Demographic and hormonal evidence for menopause in wild chimpanzees

Abstract

Among mammals, post-reproductive life spans are currently documented only in humans and a few species of toothed whales. Here we show that a post-reproductive life span exists among wild chimpanzees in the Ngogo community of Kibale National Park, Uganda. Post-reproductive representation was 0.195, indicating that a female who reached adulthood could expect to live about one-fifth of her adult life in a post-reproductive state, around half as long as human hunter-gatherers. Post-reproductive females exhibited hormonal signatures of menopause, including sharply increasing gonadotropins after age 50. We discuss whether post-reproductive life spans in wild chimpanzees occur only rarely, as a short-term response to favorable ecological conditions, or instead are an evolved species-typical trait as well as the implications of these alternatives for our understanding of the evolution of post-reproductive life spans.

Fig. 1.. Ngogo female fertility and survivorship.

Female age-specific fertility rates, ASFR, were calculated for each 5-year age group by dividing the total number of births by the years of life observed in females of each age group. (A) Ngogo ASFR (±SE, in gray) and a composite sample of six other wild chimpanzee communities reported by Emery Thompson et al. (8). (B) Plot of the probability of female survival to each age ($l_x$) [updated from Wood et al. (65)] and a composite sample of five other wild chimpanzee communities (8).

Fig. 2.. Ngogo post-reproductive females (1995–2016).

Their age at entry to the study is shown by yellow points, and age when giving birth (observed or inferred) is shown by red points. Age when exiting the study is represented by blue points if they were alive at the end of the study period, or by blue crosses if they died during the study period. Numbers plotted next to chimpanzee IDs describe the urine samples collected for hormonal analyses for that individual. Group 1 contributed samples to the analysis of FSH, LH, and ovarian steroid hormones; group 2, only FSH; and group 3, only ovarian steroid hormones. No urine samples were collected from individual BES.

Fig. 3.. Urinary hormone concentrations in females of different reproductive states.

(A) LH in samples collected in 2016–2018, (B) FSH 2016–2018, (C) FSH 2006–2007, (D) estradiol 2016–2018, (E) estrone 2016–2018, and (F) pregnanediol 2016–2018. Boxplots are based on all urine samples rather than averages per female. Black dots indicate data points above the third quartile by >1.5× the interquartile range. Median values by reproductive category are provided in table S2. For legibility, a few extreme measures have been excluded from (D) to (F), but full data ranges are displayed in fig. S3. corr. SG, corrected specific gravity.

Fig. 4.. Urinary concentrations of gonadotropins and ovarian hormones in females by age.

(A) LH in 223 samples from 58 individuals collected 2016–2018, (B) FSH in 215 samples from 57 individuals collected 2016–2018, (C) FSH in 143 samples from 15 individuals collected 2006–2007, (D) estradiol in 160 samples from 21 individuals, (E) estrone in 162 samples in 21 individuals, and (F) pregnanediol in 162 samples from 21 individuals. Points represent average levels aggregated by individual female and reproductive status at the time of sample collection. Black points in (A) to (F) represent post-reproductive females, blue points in (A) to (C) represent reproductive females, and red squares in (D) to (F) represent nonbreastfeeding cycling females. The gray age curves in (A) to (F) represent mean expected values ( ±1 SE) from fit models 10 to 15, respectively (tables S4 to S7). See fig. S3 for sample-level plotting of gonadotropin concentrations and fig. S4 for age trends in ovarian hormone concentrations in all females, including those who were breastfeeding.

Fig. 5.. Standardized age trends in female urinary hormones in Ngogo chimpanzees and human females.

(A) FSH, (B) LH, (C) estrogens, and (D) progestins, as observed at Ngogo and in studies of human females by Ferrell et al. (18, 19). The expected values for Ngogo females in all panels were generated from our study’s data and the fit models 10, 11, 14, and 15 (tables S4 and S6). The analytes from Ngogo females shown in (C) and (D) are estrone and pregnanediol, respectively. Median age trends for human females in urinary FSH, LH, estrone glucuronide (a conjugated metabolite of estrone), and pregnanediol glucuronide (a conjugated metabolite of progesterone) are derived from (18, 19).