Evidence for adolescent length growth spurts in bonobos and other primates highlights the importance of scaling laws
- Domestication Lab, Konrad Lorenz Institute of Ethology, Department of Interdisciplinary Life Sciences, University of Veterinary Medicine Vienna, Austria
- Behavioral Ecology and Ecophysiology, Department of Biology, University of Antwerp, Belgium
- Centre for Research and Conservation, Royal Zoological Society of Antwerp, Belgium
- SALTO Agro- and Biotechnology, Odisee University of Applied Sciences, Belgium
- Max Planck Institute for Evolutionary Anthropology, Germany
- Max-Planck-Institute of Animal Behaviour, Germany
- Comparative BioCognition, Institute of Cognitive Science, University of Osnabrück, Germany
- Endocrinology Laboratory, German Primate Center, Leibniz Institute for Primate Research, Germany
- Leibniz ScienceCampus Primate Cognition, German Primate Center, Leibniz Institute for Primate Research, Germany
Figures
Figure 1 with 1 supplement
Cubic isometric relationship between volume (~weight) and length growth, and likelihood to detect an existing growth spurt (GS) in linear length (schematic).
(A–E) Top/bottom: Absolute size and growth rate (=1st derivation of size). From left to right: Increasingly fast acceleration of volume (~weight) growth and the aligned length growth, from (A) no …
Figure 1—figure supplement 1
The figure shows how a change from a constant to a quadratically accelerating volume growth rate at a certain body size (identical levels of acceleration) results in different levels of acceleration in linear length growth rate depending on the age (in fact, body size) at which this change occurs, from left (change right after birth at small body size, only slight acceleration in linear length growth rate) to right (change at late age and larger body size, strong acceleration in length growth rate).
Figure 2 with 2 supplements
Growth trajectories in body weight and forearm length, and the importance of comparing them at the relevant dimension.
Fitted values and 95% CIs from Generalized Additive Mixed Models (GAMMs) are shown, implementing variability in trajectories across individuals and zoos. (A, B) Investigating both weight and length …
Figure 2—figure supplement 1
Our results on body weight (left) and forearm length (right) remained the same if (A, B) only zoo-born individuals were considered (which also allowed to additionally control for kinship [dam and sire] and maternal age at birth) or if (C, D) only those individuals were considered for which data on body weight, forearm length, dehydroepiandrosterone (DHEA), and testosterone were available.
Blue = males; red = females. 95% confidence intervals are plotted.
Figure 2—figure supplement 2
Validation of the scaling relationship between forearm length and body weight during growth in our study.
Since weight and length were not measured pairwise, we used the fitted values from the respective Generalized Additive Mixed Models (GAMMs). The power-exponent of the relationship is calculated as …
Figure 3 with 3 supplements
Physiological changes during ontogeny: markers of muscle growth (creatinine), adrenarche (dehydroepiandrosterone, DHEA), and adolescence (testosterone and insulin-like growth factor-binding protein 3 [IGFBP-3]).
Fitted values and 95% CIs from Generalized Additive Mixed Models (GAMMs) are shown, which implement variability in trajectories across individuals and zoos. (A) Males showed a pronounced growth …
Figure 3—figure supplement 1
Our results on dehydroepiandrosterone (DHEA) (left) and testosterone (right) remained the same if (A, B) only zoo-born individuals were considered (which also allowed to additionally control for kinship [dam and sire] and maternal age at birth) or if (C, D) only those individuals were considered for which data on body weight, forearm length, DHEA, and testosterone were available.
Blue = males, red = females. 95% confidence intervals are plotted.
Figure 3—figure supplement 2
Our results on creatinine (A) and insulin-like growth factor-binding protein 3 (IGFBP-3) (B) remained the same if only zoo-born individuals were considered (which also allowed to additionally control for kinship [dam and sire] and maternal age at birth).
Blue = males, red = females. 95% confidence intervals are plotted.
Figure 3—figure supplement 3
In our raw data, females and males showed a fast increase in testosterone, as also previously shown for bonobos (Behringer et al., 2014), with females (red) reaching maximal levels around the age of 5, and males (blue) around the age of 9 years.
However, this fast change was not appropriately modelled by our Generalized Additive Mixed Models (GAMMs) if the ‘automatic’ estimation of the smoothing parameters was used, leading to strong …
Figure 4
Direct comparison of age trajectories in growth patterns and physiological parameters until the age of 20 years.
Tables
Table 1
Statistical results of Generalized Additive Mixed Models (GAMMs) on growth and physiology.
Blue: Interaction term results from a separate model (see methods section). Red: Special model structure for insulin-like growth factor-binding protein 3 (IGFBP-3) models (random intercept per …
| Factor variables | Reference Category | Body weight (kg) | Body weight (√kg*) | Lower arm length (cm) | Lower arm length (cm2.5) | ||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Est. | SE | t | p | Est. | SE | t | p | Est. | SE | t | p | Est. | SE | t | p | ||
| (Intercept) | 22.4 | 0.10 | 222 | <0.001 | 3.17 | 0.01 | 581 | <0.001 | 25.2 | 0.06 | 443 | <0.001 | 3504 | 19.1 | 183 | <0.001 | |
| Males | Females | 4.10 | 0.13 | 30.8 | <0.001 | 0.20 | 0.01 | 26.9 | <0.001 | 1.26 | 0.19 | 6.77 | <0.001 | 567 | 63.0 | 9.00 | <0.001 |
| Smooth term variables | edf | Ref.df | F | p | edf | Ref.df | F | p | edf | Ref.df | F | p | edf | Ref.df | F | p | |
| Age trajectories | |||||||||||||||||
| Females | 9.12 | 9.39 | 82.3 | <0.001 | 9.00 | 9.19 | 52.1 | <0.001 | 8.32 | 8.71 | 120 | <0.001 | 8.44 | 8.78 | 54.7 | <0.001 | |
| Males | 9.53 | 9.67 | 116 | <0.001 | 9.42 | 9.52 | 52.4 | <0.001 | 7.75 | 8.37 | 115 | <0.001 | 8.06 | 8.56 | 43.2 | <0.001 | |
| Males | Females | 8.53 | 8.84 | 6.36 | <0.001 | 9.04 | 9.26 | 7.42 | <0.001 | 7.05 | 7.77 | 5.34 | <0.001 | 6.71 | 7.48 | 4.49 | <0.001 |
| Random smooths | |||||||||||||||||
| Sampling date per zoo | 103 | 175 | 2.85 | <0.001 | 97.6 | 175 | 2.53 | <0.001 | 10.7 | 44.0 | 0.49 | <0.001 | 7.05 | 37.0 | 0.47 | <0.001 | |
| Age trajectory per individual | 600 | 1544 | 14.4 | <0.001 | 577 | 1545 | 10.5 | <0.001 | 148 | 336 | 14.6 | <0.001 | 151 | 336 | 20.5 | <0.001 | |
| Age trajectory per rearing§ | 2.12 | 53.0 | 0.12 | <0.001 | 27.6 | 53.0 | 2.29 | <0.001 | 0.00 | 48.0 | 0.00 | 0.116 | 0.00 | 48.0 | 0.00 | 0.022 | |
| Female age trajectory per zoo | 32.1 | 175 | 0.29 | <0.001 | 21.9 | 175 | 0.18 | <0.001 | 0.01 | 23.0 | 0.00 | 0.070 | 0.02 | 23.0 | 0.00 | 0.055 | |
| Male age trajectory per zoo | 35.1 | 168 | 0.35 | <0.001 | 61.0 | 168 | 0.91 | <0.001 | 6.69 | 26.0 | 0.88 | <0.001 | 10.9 | 26.0 | 1.45 | <0.001 | |
| R2adj (deviance explained) | 0.995 (99.5%) | 0.997 (99.7%) | 0.988 (99.1%) | 0.986 (99.0%) | |||||||||||||
| N (p-value) | 8355 (<0.001) | 8355 (<0.001) | 641 (<0.001) | 641 (<0.001) | |||||||||||||
| Factor variables | Reference Category | Ln(Creatinine) | Ln(DHEA) | Ln(Testosterone) | Ln(IGFBP-3) | ||||||||||||
| Est. | SE | t | p | Est. | SE | t | p | Est. | SE | t | p | Est. | SE | t | p | ||
| (Intercept) | –0.02 | 0.07 | –0.96 | 0.337 | 2.99 | 0.04 | 84.2 | <0.001 | 0.43 | 0.05 | 9.15 | <0.001 | 2.06 | 0.08 | 25.6 | <0.001 | |
| Males | Females | 0.14 | 0.04 | 3.97 | <0.001 | –0.05 | 0.04 | –1.09 | 0.276 | 0.97 | 0.10 | 9.34 | <0.001 | 0.04 | 0.12 | 0.34 | 0.732 |
| Smooth term variables | edf | Ref.df | F | p | edf | Ref.df | F | p | edf | Ref.df | F | p | edf | Ref.df | F | p | |
| Daytime | 1.00 | 1.00 | 8.98 | 0.003 | 1.77 | 1.94 | 2.04 | 0.116 | 1.00 | 1.00 | 2.46 | 0.118 | 1.00 | 1.00 | 2.94 | 0.089 | |
| Age trajectories | |||||||||||||||||
| Females | 2.64 | 2.99 | 6.17 | <0.001 | 4.69 | 5.44 | 6.16 | <0.001 | 8.48 | 8.85 | 19.2 | <0.001 | 5.04 | 5.65 | 5.39 | <0.001 | |
| Males | 4.45 | 4.77 | 20.4 | <0.001 | 2.97 | 3.38 | 9.77 | <0.001 | 8.33 | 8.81 | 30.6 | <0.001 | 3.98 | 4.66 | 5.53 | <0.001 | |
| Males | Females | 4.41 | 4.73 | 3.73 | 0.016 | 1.00 | 1.00 | 0.24 | 0.622 | 8.05 | 8.63 | 8.24 | <0.001 | 3.24 | 3.62 | 3.27 | 0.010 |
| Random smooths | |||||||||||||||||
| Sampling date per zoo | 24.7 | 56.0 | 2.61 | <0.001 | 33.0 | 55.0 | 10.5 | <0.001 | 25.4 | 58.0 | 3.46 | <0.001 | - | - | - | - | |
| Age trajectory per individual | 42.0 | 385 | 0.18 | <0.001 | 14.88 | 392 | 0.05 | 0.031 | 66.4 | 397 | 0.38 | <0.001 | 0.00 | 103 | 0.00 | 0.819 | |
| Age trajectory per rearing§ | 0.00 | 28.0 | 0.00 | 0.191 | 0.00 | 28.0 | 0.00 | 0.651 | 1.79 | 28.0 | 0.24 | <0.001 | - | - | - | - | |
| Female age trajectory per zoo | 7.55 | 34.0 | 0.57 | <0.001 | 2.77 | 60.0 | 0.06 | 0.042 | 6.66 | 66.0 | 0.26 | <0.001 | 0.00 | 35.0 | 0.00 | 0.554 | |
| Male age trajectory per zoo | 0.00 | 33.0 | 0.00 | 0.087 | 0.58 | 60.0 | 0.01 | 0.13 | 2.46 | 63.0 | 0.05 | 0.006 | - | - | - | - | |
| R2adj (deviance explained) | 0.424 (48.7%) | 0.488 (52.7%) | 0.712 (75.5%) | 0.235 (28.7%) | |||||||||||||
| N (p-value) | 766 (<0.001) | 782 (0.001) | 802 (<0.001) | 163 (0.003) | |||||||||||||
Table 2
Evidence of length growth spurts (GSs) from published literature using linear length growth.
Measures of linear length growth are taken of: Body length or height = B, Crown-rump/Shoulder-rump/Anterior trunk length = CR/SR/AT, Lower/Upper/Full arm length = LA/UA/A, Thigh/Tibia/Leg length = …
| Species (w/z) | Changes in length growth rate | ||||||
|---|---|---|---|---|---|---|---|
| Acceleration | Constant (plateau) | Slowdown in deceleration | No slowdown in deceleration | Aligned with weight-GS | Comments | Publication | |
| Macaca assamensis (w) | m + f (LA) | Not available | Acceleration if scale corrected | Anzà et al., 2022; Berghänel et al., 2015 | |||
| Macaca fuscata (z) | m + f (B), m (AT, UA) | m (TH, L) | m (LA), f (LA) | f (UA) | Yes (little earlier) | Hamada, 1994; Hamada et al., 1999; Hamada and Yamamoto, 2010 | |
| Macaca nemestrina (z) | m + f (AT, CR, A, LA, L) | Yes | Nishikawa, 1985; Tarrant, 1975 | ||||
| Macaca arctoides (z) | m (CR) | Yes | Few individuals | Faucheux et al., 1978 | |||
| Macaca mulatta (z) | (B, TI)1 | m + f (CR) | Yes (little earlier) | 1Unknown sex, few individuals | Tanner et al., 19901; van Wagenen and Catchpole, 1956 | ||
| Macaca ochreata (w) | m + f (CR) | Yes | Schillaci and Stallmann, 2005 | ||||
| Theropithecus gelada (w) | m + f (SR) | Not available | Lu et al., 2016 | ||||
| Papio anubis (z) | m (CRL) | m + f (A) | m (TH), f (CRL, TH) | Yes (little earlier) | Leigh, 2009 | ||
| Papio hamadryas (z) | m (CR) | f (CR) | Yes (m) | Coarse data | Crawford et al., 1997 | ||
| Mandrillus sphinx (z) | m + f (CR) | Yes | Setchell et al., 2001 | ||||
| Pan troglodytes (z) | m + f (B) | Yes | Hamada and Udono, 2002 | ||||
| Pongo pygmaeus (z) | m + f (B, LA) | Yes | Two individuals | Vančatová et al., 1999 | |||
| Gorilla beringei beringei (w) | m (B) | m (UA), f (B, UA) | Not available | Galbany et al., 2017 | |||
Table 3
Sample sizes for measurements of growth (body weight, forearm length, and creatinine) as well as for physiological markers (dehydroepiandrosterone [DHEA], testosterone, and insulin-like growth factor-binding protein 3 [IGFBP-3]).
| Parameter | Number of males/females | Samples per ID (mean ± SD/range/median) | Number of zoos | ||
|---|---|---|---|---|---|
| All | Males | Females | |||
| Body weight | 119/139 | 32.4 ± 67.6/1–659/9 | 40.4 ± 90.3/1–659/9 | 25.5 ± 37.8/1–195/9 | 19 |
| Arm length | 56/79 | 4.8 ± 3.0/1–11/4 | 4.8 ± 2.9/1–11/5 | 4.8 ± 3.0/1–11/4 | 10 |
| Creatinine | 65/89 | 4.9 ± 3.7/1–19/4 | 5.3 ± 4.1/1–19/4 | 4.7 ± 3.5/1–16/4 | 13 |
| DHEA | 68/87 | 5.1 ± 3.7/1–19/4 | 5.1 ± 4.0/1–19/4 | 5.0 ± 3.5/1–16/4 | 14 |
| Testosterone | 68/89 | 5.1 ± 3.8/1–19/4 | 5.3 ± 4.1/1–19/4 | 5.0 ± 3.5/1–16/4 | 15 |
| IGFBP-3 | 45/61 | 1.5 ± 1.4/1–8/1 | 1.7 ± 1.6/1–7/1 | 1.4 ± 1.2/1–8/1 | 12 |
Appendix 1—table 1
Evidence of (adolescent) length growth spurts (GSs) from published literature using linear length growth.
Same table as Table 2 in main text, but additionally with literature on markers of adolescence. Changes in length growth rate (left) – Measures of linear length growth are taken of: Body length or …
| Species (w/z) | Changes in length growth rate | Markers of adolescence | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Acceleration | Constant (plateau) | Slowdown in deceleration | No slowdown in deceleration | Aligned with weight-GS | Comments | Publication | Males | Females | Publication | |
| Macaca assamensis (w) | m + f (LA) | Not available | Acceleration if scale corrected | Anzà et al., 2022; Berghänel et al., 2015 | / | / | / | |||
| Macaca fuscata (z) | m + f (B), m (AT, UA) | m (TH, L) | m (LA), f (LA) | f (UA) | Yes (little earlier) | Hamada, 1994; Hamada et al., 1999; Hamada and Yamamoto, 2010 | TS (l) | M (a) | Hamada et al., 1999 | |
| Macaca nemestrina (z) | m + f (AT, CR, A, LA, L) | Yes | Nishikawa, 1985; Tarrant, 1975 | / | S (p) | Muehlenbein et al., 2005; Hadidian and Bernstein, 1979 | ||||
| Macaca arctoides (z) | m (CR) | Yes | Few individuals | Faucheux et al., 1978 | TS (a) | / | Nieuwenhuijsen et al., 1987 | |||
| Macaca mulatta (z) | (B, TI)1 | m + f (CR) | Yes (little earlier) | 1Unknown sex, few individuals | Tanner et al., 1990; van Wagenen and Catchpole, 1956 | / | S (a), M (l) | Tanner et al., 1990 | ||
| Macaca ochreata (w) | m + f (CR) | Yes | Schillaci and Stallmann, 2005 | / | / | / | ||||
| Theropithecus gelada (w) | m + f (SR) | Not available | Lu et al., 2016 | TL (l) | Pigmentation of bare area (a) | Beehner et al., 2009; Matthews, 1956 | ||||
| Papio anubis (z) | m (CRL) | m + f (A) | m (TH), f (CRL, TH) | Yes (little earlier) | Leigh, 2009 | TS, TL, IGF1, IGFBP3 (all a) | C (a) | Bernstein et al., 2013; Bernstein et al., 2008; Mueller, 2005; Owens, 1976 | ||
| Papio hamadryas (z) | m (CR) | f (CR) | Yes (m) | Coarse data | Crawford et al., 1997 | TS, TL, IGF1, IGFBP3 (all a) | C (a) | Bernstein et al., 2013; Mueller, 2005 | ||
| Mandrillus sphinx (z) | m + f (CR) | Yes | Setchell et al., 2001 | TS (a), TL (l) | S (a) | Setchell and Dixson, 2002; Wickings and Dixson, 1992 | ||||
| Pan troglodytes (z) | m + f (B) | Yes | Hamada and Udono, 2002 | TS and TL (a) | M (l) | Anestis, 2006; Coe et al., 1979; Kraemer et al., 1982 | ||||
| Pongo pygmaeus (z) | m + f (B, LA) | Yes | Two individuals | Vančatová et al., 1999 | Highly variable | M (occurs at 5–12 yrs) | Nacey Maggioncalda and Sapolsky, 2002; Markham, 1990 | |||
| Gorilla beringei beringei (w) | m (B) | m (UA), f (B, UA) | Not available | Galbany et al., 2017 | / | / | / | |||
