressful event for the older offspring" (lines 374-375). The limited scope of available behavioral data also raises additional interpretative questions. Cortisol increases for a circumscribed period of time-seven months, according to the authors--after which levels are indistinguishable from pre-birth concentrations (line 186). The authors attribute this to behavioral adaptation, but we have no idea whether/how bonobos in fact behaviorally adjust to their new conditions or their siblings.

    In sum, the manuscript presents some very interesting patterns, but a number of important limitations must be overcome before it can speak to evolutionary and developmental theories of TTS.

  5. eLife

    Reviewer #3 (Public Review):

    The study design was excellent, and I really enjoyed seeing how the physiological (urinary hormones) and behavioral (infant feeding and proximity to the mother) measures related to one another. The set-up of the article was good and outlined why this study was necessary and important. The authors did a great job using statistical analyses to disentangle the various effects of different variables, particularly that of TTS (birth of a new sibling) from age and sex on the main behavioral and physiological measures. The conclusions of the article are well supported by the data and the analyses, and the discussion addresses several possibilities and lines of evidence, which I agreed with, and thought was quite thorough. I am not an expert on the urinary hormones tested and used in the study (cortisol, T3, neopterin), so am unfortunately not able to thoroughly evaluate the credibility of these measures and methods. My main requested changes concern clarity of various concepts and ideas, and an elaboration of two major concepts that are assumed but that are not properly discussed or fleshed out in the paper. Namely, the idea of a nutritional weaning that is separate from social/behavioral weaning, and the discussion about the evolutionary origins of the mechanism uncovered in the paper.

    First, throughout the manuscript, the authors assume a distinction between nutritional versus social or behavioral weaning. I am very happy the authors are making this important distinction; however, this concept in itself is fairly innovative. The idea that there are two components to weaning, the milk-transfer component versus the psycho-social relationship between the mother and the infant (sometimes including continued nipple contacts without milk transfer, so regardless of whether or not milk transfer occurs), is an idea that needs to be supported with literature in your paper, and that needs to be explained a little bit somewhere in the text. For example, research has shown that comfort nursing, without milk transfer, can occur for years after lactation has ended in some primates (e.g., chimpanzees). This sets up a situation where you have two separate weaning periods: weaning from milk and weaning from nipple contact, or weaning from milk and weaning from behaving as an infant (i.e., the nutritional versus social/behavioral weaning that you talk about). Thus, the mother-infant behavioral relationship can develop separately from the mother-infant nutritional relationship, despite considerable overlap between the two. This concept is innovative because it is a little bit different from the classic mother-offspring conflict and maternal investment theories (Trivers). I would like the authors to explain this distinction between behavioral and nutritional weaning, and explain its importance for the infant and mother, and give credit to others who have worked on this idea.

    Second, the concluding statements in the discussion that the results highlight the evolutionary history of a stress response and TTS for immature individuals is vague and almost seems like a throw away idea because it is not specific enough. I would like the authors to go a step further and talk about the possible timing of an evolutionary link between stress and TTS. Presumably, this important interaction would have appeared with the great ape transition, or possibly with the transition between genus Pan and Homo. I would like the authors to dig a little deeper in this idea and use the comparisons in life history traits and infant development of humans and the other great apes that would be set up in the introduction to infer when this stress mechanism they found could have become more prominent in the evolutionary history of primates.

    Lastly, the introduction (and a bit in the discussion) at times lacked clarity because the reader did not receive all the information needed, or the connection between two ideas was not made explicit enough. Sometimes things were implied (and would be understood by a specialist audience) but not made explicit so that a non-specialist reader might have trouble completely making the link between the ideas. Thus, there were several sections I will point out in my line-by-line review that could use either a reformulation of the statement or an elaboration of the ideas to make them clearer for the reader.

  6. Version published to 10.1101/2022.02.14.480345v1 on bioRxiv