Sex Differences in Age-Related Decline of Urinary Insulin-Like Growth Factor-Binding Protein-3 Levels in Adult Bonobos and Chimpanzees

Abstract

There is increasing interest in the characterization of normative senescence in humans. To assess to what extent aging patterns in humans are unique, comparative data from closely related species, such as non-human primates, can be very useful. Here, we use data from bonobos and chimpanzees, two closely related species that share a common ancestor with humans, to explore physiological markers that are indicative of aging processes. Many studies on aging in humans focus on the somatotropic axis, consisting of growth hormone (GH), insulin-like growth factors (IGFs), and IGF binding proteins (IGFBPs). In humans, IGFBP-3 levels decline steadily with increasing age. We used urinary IGFBP-3 levels as an alternative endocrine marker for IGF-I to identify the temporal pattern known to be related with age-related changes in cell proliferation, growth, and apoptosis. We measured urinary IGFBP-3 levels in samples from 71 bonobos and 102 chimpanzees. Focusing on samples from individuals aged 10 years or older, we found that urinary IGFBP-3 levels decline in both ape species with increasing age. However, in both species, females start with higher urinary IGFBP-3 levels than males, experience a steeper decline with increasing age, and converge with male levels around the age of 30-35 years. Our measurements of urinary IGFBP-3 levels indicate that bonobos and chimpanzees mirror human patterns of age-related decline in IGFBP-3 in older individuals (<10 years) of both sexes. Moreover, such as humans, both ape species show sex-specific differences in IGFBP-3 levels with females having higher levels than males, a result that correlates with sex differences in life expectancy. Using changes in urinary IGFBP-3 levels as a proxy for changes in GH and IGF-I levels that mark age-related changes in cell proliferation, this approach provides an opportunity to investigate trade-offs in life-history strategies in cross-sectional and in longitudinal studies, both in captivity and in the wild.

Keywords: IGFBP-3; aging pattern; ape species; pan paniscus; pan troglodytes; primate; urinary marker.

Figure 1

Measures of urinary IGFBP-3 levels corrected for specific gravity (corr. SG) from bonobos (upper plot) and chimpanzees (lower plot) in relation to chronologic age. Sample sizes: N_bonobos = 71 (31 males, 40 females), N_chimpanzees = 102 (33 males, 69 females).

Figure 2

Measures of urinary IGFBP-3 levels corrected for specific gravity (corr. SG) from female (upper plot) and male (lower plot) bonobos (open triangles) and chimpanzees (filled triangles) in relation to chronologic age. The y-axis is displayed on a log scale. Sample sizes: N_bonobos = 71 (31 males, 40 females), N_chimpanzees = 102 (33 males, 69 females).

Figure 3

Measures of urinary IGFBP-3 levels corrected for specific gravity (corr. SG) obtained from female (upper plot) and male (lower plot) bonobos and chimpanzees in relation to their chronologic age (year). Shaded areas represent bootstrapped 95% confidence intervals for expected urinary IGFBP-3 levels. The area of the circles corresponds to the number of individuals. The y-axis is displayed on a log scale. Sample sizes: N_bonobos = 71 (31 males, 40 females), N_chimpanzees = 102 (33 males, 69 females).