Massive Mammals With Menopause

Source: Original cartoon by Alex Martin

Around age 50, women abruptly become infertile in a striking and puzzling permanent “change of life”—menopause. Although age at menopause ranges from 42 to 56 between women, an average near 50 is remarkably consistent worldwide. This is hence a universal feature of our species, little affected by environmental influences.

Do other mammals have menopause?

Menopause has been widely regarded as uniquely human. Certainly, no other primate has anything like it, although some see the distinctive human condition as different only in degree. A 2008 review by Margaret Walker and James Herndon, for instance, concluded: “Existing data support the view that menopause occurs in a number of primate species and is not unique to humans.” But humans are unquestionably extreme outliers when the duration of post-reproductive infertility is compared to overall lifespan. Maximum human longevity is 125 years, so a woman can potentially live longer after menopause than before.

Two portrayals of the major distinction between humans and non-human primates with respect to the post-reproductive period. Upper Graph: Period between last birth and death plotted against body weight for human and nine non-human primates. The human value is an extreme outlier above the line, showing that the human post-reproductive period is unusually long relative to body size. Lower Graph: 90th percentile for age at last birth plotted against 90th percentile for age at death (i.e., the age at which 90% of individuals ceased reproduction and the age at which 90% of individuals had died). The human value is an extreme outlier below the line because of the unusually long interval between menopause and death.

Source: Author’s illustration based on data presented by Caro et al., 1995 (Upper Graph) and by Alberts et al., 2013 (Lower Graph).

Long-term breeding data for primates clearly show that humans are quite distinctive. A 1995 paper by Tim Caro and colleagues examined age-related changes in female reproduction for 13 primate species bred in captivity. Data for a human population in Krummhorn, northwestern Germany during the 18th/19th centuries—approximating natural fertility—were taken for comparison. Plotting the average post-reproductive interval (age at last birth to age at death) against body weight clearly showed that humans have a far longer post-reproductive period, relative to body size, than any other primate

This finding was subsequently corroborated by Susan Alberts and colleagues in a 2013 paper examining long-term data for wild populations of seven non-human primate species. Data for Dobe !Kung hunter-foragers of southern Africa—with natural fertility and mortality—provided a human comparison. Because of natural variation, there will always be occasional females in any primate population that stop breeding several years before they die. This is very different from having a genuine post-reproductive life stage shown by all females. Alberts and colleagues aimed to establish whether the aging of the reproductive system occurred significantly earlier than the general aging of the body. To gauge this at the population level, for each species they identified the age at which 90% of individuals had given birth for the last time and the age at which 90% had died. For all seven primate populations, most individuals showed little reproductive decline before death, contrasting starkly with the typical human post-reproductive period of some 30 years.

Seeking further cases of post-reproductive life stages, a 2018 paper by Samuel Ellis and colleagues analyzed life tables constructed for wild-living populations of 52 mammal species. For each population they calculated post-reproductive representation (PrR) — the ratio of years lived by post-reproductive females to total years lived. PrR has two advantages: it is directly comparable between species with different lifespans, and it is possible to test whether the proportion of females surviving into an infertile life stage is significantly greater than zero. Using that criterion, true menopause proved to be rare among mammals. Only three of the 52 species had a PrR significantly exceeding zero: humans, killer whales and short-finned pilot whales. The sample included nine primates other than humans, none of which yielded a PrR value indicating true menopause.

A pod of killer whales in the North Pacific.

Source: Wikimedia Commons

Menopause in Whales

Although primates other than humans clearly lack menopause, it has gradually emerged that certain whale species do have a definite post-reproductive life stage. Ellis and colleagues neatly confirmed this for killer whales and short-finned pilot whales by showing that both have PrR values significantly greater than zero.

A quiet revolution in recognizing menopause in other mammals was sparked by a 1990 whaling report indicating the presence of post-reproductive females among resident killer whales in coastal waters off northwestern America. The lead author, Peter Olesiuk, and others provided full details in a substantial monograph 15 years later. Female killer whales typically breed between the ages of 12 and 40 years but can survive beyond 90. In 2008, Andrew Foote discussed evidence for a distinct post-reproductive lifespan in killer whales and also in another species living in stable matrilineal groups: the short-finned pilot whale.

A brief report published in 2012 by Emma Foster and colleagues analyzed data for the resident killer whales studied by Olesiuk and colleagues and proposed that offspring benefit from the prolonged post-reproductive life stage of old females. Because pods have a matrilineal structure, a female’s relatedness to other group members increases as she ages, meaning that old females can promote survival and reproductive success of their own offspring.

Subsequently, members of the same research group published several papers reporting findings for grandmothers in two pods of resident killer whales. In 2015, Lauren Brent and others showed that post-reproductive females are more likely than other group members to lead during feeding on salmon (97% of the diet). Such leadership was particularly evident in challenging years with salmon scarcity. Then, in 2017, Darren Croft and others examined the potential significance of reproductive conflict between younger and older females within a pod. Having confirmed that relatedness in the pod increases with female age up till menopause, they developed a model predicting that—if mothers and daughters breed at the same time—selection should favour younger females investing more in competition. Data collected over 43 years revealed that, when both are breeding, calves born to mothers are almost twice as likely to die as those born to daughters. A third paper in 2019, with Stuart Nattrass as lead author, directly tested whether post-reproductive female killer whales enhance survival of their grandoffspring. Survival of grandoffspring was evaluated according to presence or absence of breeding or post-reproductive grandmothers in the pod. It emerged that grandoffspring received significant survival benefits from both but particularly from post-reproductive grandmothers.

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Distribution map for pilot whales, combined with images of the short-finned and long-finned species, which occupy largely separate ocean regions. The short-finned pilot whale was photographed along the western coast of Tenerife, Canary Islands; the long-finned pilot whale was photographed at Blue Horizons Dolphin Stadium.

Source: Images from Wikimedia Commons. Distribution Map: Author: Pengo assumed (own work assumed; 2007); file licensed under the Creative Commons Attribution-Share Alike 3.0 Unported license. Short-Finned Pilot Whale: Author: Cayambe (own work, 2012); file licensed under the Creative Commons Attribution-Share Alike 3.0 Unported license. Long-Finned Pilot Whale: Author: Curimedia | P H O T O G R A P H Y (2012); file licensed under the Creative Commons Attribution 2.0 Generic license.

At this point, a surprising difference between the short-finned pilot whale and its sister species, the long-finned pilot whale, must be mentioned. Whaling records from the 1980s indicated that, whereas the short-finned species has a well-defined post-reproductive life stage, its long-finned relative does not. This was neatly confirmed in 2018 by Ellis and colleagues in a second paper, which reported a PrR value close to zero for long-finned pilot whales but a statistically significant value for the short-finned sister species, with females surviving an average of over 20 years after ceasing to breed. This unusual case presents researchers with a golden opportunity to test the general validity of explanations proposed for killer whales.

Asian elephants (left) have menopause, but African elephants (right) do not.

Source: Images from Wikimedia Commons. Image of Asian elephant mother with infant (left) originally posted to Flickr by Rison Thumboo, reviewed on 7 November 2018 by FlickreviewR 2 and confirmed to be licensed under the terms of the cc-by-2.0. Image of African elephant mother with infant (right) from author Axel Tschentscher. File licensed under the Creative Commons Attribution-Share Alike 4.0 International license.

Menopause in Elephants

Whales are large-bodied, long-lived mammals. So an obvious question is whether female elephants also have menopause. In a 2015 post for his National Geographic blog, science journalist Ed Yong tackled this issue in a piece entitled “Why Killer Whales Go Through Menopause But Elephants Don’t." He suggested that a crucial difference in resident killer whales is that both sons and daughters remain in the pods of their birth. This is why, as a female ages, her pod increasingly includes direct relatives. In elephants, by contrast, sons eventually migrate out of their birth group, so aging females become less related to other group members over time.

Data from an Asian elephant population in Myanmar. Left: Histogram showing frequencies for ages at last birth. Right: Plot of years since last birth by (current/death) age. The horizontal lines show the mean interbirth intervals (blue) and mean plus two standard deviations (red).

Source: Coloured version of histogram and plot from an open access article by Chapman et al. (2019). Article distributed under the terms of the Creative Commons Attribution 4.0 International License. Asian elephant Icon added from Wikimedia Commons. Author: Shyamal (own work, 2013). File made available under the Creative Commons CC0 1.0 Universal Public Domain Dedication.

Yong’s comments presumably reflected fieldwork with African elephants, which have been intensively studied; but a 2019 paper by Simon Chapman and colleagues has now revealed that significant post-reproductive lifespans do characterize Asian elephants. Only the African elephant was included in the first 2018 paper by Ellis and others, who reported a PrR value close to zero. Contrastingly, Chapman and colleagues calculated a PrR value significantly greater than zero for Asian elephants.

It remains to be seen whether the post-reproductive lifespan in Asian elephants accords with explanations of menopause proposed for killer whales and humans. Moreover, do similar explanations also account for the disparity between short- and long-finned pilot whales? In fact, the second 2018 paper by Ellis and others identified two additional whales with significant post-reproductive life stages: narwhal and beluga. They must also be investigated to expand our understanding of menopause. Last but not least, menopause in killer whales has some puzzling features, notably the fact that males die much earlier than females, rarely surviving beyond 50. This raises concerns about extrapolating results between humans and killer whales. In short, much work remains to be done to achieve convincing explanations for the evolution of menopause.