In mammals, weaning refers to the transition from nutritional dependency to a stage when immatures are independent of maternal food provisioning. The term weaning is often used for the attainment of nutritional independence, but also comprises the process of social independence and behavioral maturation, which can occur at different ages. Weaning age varies within and across species, and is an important developmental stage in the life history of mother and offspring (Smith, 2013; Weary et al., 2008). While the dependency on post-weaning maternal support can be inferred from behavioral observations, the putative fitness effects are rarely explored. A reduction or complete loss of maternal support has substantial fitness costs throughout an individual’s life span (Zipple et al., 2021). However, while maternal loss is a dramatic event, there are normative events such as sibling birth that affect the life of the older offspring. In vertebrate species with a slow development, many immatures grow up with siblings, and sibling relationships can have profound influences on fitness (Berger et al., 2021; Nitsch et al., 2013). The younger sibling may benefit from an older sibling in terms of survival, reproductive maturation, and socialization (Berger et al., 2021; Nitsch et al., 2013; Stanton et al., 2017). However, the older offspring must share maternal care, which may influence its social behavior as well as its physiological constitution.

Primates differ from most other social mammals in having remarkably slow life histories (Charnov and Berrigan, 1993; Jones, 2011). Immatures grow slowly, social maturation extends well into adulthood, and to a certain degree, beneficial mother–offspring relationships can last a lifetime (Jones, 2011; Pereira and Fairbanks, 1993; Surbeck et al., 2019). Therefore, female primates may give birth to another infant before the older offspring reaches physical or social maturity, or even before being weaned. For the older offspring, this transition to siblinghood (TTS) marks the onset of considerable changes, including the sudden emergence of a competitor for maternal resources (sibling rivalry; Dettwyler, 2017; Myers and Bjorklund, 2018) and a decline in maternal support (Kramer, 2011). Accordingly, in humans, TTS is considered to be a stressful life event for the older sibling even under favorable conditions, a perspective that seems to be supported by TTS-related behaviors of the older offspring such as aggression, clinginess, and depressive syndromes. However, sibling birth also presents opportunities for the older offspring, such as social and emotional growth through interacting with the newborn. Individuals vary in how they adjust to the birth of a younger sibling; some children have difficulties while others cope well (reviewed in Volling, 2012; Volling et al., 2017). In any case, the birth of a sibling is linked to a time of change the older child must cope with. Evidence from nonhuman primates is scarce, but the available information resembles reports from humans (Devinney et al., 2003; Schino and Troisi, 2001). However, whether behavioral changes during TTS are actually associated directly with sibling birth, or are rather simply a result of age-related withdrawal of maternal support, remains to be resolved (Volling, 2012; Volling et al., 2017).

TTS could overlap with and/or accelerate weaning and attainment of physical independence, which, on its own, is known to be stressful in primates and other mammals (e.g., Hau and Schapiro, 2007; Mandalaywala et al., 2014). As a result, it is difficult to differentiate between the effects of sibling birth and weaning (Volling, 2012; Weary et al., 2008). Nutritional weaning refers to the termination of an offspring’s consumption of maternal milk, though they may still continue nipple contact (without milk transfer) – this is assumed to be a social comfort behavior (Bădescu et al., 2017; Berghänel et al., 2016; Matsumoto, 2017). It is common that females give birth to another infant before the older offspring reaches full independence, resulting in an overlap of dependency in siblings of different ages (Achenbach and Snowdon, 1998). In nonhuman primates, sibling birth affects the quality and quantity of interactions between the older offspring and the mother (Schino and Troisi, 2001; van Noordwijk and van Schaik, 2005), and may affect the fitness of the older offspring throughout its life (Alberts, 2019; Bădescu et al., 2022; Thompson et al., 2016; Tung et al., 2016; Zipple et al., 2019).

Apes offer a particularly suitable model to explore developmental changes in an evolutionary context (Sayers, 2015): maternal support is intense and persists for a long time (Stanton et al., 2020; van Noordwijk et al., 2018), and extended periods of parental care of two dependent offspring of different ages are common (Achenbach and Snowdon, 1998). Juvenile apes associate with their mother for several years after nutritional weaning. While data on mother–offspring relationships are abundant, little is known about the interactions between immatures and infants born to the same female (Watts and Pusey, 1993). Wild orangutans have the longest known mammalian inter-birth interval (7–9 years), and sibling rivalry is likely modest or less intense since the close association of the mother with the older offspring ends before the next infant is born (van Noordwijk et al., 2018; van Noordwijk and van Schaik, 2005). In gorillas, inter-birth intervals range from 4 to 6 years (Stoinski et al., 2013). In male mountain gorillas, sibling bonds may last into adulthood (Robbins, 1995), and following maternal loss, siblings may provide social support (Morrison et al., 2021), indicating that siblings are strong partners in this species. In wild chimpanzees, inter-birth intervals range from 2 to 11 years (Thompson, 2013). There is one anecdotal report of an older offspring responding to sibling birth with increasing attempts to establish physical contact with the mother and the emergence of signs of depression (Clark, 1977). Based on this, it can be assumed that depending on the species, immature apes experiencing the birth of a sibling are exposed to different social environments: Because a greater difference in sibling ages may correspond to less conflict in terms of their maternal support needs, it is likely that species with shorter inter-birth intervals (gorillas and chimpanzees) experience stronger effects of TTS than those with longer intervals (orangutans).

Immature bonobos depend heavily on their mothers and maintain close spatial and physical contact during the first 2 years of life (De Lathouwers, 2004; Kuroda, 1989; Lee et al., 2020). After the age of 5 years, spatial distance to the mother increases (Kuroda, 1989; Toda et al., 2021), but in the case of sons, associations between mothers and offspring persist even when sons reach adulthood (Hohmann et al., 1999; Surbeck et al., 2019). Nutritional weaning occurs between 4 and 5 years of age (Kuroda, 1989; Oelze et al., 2020), and behavioral observations and urinary cortisol measures indicate that nutritional weaning is less stressful in bonobos than in chimpanzees (De Lathouwers and Van Elsacker, 2006; Tkaczynski et al., 2020). Notably, monitoring changes in urinary cortisol levels during weaning revealed the first evidence that the older offspring may respond physiologically to the birth of a sibling (Tkaczynski et al., 2020).

Here, we investigate TTS-related changes in physiological responses in wild habituated juvenile bonobos (Pan paniscus) at LuiKotale in the Democratic Republic of Congo. We used multiple physiological and behavioral measures to investigate the responses of older siblings to the birth of their younger sibling. We sought to disentangle the effects of changes in mother–offspring relationships and energetics that are associated with nutritional and social weaning, from the specific effects of a younger sibling’s birth. We leveraged the large variation in inter-birth intervals in bonobos (Knott, 2001; Tokuyama et al., 2021) to differentiate between the effects of TTS versus nutritional and social weaning. In our study population, inter-birth intervals ranged from 2.3 to 8.6 years (mean ± SD = 5.4 ± 1.5 years) (Tkaczynski et al., 2020), and thus the developmental status of older siblings at the time when their mothers gave birth to another infant ranged from highly dependent in terms of travel support and foraging skills (i.e., time carried and nursed) to mostly independent. This discordance between inter-birth interval lengths and the developmental timelines of the older offspring enabled us to explore the specific effects of TTS on older siblings’ (a) physiological stress response (cortisol), (b) immunity (neopterin), (c) energetic change (total T3), (d) relationships with their mothers, and (e) changes in foraging and travel competence, while controlling for (f) offspring sex and age.

Changes in cortisol are widely accepted as a physiological marker to quantify stress responses in humans and other mammals because after exposure to a stressor – an event that challenges homeostasis – cortisol is secreted to restore homeostasis (Karatsoreos and McEwen, 2010; Romero and Beattie, 2022). Cortisol is produced in response to physical as well as psychosocial stressors (Kirschbaum and Hellhammer, 1994; McEwen, 2017). In children, salivary cortisol levels increase during traumatic family events and/or in anticipation of important positive or negative events, indicating that cortisol measurements are a valuable tool to assess children’s stress responses to family and social interactions (Flinn et al., 2012; Flinn et al., 2011). We expected that TTS is experienced by the older offspring as a challenging event. Therefore, we predicted a sudden increase in cortisol levels at the time of sibling birth in reaction to this event.

Neopterin is produced by macrophages, monocytes, and dendritic cells after activation. Therefore, an increase in neopterin levels reflects the activation of cell-mediated immune response after an infection with intracellular pathogens (Murr et al., 2002). Immune responses are linked to changes in cortisol levels. While a short increase in cortisol levels can support immune functions, long-term elevation of cortisol levels suppresses immune function (Dhabhar, 2014). Therefore, if TTS stimulates a short increase in cortisol levels, we expect increasing or unchanged neopterin levels, whereas if TTS causes a long-lasting cortisol response, we expect a decline in neopterin levels.

Triiodothyronine (T3) is a thyroid hormone that influences metabolic rate. T3 levels decline during times of energy restriction to conserve energy (reviewed in Behringer et al., 2018). Measuring total T3 levels allows for disentangling the effects of energetic and social stressors, which may both occur around the age of nutritional weaning and/or TTS (Maestripieri, 2018; Mandalaywala et al., 2014). If sibling birth induces metabolic issues in the older offspring, we would expect a decline in total T3 levels following sibling birth.

We complemented physiological measures with behavioral scores of nipple contact and riding, the time offspring spent in body contact with their mothers, 5 m proximity to the mother, and independent foraging. Changes in these parameters can indicate nutritional weaning and attainment of physical and social independence around TTS. We compared measures of these parameters in the older offspring before versus after the birth of a sibling to investigate whether TTS-related changes in cortisol can be linked to similar changes in behavior and thus to weaning patterns and changes in the mother–offspring relationship.

Our main results are summarized in Table 1, and model structures can be derived from Tables 2 and 3, and from Supplementary file 1. We applied nonlinear generalized additive mixed models (GAMM) to investigate continuous changes in our parameters of interest around the time of sibling birth and compared those models to identical ones in which we added a categorical distinction between before and after sibling birth to allow noncontinuous, sudden changes at sibling birth. We considered that our response variables may naturally change with offspring age. Age-related changes in our response variables might (a) directly mediate potential changes during TTS in case of strong temporal overlap and (b) moderate these effects as the impact of TTS may decline with decreasing dependency of older offspring from maternal support. To control for potential mediation, we ran a model with age for all our response variables. If TTS has effects beyond weaning, we would expect sudden changes at the time of sibling birth also after controlling for age-related changes. To investigate whether continuous and sudden effects of sibling birth decrease with increasing age at sibling birth, we split individuals along the median (5.11 years old at sibling birth) and ran additional models that allowed for different trajectories around sibling birth for the two age cohorts. Finally, we generated continuous two-way interaction plots to visually inspect whether and how the trajectories around sibling birth changed with increasing offspring age (for more details see ‘Methods’).

Physiological changes during TTS

Urinary cortisol level changes in response to TTS

At the time of sibling birth, older offspring’s cortisol levels showed a significant and sudden, noncontinuous, up to fivefold increase from the level prior to this event (cortisol model with one sudden change; Figure 1A–C, Table 2). Compared to a model that allowed for nonlinear, but only continuous, fitting of the data (cortisol model without sudden change, Figure 1—figure supplement 1A and B), allowing for discontinuity (i.e., a sudden change) in cortisol levels at the time of sibling birth (cortisol model with sudden change), significantly improved model fit (Figure 1—figure supplement 1A and B; Chi²(1) = 9.30, p<0.001), even if the continuous model was allowed to be wiggly and to overfit the data (Figure 1—figure supplement 2A).

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Post-hoc visual inspection of urinary cortisol levels indicated that urinary cortisol remained high for a long time. None of the older offspring’s samples collected during the months after sibling birth had low cortisol levels (Figure 1A–C, Figure 1—figure supplement 3); cortisol measures in all samples collected within 7 months following sibling birth were above the upper 99.9% confidence interval of the values from before sibling birth. Lower cortisol values appeared later, only after 7 months post-birth (Figure 1—figure supplement 3). To verify this unexpected pattern, we ran another model allowing for an additional discontinuity in cortisol levels, that is, one at sibling birth and another one 7 months later. This model (Supplementary file 1) significantly improved model fit (cortisol model with two sudden changes compared to the model with only one sudden change at sibling birth, Figure 1—figure supplement 4A: Chi²(1) = 18.36, p<0.001; compared with the continuous model without sudden change, Figure 1—figure supplement 1A: Chi²(2) = 27.65, p<0.001). Cortisol levels in samples collected after the 7-month period were not different from before sibling birth (Supplementary file 1). While the model with the two discontinuities describes our data better mathematically, there is no obvious biological explanation for the second change (i.e., the sudden decline in cortisol) after 7 months. However, also in the model with only one discontinuity at sibling birth and a smooth continuous decline thereafter (Figure 1A–C), the cortisol levels took over 7 months to return to previous levels. Hence, the absence of low cortisol levels after sibling birth was evident in both models.

Cortisol trajectories around sibling birth were independent of the age of the older sibling. Allowing for different levels and trajectories in older and younger individuals did not improve the model (Figure 1B, Figure 1—figure supplement 4B; Chi²(3) = 0.28, p=0.91), suggesting that the cortisol level changes were not moderated by offspring age, a finding that was also apparent from visual inspection of continuous interaction plots (see Figure 1C, Figure 1—figure supplement 5A, B for perspective plots). Hence, the effect of TTS did not decrease with increasing age of the older sibling. Introducing two sudden changes, cortisol trajectories around sibling birth did not decrease with increasing age of the older sibling (Figure 1B, Figure 1—figure supplement 4B, C; Chi²(3) = 1.12, p=0.53) and sex of older sibling did not affect the results (Figure 1A, Table 2).

Urinary neopterin level changes in response to TTS

Just after sibling birth, urinary neopterin levels of older offspring decreased significantly and discontinuously (neopterin model with one sudden change, Figure 1D–F, Table 2). Compared to the model allowing for nonlinear but continuous fitting of the data (neopterin model without sudden changes, Figure 1—figure supplement 1D), a model with discontinuity in neopterin levels at the time of sibling birth significantly increased model fit (neopterin model with one sudden change, Figure 1D; Chi²(1) = 4.28, p=0.003), even if the continuous model allowed for extreme wiggliness and overfitting of the data (Figure 1—figure supplement 2B). Post-hoc visual inspection of neopterin data suggested a 4.5-month post-birth period with particularly low neopterin levels (all values during the 4.5-month post-birth period were below the mean from before or after sibling birth). Running an additional model, allowing a second discontinuity in neopterin levels at 4.5 months, slightly improved model fit (neopterin model with two sudden changes, Figure 1—figure supplement 4D–F; Chi²(1) = 1.95, p=0.048). However, even when allowing for a second discontinuous change, neopterin levels in samples collected after sibling birth remained significantly lower than before sibling birth (Supplementary file 1).

Model fit did not improve when we allowed moderation of this effect by the age of the older offspring at sibling birth (allowing for different pattern in older and younger individuals: Chi²(3) = 1.19, p=0.50, Figure 1E, F, Figure 1—figure supplement 4E, F), and again, there was no sex difference in neopterin levels before or after sibling birth (Figure 1D, Table 2).

Total T3 levels during TTS

Urinary total T3 levels increased around the time of sibling birth (Figure 1G–I), but this change could neither be attributed to the age of the older siblings nor to the event of sibling birth. The model including both variables was not significantly different from the null model (p=0.096). A reduced model including only the event of sibling birth but not age was significantly better than the null model (p=0.020, Figure 1G, Table 2). There was neither a significant sex effect on urinary total T3 levels during TTS nor a significant and sudden change in total T3 levels at sibling’s birth (Figure 1G, Table 2; allowing for sudden change: Chi²(1) = 1.27, p=0.11). Adding interaction terms with age of the older offspring did not improve the model, nor did it if allowed for differences between older and younger individuals (Chi²(3) = 0.40, p=0.85; Figure 1I).

Behavioral changes during TTS

Nipple contact during TTS

The proportion of time the older offspring was observed in nipple contact showed a continuous decrease prior to sibling birth in both males and females, and reached zero about 2 months before sibling birth (Figure 2A–C, Table 3). Consequently, there was no sudden change at sibling birth in terms of nipple contact (Figure 2A–C, Table 3; Chi²(1) = 0.81, p=0.20). Allowing for different trajectories depending on the age categories of the older offspring at sibling birth (younger or older than 5.11 years old at sibling birth) significantly improved the model (allowing for different pattern in older and younger individuals: Chi²(3) = 4.99, p=0.019) and visual inspection of the data indicated that nipple contact persisted mainly in younger offspring (Figure 2B and C, Figure 2—figure supplement 1A).

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Riding on the mother during TTS

The proportion of time the older offspring was riding on the mother during travel continuously decreased before sibling birth, then showed a significant and sudden decline at the time of sibling birth, and remained low thereafter (Figure 2D–F, Table 3; allowing for discontinuity at sibling birth: Chi²(1) = 6.06, p<0.001). Overall, sons spent significantly more time riding on their mothers than daughters, and the continuous decline before sibling birth was only significant in daughters, whereas the sudden decline at sibling birth appeared to be stronger in sons (Figure 2D, Table 3).

Adding the older offspring’s age categories significantly improved the model (allowing for different trajectories in younger and older individuals: Chi²(3) = 9.32, p=0.001; Figure 2E). Visual inspection of the data showed that the sudden decline in riding at sibling birth was only evident in older siblings belonging to the younger age cohort (less than 5.11 years old at sibling birth), whereas older siblings in the older age cohort were completely independent from maternal carrying before sibling birth (Figure 2E and F, Figure 2—figure supplement 1B). Hence, the effect of TTS on riding disappeared with increasing age of the older sibling.

Independent foraging during TTS

There was no effect of TTS on the proportion of time that offspring spent foraging on their own at times when mothers were foraging, and none of the full or reduced models was significantly different from the corresponding null models. Visual inspection of model results revealed that the proportion of time spent foraging independently reached high levels before sibling birth and did not change during the time window around sibling birth that was considered in our models (Figure 2—figure supplement 1A–D). In fact, all subjects were rather independent in terms of foraging at the time of sibling birth, irrespective of their age. In particular, there was no significant discontinuity at sibling birth (Figure 2—figure supplement 2A–D).

Body contact and 5 m proximity with the mother during TTS

The proportion of time that older offspring spent in body contact with or in proximity (within 5 m) to their mothers showed similar trajectories relative to sibling birth (Figure 2G–L). Both variables decreased before and around the time of sibling birth, reaching low levels at the time of gestation (Figure 2G–L, Table 3). This pattern could be attributed neither to the age of older offspring nor to the event of sibling birth. The models including both age and time around sibling birth were not significantly different from corresponding null models (body contact: p=0.055, 5 m proximity: p=0.062) but models without age were significantly different from the respective null models (both p<0.001, Table 3).

For 5 m proximity, there was no sudden change at sibling birth (Figure 2J–L; allowing for discontinuity at sibling birth: Chi²(1) = 0.016, p=0.86), nor did the pattern change with the age categories of the older sibling at sibling birth (allowing for different trajectories in younger and older individuals: Chi²(3) = 0.33, p=1; Figure 2K).

For body contact, there was a significant sudden change at sibling birth (Chi²(1) = 7.60, p<0.001), but in contrast to what one would expect to see in case of social weaning, this change was a sudden increase in body contact with the mother (Figure 2G, Table 3). Allowing moderation of the TTS effect by the age of the older offspring did not improve the model (allowing for different levels and trajectories in younger and older individuals: Chi²(3) = 1.86, p=0.29; Figure 2H and I), and the sudden increase in body contact at the time of sibling birth was independent of the age of the older offspring at sibling birth.

Our data from wild bonobos demonstrate that the birth of a sibling induced a sudden increase in urinary cortisol levels in the older offspring, a physiological response that occurred in all subjects regardless of their age. Upon birth of a sibling, urinary cortisol levels in the older offspring increased fivefold and remained at this level for about 7 months. Simultaneously, neopterin levels declined at the time of the birth of a sibling and remained at low levels for about 5 months. This suggests that the birth of a sibling induced a cortisol response and reduced or suppressed cell-mediated immunity in the older offspring. Older offsrping’s physiological changes around sibling birth did not decrease with increasing age of the older sibling and were independent of behavioral measures of weaning and attainment of physical independence. At sibling birth, weaning-related behavioral changes were either already completed (independent foraging and nipple contact), did not change discontinuously (urinary total T3, nipple contact, time in spatial proximity to mother, and independent foraging), changed suddenly in directions opposite of our expectation (increasing body contact time with the mother), or were significant only in subjects belonging to the younger age cohort (riding).

The fivefold increase in cortisol levels in our study is an unusually strong physiological response. For comparison, captive bonobos exposed to an experimental stress test exhibited a twofold increase in cortisol levels (Verspeek et al., 2021). A similar cortisol response occurred in bonobos in response to a group member giving birth, but in this case, the individual’s cortisol levels returned to previous values within 1 day (Behringer et al., 2009). In wild chimpanzees, urinary cortisol levels were found to increase by a factor of 1.5 when subjects encounter a neighboring group, an event that exposes all group members to potentially lethal aggression (Samuni et al., 2019). Changes in cortisol that exceeded the magnitude of the changes observed in our study occurred in a population of wild chimpanzees who experienced a tenfold cortisol increase during a respiratory disease, which killed a number of group members (Behringer et al., 2020). The intensity of a stress response is generally determined by the severity, controllability, and predictability of the stressor (Seiler et al., 2020); TTS is novel, severe, uncontrollable, and relatively unpredictable for the older offspring, all characteristics that likely contributed to the comparably high cortisol response that we observed in our study.

In addition to the age-independent, sudden, and substantial physiological response that we observed, a post-hoc analysis revealed that cortisol levels remained elevated for 7 months after sibling birth. Anecdotal reports indicate that, in wild chimpanzees, it may take up to 1 year until the older offspring adapts behaviorally to the presence of a younger sibling (Clark, 1977). While the physiological effects of sibling birth in human children are still unknown, behavioral data suggest that it may take up to 8 months until the older sibling adapts to the novel situation (Oh et al., 2017; Stewart et al., 1987). This indicates that humans, bonobos, and chimpanzees respond similarly to the challenge deriving from the arrival of a sibling.

The sudden decline of cortisol and neopterin levels to pre-sibling birth levels after 7 and 5 months, respectively, was unexpected. It is important to note that in the model with only one sudden change the cortisol levels needed many months to decline. While this result requires explanation, it is important to differentiate what our data can show and what remains to be explored in future studies. Regarding cortisol levels, our results do show that for a period of about 7 months none of the older siblings had low or average cortisol levels, but all had values within a narrow range of extremely high levels until they returned to their typical wide distribution. However, our data resolution does not allow the exact tracking of individual cortisol trajectories and it remains unclear at which time and speed different individuals return to ‘normal’ levels following the 7-month period. This aspect was even more pronounced in the case of neopterin levels. After the 5-month period of almost exclusively low neopterin levels, some individuals returned to previous levels but others remained low. Therefore, the time at which individuals return to ‘normal’ level, and the factors determining this shift remain to be investigated in future studies aiming at higher sampling rates per individual.

Cortisol levels are known to increase in response to psychological and social stressors, like predation risk or social instability, as well as energetic and physiological events (McEwen and Karatsoreos, 2020). Our study indicates that the sudden and persistent increase in cortisol levels in the older sibling was not related to energetic stress. Neither urinary total T3 levels, nor nipple contact, nor time spent foraging independently from the mother showed a sudden change at the onset of TTS. Similarly, if the cortisol increase at sibling birth would have been triggered by energetic challenges, the intensity of the cortisol level change should decline with the age of the older offspring as nutritional dependency on the mother decreases with age. In our study, the age of the older offspring at sibling birth ranged from 2.3 to 8.6 years, and preliminary analyses of stable isotopes in fecal samples collected from the same population suggest that nutritional weaning terminates at the age of 4.5 years (Oelze et al., 2020). However, the age of the older sibling at sibling birth had no effect on the strength of the cortisol response and the behavioral changes (body contact, nipple contact, riding, and independent foraging) did not follow the sudden shift in cortisol levels at the time of sibling birth.

In conjunction, our results indicate that the sudden increase in cortisol levels is independent from nutritional weaning effects and resembles behavioral responses of human children to the birth of a sibling (Dunn and Kendrick, 1980; Stewart et al., 1987). In human children, changes at sibling birth can be age-dependent. In response to sibling birth, scores for, for example, clinging and other gestures of reassurance were negatively correlated with the age of the older sibling (Dunn et al., 1981; Nadelman and Begun, 1982; Volling, 2012). Thus, in children, age seems to affect the behavioral response toward, or the perception of, the arrival of a sibling. Based on the results of our study, a sibling birth event is perceived similarly and independently of age. Hence, within the scope of our behavioral metrics, cortisol patterns did not match changes in single or cumulative behavioral changes around or after sibling birth.

Sibling birth is likely to cause multiple changes in the relationship between the mother and the older offspring, and only a few of them were considered in our study. For example, cortisol levels increase in response to positive arousal in children (Flinn et al., 2011), and while the newborn attracts the full attention of the mother it may also attract the older sibling’s interest. Accordingly, it is not possible to exclude that the response of older siblings was influenced by affiliative intentions. Mothers may not always tolerate interactions between siblings and might prevent the older one from initiating interactions, which can also result in frustration and a concomitant increase in cortisol (Gunnar et al., 2010; Stroud et al., 2000). At the time of sibling birth, the social environment of the older offspring is likely to change. For example, during the first weeks after birth, female bonobos tend to avoid large parties and forage alone or associate with a few other females (Douglas, 2014). This may lead to reduced rates of interactions with similar aged immatures and increased demand for social interactions with the mother who may not always be responsive to the needs of the older offspring. Another source affecting cortisol levels is aggression from group members. In bonobos, aggression against infants is rare but juveniles of both sexes can be exposed to physical aggression from adult males. Rates of aggression were found to increase with age of the immature target and were particularly high at times when mothers of targets had given birth (Hohmann et al., 2019; ). Thus, when females give birth, the older offspring is likely to be exposed to multiple challenges that may affect allostatic load and require the development of coping mechanisms, an achievement that requires time.

Although body contact between the older offspring and the mother decreased with age, it also suddenly increased for a short period after sibling birth. This response is not unknown: during TTS, juvenile marmosets increase proximity to parents (Achenbach and Snowdon, 1998), infant rhesus macaques intensify their effort to maintain contact with their mothers (Mandalaywala et al., 2014), and human children exhibit increased rates of clinging behavior (Volling et al., 2017). In our study, we did not find consistent effects of TTS on proximity within 5 m. If such changes in proximity and body contact reflect reduced maternal attention, the older offspring may aim to regain more attention from their mothers or other caregivers (Baydar et al., 1997). Reduced maternal attention could contribute to the increase in cortisol levels that we found, but it is still unclear why this change persists for several months. Moreover, the most consistent effect of TTS on offspring behavior in humans was a decrease in affection and responsiveness to the mother (Volling, 2012), which seems to contradict this interpretation. Alternatively, young female primates are known to show a high interest in new babies (Maestripieri and Pelka, 2002) and the increase in body contact may reflect the interest of the older offspring in the younger sibling.

The sudden increase in cortisol and the abrupt decline in neopterin levels in our study emphasize the homeostatic challenges affecting the older offspring during TTS. It is possible that the increase in cortisol levels negatively affected cell-mediated immunity. In other mammals, stress responses to weaning had a negative effect on immunity (Kick et al., 2012; Kim et al., 2011), and stressful events were associated with changes in immune function in humans (Herbert and Cohen, 1993). While short-term increases in cortisol levels enhance immune functions in humans, long-lasting elevations of cortisol levels – such as those found in our study – dysregulate immune responses (Dhabhar, 2014). In our study, urinary cortisol and neopterin levels recovered several months after sibling birth, indicating that individuals can cope with TTS to some degree, for example, by becoming habituated to the new conditions or by recruiting social support from other group members.

Persistent early-life cortisol elevations can affect an individual’s ontogeny, with long-lasting consequences for its fitness, affecting its growth trajectory, metabolism, social behavior, immunity, stress reactivity, reproduction, and life history strategies (Berghänel et al., 2017; Maestripieri, 2018; Seiler et al., 2020). In view of our results, such effects may contribute to the observed negative effects of sibling birth on the fitness of the older offspring in nonhuman primates (Thompson et al., 2016; Tung et al., 2016; Zipple et al., 2019). However, the impact of sibling birth is not necessarily that strong. For example, the presence of a sibling did not affect the hypothalamic-pituitary-adrenal axis later in life in baboons, but other early-life adversities had lasting consequences (Rosenbaum et al., 2020). The physiological effects caused by a normative stressor that affects most individuals, such as the birth of a sibling, should be under negative selection and would therefore be considered to be a nonadaptive trait. Alternatively, it has been suggested that early-life events of ‘tolerable stress’ (McEwen and Karatsoreos, 2020) may serve to prime subjects to develop stress resistance later in life. Moreover, TTS may accelerate acquisition of motor, social, and cognitive skills (Azmitia and Hesser, 1993; Maestripieri, 2018; Song et al., 2016). Siblings are not only rivals but also important social partners, and the presence of an older sibling can buffer behavioral and physiological changes in response to stressful events like TTS (Hrdy, 2011). Having an older sibling may enhance the development and survival of the younger sibling that contributes to the inclusive fitness of both the older sibling and the mother (Salmon and Hehman, 2015; Stanton et al., 2017). Returning to our study, future studies should integrate behavior and physiological measures to estimate the impact of TTS for the older sibling and explore the long-term effects of increasing cortisol levels. The combination of physiological and behavioral measures could help to disentangle why immature bonobos show such an intense cortisol response. This would allow testing the hypotheses that the novel mother–infant constellation is an expression of positive valence arousal or a normative change of maturation.

To our knowledge, our study on wild bonobos is the first to investigate the physiological response during TTS and, along with other studies on nonhuman primates. In many human cultures, inter-birth intervals are shorter and children are weaned at a younger age than in wild apes (Humphrey, 2010; Robson et al., 2006), despite humans having slower development and longer ontogeny. However, parental effort varies tremendously across human cultures and is often supplemented by intense allomaternal care (Hrdy and Burkart, 2020). Thus, it is possible that human children do not necessarily experience such extreme and long-lasting cortisol elevation. In some families in Western societies and traditional societies, allomaternal caregivers provide nutritional, physical, and mental support to older children (Baydar et al., 1997; Kramer and Veile, 2018), which may buffer physiological responses. However, when such social buffering systems are absent or weakly developed, as in some Western societies, older children may experience the birth of a sibling as a particularly stressful time. Studies in humans are generally biased toward middle-class families in Western industrialized countries (Fouts and Bader, 2016; Volling, 2012), and our study expands research on TTS to a nonhuman primate.

The results of our study showed that bonobos, one of humans’ closest living relatives, had high cortisol levels during TTS. Together with anecdotal evidence from chimpanzees (Clark, 1977), the information obtained in our study may shed light on the evolutionary history of the behavioral and physiological changes associated with TTS. More detailed comparisons are required to identify the emergence of behavioral and physiological traits related to TTS, their interactions, and fitness consequences. Yet, the results obtained from wild bonobos render support to the long-standing but untested and recently questioned assumption that the birth of a sibling is a notable event for the older offspring (Volling, 2012; Volling et al., 2017). It highlights the ubiquity of this pattern across individuals and age classes, and indicates that emergence of this developmental period may not be a derived trait. Interpretation of data of nonhuman primates in an evolutionary context can lead to unjustified generalization (Sayers et al., 2012), and it is important to note that behavioral responses to TTS in human children are highly variable and individual- and age-dependent, ranging from aggression, emotional blackmailing, and psychological disturbances, to positive attitudes toward the new family constellation (Volling, 2012; Volling et al., 2017). This raises questions regarding the coping strategies and how they are (a) influenced by the socioecological conditions including actual parent–offspring and other caretaker relationships, (b) effective in modulating and buffering the shown physiological stress response, and (c) their phylogenetic history (Hrdy, 2011; Lonsdorf et al., 2018).

Source data for statistics and figures in the paper is permanently stored at GRO (https://doi.org/10.25625/O1OD2I).

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Author details

1. Verena Behringer

   1. Endocrinology Laboratory, German Primate Center, Leibniz Institute for Primate Research, Göttingen, Germany
   2. Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

   Contribution

   Conceptualization, Resources, Data curation, Funding acquisition, Validation, Investigation, Methodology, Writing – original draft, Writing – review and editing

   Contributed equally with

   Andreas Berghänel

   For correspondence

   VBehringer@dpz.eu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-6338-7298

2. Andreas Berghänel

   Domestication Lab, Konrad Lorenz Institute of Ethology, Department of Interdisciplinary Life Sciences, University of Veterinary Medicine Vienna, Vienna, Austria

   Contribution

   Conceptualization, Resources, Data curation, Software, Formal analysis, Visualization, Methodology, Writing – original draft, Writing – review and editing

   Contributed equally with

   Verena Behringer

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3317-3392

3. Tobias Deschner

   Comparative BioCognition, Institute of Cognitive Science, University of Osnabrück, Osnabrück, Germany

   Contribution

   Resources, Supervision, Funding acquisition, Validation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

4. Sean M Lee

   Center for the Advanced Study of Human Paleobiology, Department of Anthropology, George Washington University, Washington, United States

   Contribution

   Conceptualization, Data curation, Funding acquisition, Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

5. Barbara Fruth

   1. Max Planck Institute of Animal Behavior, Konstanz, Germany
   2. Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, Belgium

   Contribution

   Resources, Data curation, Supervision, Funding acquisition, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

6. Gottfried Hohmann

   1. Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
   2. Max Planck Institute of Animal Behavior, Konstanz, Germany

   Contribution

   Conceptualization, Resources, Data curation, Supervision, Investigation, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

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