Five years later, with double the demographic data, naked mole-rat mortality rates continue to defy Gompertzian laws by not increasing with age

Abstract

The naked mole-rat (Heterocephalus glaber) is a mouse-sized rodent species, notable for its eusociality and long lifespan. Previously, we reported that demographic aging, i.e., the exponential increase of mortality hazard that accompanies advancing age in mammals and other organisms, does not occur in naked mole-rats (Ruby et al., 2018), a finding that has potential implications for human healthy aging. The demographic data supporting that conclusion had taken over three decades to accumulate, starting with the original rearing of H. glaber in captivity. This finding was controversial since many of the animals in that study were relatively young. In the 5 years following that study, we have doubled our quantity of demographic data. Here, we re-evaluated our prior conclusions in light of these new data and found them to be not only supported but indeed strengthened. We additionally provided insight into the social dynamics of captive H. glaber with data and analyses of body weight and colony size versus mortality. Finally, we provide a phylogenetically proximal comparator in the form of lifespan data from our Damaraland mole-rat (Fukomys damarensis) colony and demographic meta-analysis of those data along with published data from Ansell's mole-rat (Fukomys anselli). We found Fukomys mortality hazard to increase gradually with age, an observation with inferences on the evolution of exceptional lifespan among mole-rats and the ecological factors that may have accompanied that evolution.

Keywords: Demographic aging; social dynamics.

Fig. 1

The mortality hazard of naked mole-rats failed to increase with age. A Kaplan-Meier survival curve for naked mole-rats (green) after reaching reproductive maturity (T_sex; 6 months from birth; 183 days; red). Plotted as in Fig. 1A of Ruby et al. (2018), with a histogram of death and censorship (pink and purple, respectively) in the inset, up until 5306 days of age, at which point 174 animals remained in the population; and with censorship events after that indicated by vertical ticks (purple), the size of which is proportional to the number of animals censored at each day-of-life. B Mortality-hazard estimates (solid green) with 95% confidence intervals (dotted green) across the observed naked mole-rat lifespan. Estimates were calculated across time intervals of increasing size (demarked by grey lines) to compensate for decreasing accuracy per unit time as the population size decreased. The borders of the age bins (black), along with the number of deaths (pink) and total years of animal life observed (green) per bin, are indicated at the bottom.

Fig. 2

Exclusion of neither pre-2008 nor pre-2016 lifespan data through left-censorship modified the observed lifespan demographics of H. glaber. A The number of naked mole-rats observed (y-axis) at each age (x-axis) for four datasets: (i) the original data set presented in (Ruby et al., 2018) (pink); (ii) that data set left-censored on January 1, 2008, as presented in (Ruby et al., 2019) (yellow); (iii) the full data set compiled in 2021 for this manuscript (green); (iv) that data set left-censored on May 17, 2016 (navy), i.e., data collected after the compilation of data for (Ruby et al., 2018). B Kaplan–Meier survival curves starting at T_sex (183 days; red) for the four demographic data sets, as colored and described in panel A. C Mortality hazard estimates (y-axis) across each of the lifespan bins from panel B (indicated on the x-axis), for each of the four demographic data sets, as colored and described in panel A. Horizontal bars indicate hazard estimates, and vertical bars indicate 95% confidence intervals.

Fig. 3

Breeding and non-breeding male and female naked mole-rats exhibited non-increasing mortality hazard as a function of age. A Kaplan-Meier survival starting at T_sex (183 days; red) for each of four reproductive categories of naked mole-rats: male breeders (navy), female breeders, (red), male non-breeders (cyan), and female non-breeders (pink). B Mortality hazard estimates (y-axis) for the indicated lifespan bins (x-axis), calculated for non-breeding males (cyan) and females (pink). The numbers of observed death events per bin are indicated at the top of each bin. C Mortality hazard estimates (y-axis) for the indicated lifespan bins (x-axis), calculated for breeding males (navy) and females (red). The numbers of observed death events per bin are indicated at the top of each bin.

Fig. 4

Non-breeding naked mole-rat mortality hazard decreased with increasing body weight and colony size. A Individual body weight values (y-axis) plotted longitudinally versus age (x-axis) for breeding males (navy), non-breeding males (cyan), breeding females (red), and non-breeding females (pink). B Mean body-weights for each of the categories from panel A, for all weight measurements taken across each of the following age bins: 50–120 days, 120–200 days, 200–400 days, 400–700 days, 700–1000 days, 1000–1500 days, and 1500–2000 days; inclusive of the 1^st day and non-inclusive of the last day for each bin. Solid lines indicate mean body weights; dotted lines indicate standard deviations. C Top panel: body weight quartiles for male (left) and female (right) non-breeding animals, organized based on the last recorded weight measurement for each animal and only included if that measurement was taken at an older age than 500 days. Horizontal bars indicate the mean body weight for each quartile; vertical bars indicate standard deviations. Bottom panel: mortality hazard for each body weight quartile in the top panel, calculated for the year following weight measurement. See the “Methods” section for details. Horizontal bars indicate mortality hazard estimates; vertical bars indicate 95% confidence intervals. D Examples of colony-size versus mortality-hazard plots. For each indicated year (2019 on the left; 2015 on the right), and for each indicated non-breeding sex (males on the left; females on the right): animals were organized into quartiles based on the number same-sex, non-breeding animals in their colony. Top panels: the mean colony sizes for animals in each quartile; vertical bars indicate standard deviations. Bottom panels: mortality hazard estimates for each colony-size quartile from the top panel; vertical bars indicate 95% confidence intervals. Similar analyses were performed for each year, 2012–2020; all plots are provided in Supplemental Figure S1. See the “Methods” section for details. E For all colony-size quartiles, from all years analyzed in Supplemental Figure S1: a meta-analysis of quartile mean colony sizes (x-axis) versus 1-year mortality hazards (y-axis). Non-breeding males (cyan) and females (pink) were meta-analyzed separately. Regression lines for each sex are shown (p-values, 9.8 × 10⁻⁴ for males, 0.018 for females).

Fig. 5

The mortality hazard of Fukomys mole-rats increased with age. A Kaplan-Meier survival curve for combined data from the F. anselli and F. damarensis species of mole-rats (green) after reaching reproductive maturity (T_sex; 9 months from birth; 270 days; red). Plotted as in Fig. 1A, with a histogram of death and censorship (pink and purple, respectively) in the inset, up until 3400 days of age, at which point 120 animals remained in the population; and with censorship events after that indicated by vertical ticks (purple), the size of which is proportional to the number of animals censored at each day-of-life. Equivalent per-species analyses are provided in Supplemental Figure S2. B Mortality-hazard estimates (solid green) with 95% confidence intervals (dotted green) across the observed Fukomys mole-rat lifespan. Estimates were calculated across time intervals of increasing size (demarked by grey lines) to compensate for decreasing accuracy per unit time as the population size decreased. The borders of the age bins are indicated in gray, and the number of deaths (pink) and total years of animal life observed (green) per bin are indicated at the bottom of the panel. Equivalent per-species analyses are provided in Supplemental Figure S2. C For F.damarensis only: Kaplan-Meier survival starting at T_sex (270 days; red) for each of four reproductive categories of Damaraland mole-rats: male breeders (navy), female breeders, (red), male non-breeders (cyan), and female non-breeders (pink).

Fig. 6

In contrast to the mortality hazards of other mammals, which increased with chronological age, the mortality hazard of naked mole-rats remained constant. A Age-specific mortality hazard for humans (navy), mice (cyan), horses (orange), Fukomys mole-rats (purple), and naked mole-rats (green); with age (x-axis) normalized to T_sex for each species. Reproduced from (Ruby et al, 2018), with Fukomys data added and H. glaber data updated using results from this study. See the “Results” for references to original data sources. B A phylogenic tree for the species from panel A. See the “Results” section for references to data sources.