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Reproductive senescence and menopause are rare in nature. Only five species of
mammals have females with a post-reproductive life span: humans, killer whales,
short-finned pilot whales, belugas, and narwhals. What are the possible hypotheses
for the evolution of this unusual trait?
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Introduction
Menopause and post-reproductive life spans (PRLSs), often deemed as unusually evolved
traits in the animal kingdom, are seen in very few mammals; limited to humans (Homo
sapiens), beluga whales (Delphinapterus leucas), narwhals (Monodon monoceros), short-
finned pilot whales (Globicephala macrorhynchus) and killer whales (Orcinus orca). The
evolution of PLRSs in these species has been studied resulting in adaptive and non-
adaptive(Ward, et al., 2009). Hypotheses vary in reliability, with continuous long-term
research supporting the ‘grandmother hypothesis’, whereas the ‘mate-choice’ hypothesis is
based on computational models (Nattrass, et al., 2019) (Takahashi, et al., 2017). It is likely
that multiple hypotheses combine to explain the evolution of reproductive senescence and
menopause. In this essay I will investigate hypotheses for the evolution of PLRSs and
menopause and explore the evidence to support them.
Key words: senescence; grandmother hypothesis; post-reproductive lifespan; menopause
Background
The study of reproductive life spans has found a range in length, but in all species
reproductive senescence is more rapid than somatic deterioration (Blell, 2017). Hypotheses
for the evolution of reproductive senescence have been divided into either adaptive or
nonadaptive; where adaptive theories claim females end their reproductive life spans to
increase survival rates of their existing descendants, whereas non-adaptive theories suggest
menopause is due to an evolutionary recent increase in human lifespan (Austad, 1994).
Evolutionary scientists support the idea that menopause is directly affected by longevity, and
that longevity is the factor that differentiates human beings from apes, who don’t have a
PLRS (University of Georgia, 2020). The evolution of the reproductive life span in humans
comes from the benefits post-reproductive females can obtain having provided for their
offspring, introducing the ‘grandmother hypothesis’ (Nattrass, et al., 2019).
Very few species have been found to have a PLRS so we can study the 5 that do and
compare them. One way of comparing PLRSs between species is using ‘post-reproductive
representation’ (PrR) which measures lifespan of females who have undergone menopause
(Johnstone & Cant, 2019). Only 5 species have a PrR considerably greater than 0; we can
see that killer whales have a value of 0.31, compared to chimpanzees with a value of 0.01
(Johnstone & Cant, 2019). This is illustrated in figure 1, where we see only killer whales,
short-finned pilot whales, beluga whales, narwhals and humans with significant PLRSs (also
9 species with negligibly small PLRSs, e.g. Steller’s sea lions).

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Fig. 1: a bar graph showing the number of species, out of a sample of 51 species of
mammals, that have a PLRS. In green, the reproductive lifespan, and in orange, the PLRS
(Johnstone & Cant, 2019). Graph reproduced from (Ellis, et al., 2018).

1. Adaptive hypotheses
Menopause can be explained by adaptive hypotheses, which are based on the idea that
females stop reproducing due to a selective advantage (Austad, 1994). Females who have
offspring towards the end of their reproductive lifespan are more at risk of death to
themselves or their offspring (Huang, et al., 2008). So, it would maximise their survival rates
to use their resources and energy increase the chances of survival of their offspring or grand
offspring to pass on their genes (Pavard, et al., 2008). This type of hypothesis is used to
explain the evolution of menopause and PRLSs by looking at how they could affect inclusive
fitness.

Mother hypothesis
One adaptive hypothesis, the ‘mother hypothesis’, involves helping kin later in life (Croft, et
al., 2015). It suggests that older mothers will increase their fitness by investing in their
existing kin (Pavard, et al., 2008). This hypothesis also explains evolution of menopause by
claiming that the trait reduces mortality associated with reproduction in females who are
reaching the end of their fertile lifespan (Lahdenperä, et al., 2010). As infants are born and

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require more care, reproductive senescence allows the mothers to improve the chances of
their kin’s survival by avoiding risky pregnancies later in their lives and investing in providing
for their offspring, as reproduction is more costly for older females (Ward, et al., 2009).
There was little significant evidence for this hypothesis in studies on the impact of mother
loss on offspring in Finns and Canadians (Lahdenperä, et al., 2010).
Grandmother hypothesis
Alternatively, the ‘grandmother hypothesis’ has been proposed to explain the evolution of
PLRSs; it suggests that grandmothers can increase the chance of survival of their grand
offspring by sharing food with nursing mothers or infants and teaching about hunting
(Hawkes, et al., 1998; Johnstone & Cant, 2010). This hypothesis has also been described as
kin selection because genes for PLRSs are passed on due to the benefits they have on
offspring, where grandmothers who care for their grandchildren improve their chances of
survival considerably (Blell, 2017).
There is a large bank of evidence supporting this hypothesis amongst humans as well as
with a long-term study on some Southern resident killer whale populations (Nattrass, et al.,
2019). Studies have proved that when a grandmother whale dies, her grand offspring are
less likely to survive; if the maternal grandmother dies the offspring have a mortality rate that
is 4.5 times multiplied for the 2 years after her death (Nattrass, et al., 2019).

Fig. 2: Graphs showing the survival rates for a variety of ages of whale ((A) 5-year-old, (B)
15-year-old and (C) 20-year-old) with either a living grandmother, a recent post-reproductive
grandmother death or a recent reproductive grandmother death (Nattrass, et al., 2019).
The graph in figure 2 shows significant correlation in the survival rate of the offspring and the
presence of its grandmother. Younger whales are much less likely to survive without a
grandmother than 15 and 20-year-old whales. However, another study on a group of 30
whales shows no strong evidence for an adaptive evolutionary explanation to the evolution
of menopause; only some support that grandmothers may have an effect on the survival of
young juveniles and that there may be evidence for gained wisdom with age (Ward, et al.,
2009).
Resident killer whales feed primarily on Chinook salmon (Oncorhynchus tshawytscha) and
when abundance is low, killer whale mortality increases (Ford, et al., 2009). It is theorised
that when populations are low, grandmother killer whales will have the knowledge of where
and when to find resources and will share her hunt with her grand offspring (Nattrass, et al.,
2019). Analysing video footage of the Southern resident killer whales showed that post-
reproductive females lead their group more often than reproductive females or males, and

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they were even more likely to lead when there was low salmon availability (Brent, et al.,
2015).

Fig. 3: negative correlation between post-reproductive female leadership and salmon

abundance compared to reproductive female Southern resident killer whales (Brent, et al.,
2015).
The graph in figure 3 demonstrates that with low salmon abundance, post-reproductive
females take a leadership role. It was also shown that males are more likely to follow their
mother because they mate outside of their group, so are disproportionally favoured as they
don’t have to provide for the son’s offspring (Brent, et al., 2015).
Absent father hypothesis
The ‘absent father’ hypothesis suggests that an increase in the absence of fathers could
have contributed to the evolution of menopause. This complements the grandmother
hypothesis as paternal investment could be costly in female reproduction; it suggests that if
fathers were less invested in offspring, this would have a negative impact on older mothers,
as they would struggle to look after their kin. (Kuhle, 2007).

1. Non-adaptive hypotheses
Non-adaptive hypotheses have also been proposed in which PLRSs have evolved due to
reproductive senescence with ageing (Austad, 1994). An example is the ‘mutation
accumulation’ model which theorises that females stop reproducing due to physiological
degradation and older individuals are selected against, resulting in evolution of menopause
(Ward, et al., 2009). Reproductive and somatic lifespans have gradually increased in
difference, supporting this theory (Ward, et al., 2009).
Mutation accumulation (mate-choice) hypothesis
The mutation accumulation hypothesis is also known as the ‘mate-choice’ hypothesis where
adults of both sexes change their mating behaviour. This reduces selection on older females
so fertility reducing genes having little effect and mutant alleles increase in numbers over
time, subsequently evolving reproductive senescence (Takahashi, et al., 2017). A computer

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model was used to study this hypothesis, but there is no tangible data to support it in the wild
(Morton, et al., 2013). The two scenarios tested were young female competition with older
females for mates, or males selecting younger females as mates; but this hypothesis is not
widely accepted due to the fact it is based purely off mating behaviour (Takahashi, et al.,
2017).
When looking at reviews of data for PLRSs across multiple taxa, a non-adaptive hypothesis
was suggested where there are two types of selection acting on reproductive and somatic
lifespans separately (Cohen, 2007). This hypothesis has the potential to explain PLRSs but
doesn’t have the data to support it due to the longevity of the species studied (Ward, et al.,
2009).

Conclusions
When inspecting the various hypotheses, we can see how the organization of a family has
played an important role in the evolution of menopause and PLRSs by influencing which
generation of females stop reproducing and when. Investigating the evolution of traits in
species with such longevity poses challenges, so it is much harder to conclude on a suitable
hypothesis. Studies using computer models can be helpful to illustrate hypotheses
theoretically, but real-life data is invaluable.
There is strong evidence for the grandmother hypothesis, when we look at the studies done
on the Southern resident whales, as the research has been conducted over a suitably long
period of time. The data to support the grandmother hypothesis is undeniable in showing
that juvenile killer whales have a significantly increased chance of survival with a
grandmother present, especially on the maternal side, whether it be due to offspring care or
experience in hunting.

Reference List
Austad, S. N. (1994) ‘Menopause: an evolutionary perspective’, Experimental Gerontology, 29(3-4),
pp. 255-63.

Blell, M. (2017) ‘Grandmother Hypothesis, Grandmother Effect, and Residence Patterns’, The
International Encyclopedia of Anthropology.

Brent, L. J., Franks, D.W., Foster, E.A., Balcomb, K.C., Cant, M.A. & Croft, D.P. (2015) ‘Ecological
Knowledge, Leadership, and the Evolution of Menopause in Killer Whales’, Current Biology, 25(6),
pp. 746-750.

Cohen, A. A. (2007) ‘Female post-reproductive lifespan: a general mammalian trait’, Biological

Reviews, 79(4), pp. 733-750.

Croft, D. P., Brent, L. J. N., Franks, D. W. & Cant, M. A. (2015) ‘The evolution of prolonged life after
reproduction’, Trends in Ecology & Evolution, 30(7), pp. 407-416.

Ellis, S., Franks, D.W., Nattrass, S., Currie, T.E., Cant, M.A., Giles, D., Balcomb, K.C. & Croft, D.P.
(2018) ‘Analyses of ovarian activity reveal repeated evolution of post-reproductive lifespans in
toothed whales’, Scientific reports, Volume 8.

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Ford, J. K. B., Ellis, G.M., Olesuik, P.F. & Balcomb, K.C. (2009) ‘Linking killer whale survival and prey
abundance: food limitations in the oceans' apex predator?’, Biology Letters, 6(1), pp. 139-142.

Hawkes, K., O’Connel, J.F. & Blurton Jones, N.G. (1998) ‘Grandmothering, menopause, and the
evolution of human life histories’, Proceedings of the National Academy of Sciences of the United
States of America, 95(3), pp. 1336-1339.

Huang, L., Sauve, R., Birkett, N., Fergusson, D. & van Walraven, C. (2008) ‘Maternal age and risk of
stillbirth: a systematic review’, Canadian Medical Association Journal, 178(2), pp. 165-172.

Johnstone, R. A. & Cant, M. A. (2010) ‘The evolution of menopause in cetaceans and humans: the
role of demography’, Proceedings of the royal society, 277(1701), pp. 3765-3771.

Johnstone, R. A. & Cant, M. A., (2019) ‘Evolution of menopause’, Current biology, 29(4), pp. 112-115.

Kuhle, B. X. (2007) ‘An evolutionary perspective on the origin and ontogeny of menopause’,
ScienceDirect, pp. 329-337.

Lahdenperä, M., Russell, A. F., Tremblay, M. & Lummaa, V. (2010) ‘Selection on menopause in two
premodern human populations: no evidence for the mother hypothesis’, Evolution, 65(2), pp. 476-
489.

Morton, R. A., Stone, J. R. & Sing, R. S. (2013) ‘Mate Choice and the Origin of Menopause’, PLOS
COMPUTATIONAL BIOLOGY.

Nattrass, S., Croft, D.P., Ellis, S. & Franks, D.W. (2019) ‘Postreproductive killer whale grandmothers
improve the survival of their grandoffspring’, Proceedings of the National Academy of Sciences of the
United States of America, 116(52), pp. 26669-26673.

Pavard, S., Metcalf, C. J. E. & Heyer, E. (2008) ‘Senescence of reproduction may explain adaptive
menopause in humans: a test of the "mother" hypothesis’, The American Journal of Physical
Anthropology, 136(2), pp. 194-203.

Takahashi, M., Singh, R. S. & Stone, J. (2017) ‘A Theory for the Origin of Human Menopause’,
Frontiers in Genetics, Volume 7.

University of Georgia (2020) ‘What is the evolutionary purpose of menopause?’, Newswise, 18

February.

Ward, E. J., Parsons, K., Holmes, E.E., Balcomb III, K.C. & Ford, J.K.B (2009) ‘The role of menopause
and reproductive senescence in a long-lived social mammal’, Frontiers in Zoology, 6(4).