Discussion
We show that three sympatric killer whale populations, have comparably
long post-reproductive female lifespans. With a median of more than 30%
of all adult female years in all three populations being lived by
post-reproductive females, it is a substantial life history stage (Fig.
3). This is the first evidence showing a long post-reproductive period
as a shared trait among genetically distinct killer whale populations,
suggesting that it could have evolved in a common ancestor to current
killer whales and that it might be present in other discrete
populations. Indeed, phylogenomic analysis suggests that the divergence
between the lineages leading to resident and Bigg’s ecotypes is the
earliest divergence of extant killer whale lineages occurring over
350,000 years ago64. If the shared presence of a
post-reproductive lifespan in both residents and Bigg’s is due to a
shared ancestral trait, this suggests that a post-reproductive lifespan
is an ancestral state of all extant killer whale ecotypes.
From the survival model output, the survival patterns is similar in all
three killer whale populations, with females expected to live
substantially longer than males and females being able to live
>50 years (Fig. 2). Interestingly, the model predicts that
male Bigg’s killer whales may have a longer expected lifespan compared
to resident males (Fig. 2.), a pattern that may be influenced by the
difference in their environments, both social65,66 and
ecological (such as the recent prey abundance of the favourable prey of
Bigg’s67). However, this could also be an effect of
male dispersal in Bigg’s, resulting in more uncertainty for the model
around the ages at death of males. In females the survival trajectory of
this study is generally supported by previous estimates of lifespan in
killer whales29,30. We used a Bayesian hierarchical
approach to estimate the age-specific survival, with the benefit of
being able to include individuals with unknown age of birth and death.
Further, through permutations we were able to include individuals of
unknown sex which likely produces random variation in the model output.
Rather than considering maximum longevity, comparing the ages when 95%
of years have been lived in each population is a more reliable measure
(Fig. 2). This metric indicates that Bigg’s females are expected to live
longer than females from both resident populations with a difference of
~10 years (Fig. 2). However, despite the differences in
the estimated maximum lifespan, the results clearly show that all three
populations have significant post-reproductive periods with similar ages
of onset of the post-reproductive life stage in females (Table 4).
The cessation of female reproduction well before the end of life in a
limited number of wild mammals largely remains an evolutionary puzzle.
Yet, there is growing evidence that it has evolved based on the combined
inclusive fitness benefits of helping and the costs of reproductive
conflict for older females3. The opportunity for
females to help kin is integral to the adaptiveness of ceasing
reproduction well before the end of life9,15. Previous
research in both humans and resident killer whales, has shown that older
females are able to provide help that positively affects the survival
and reproduction of their kin15,68,69. Especially in
humans, offspring can have a long period, where they rely on older
individuals for help providing food4. Our study
demonstrates that females of both resident and Bigg’s killer whales can
expect to live more than 20 years after they cease reproduction,
allowing for a substantial period with the potential for helping kin. In
resident killer whales, mothers impact the survival of their offspring
well into their adult years15, and grandmothers are
important repositories for ecological knowledge for
relatives11 increasing the survival of their
grandoffspring8. Although dispersal of both males and
females is more pronounced within the Bigg’s ecotype, the
post-reproductive females are never observed on their own, but always
with either their son(s) or daughter(s)41. Further,
the smaller matrilines may consist of up to three generations of
maternally related kin and are regularly observed associating with
individuals outside of the maternal group31,41. These
patterns of association provide opportunities for social interactions
that can lead to inclusive fitness benefits for older
females11,70. While the earlier dispersal of females
from Bigg’s groups likely reduces the occurrence of reproductive
conflict between mothers and daughters (Fig. 1)4,
Bigg’s groups can also consist of reproductively active females from
different generations, similar to the resident killer whales. The
similarity in the timing of the cessation of reproduction at around 40
years in both the resident and Bigg’s ecotypes, indicate that Bigg’s
females may also experience inter-generational reproductive conflict and
that this plays an important role in shaping fertility patterns across
the different ecotypes. Testing this hypothesis requires more work on
quantifying the kin structure and mortality patterns of Bigg’s killer
whales.
Here we found that the differences in dispersal patterns between
resident and Bigg’s killer whales did not predict the timing of the
cessation of reproduction and the length of the post-reproductive
lifespan. Similarly in humans, Snopkowski et al. (2014) compared age at
menopause across ethnic groups with different patterns of post-marital
residence to explore whether differences in dispersal pattern had an
effect on the timing of menopause71. They showed that
female-biased dispersal, expected to lead to an increase in female local
relatedness with age, did not result in an earlier age at menopause
compared to groups with male-biased dispersal
patterns71. It is possible that modern societies in
both humans and killer whales are different from the ancestral societies
in which the evolutionary effects of reproductive conflict and the
timing of menopause occurred. The lack of variation in the timing of
reproductive cessation despite differences in dispersal patterns has
important implications for our understanding of the evolution of a long
post-reproductive period in mammals, including humans. Although patterns
of kinship dynamics may predispose females to evolve a prolonged
post-reproductive lifespan, the costs and benefits of reproductive
conflict and helping are going to be shaped by the ecology of the
population. For example, despite the close resemblance of demographic
patterns between short- and long-finned (Globicephalas melas )
pilot whales72,73, indicating similar kinship
patterns, a long post-reproductive lifespan has only been observed in
the short-finned pilot whales1, which could be a
result of difference in ecology of the two species. Moreover, there are
several examples of primate species with female-biased dispersal and
local mating (e.g. chimpanzee, bonobos and
gorillas74–76), and thus an increase in female local
relatedness with age similar to humans, where a prolonged
post-reproductive lifespan has not evolved1. It is
likely that we may find similarly prolonged post-reproductive lifespans
in other killer whale populations or other mammal species as we gather
more individual-based data on long-lived social mammals. Some evidence
already suggests that false killer whales (Pseudorca
crassidens )5 and Asian elephants (Elephas
maximus ) have a long period as post-reproductive, although for Asian
elephants it is likely a social rather than physiological
trait77.
The similarity in the timing of
menopause among killer whales and humans is curious and could hint at
there being a similar driver of the evolution of onset of menopause.
Current models investigating the role of kinship dynamics for driving
the evolution of menopause make specific predictions regarding how
patterns of helping and harming will change with
age4,19 yet they do not predict how these patterns
will drive the timing of menopause or the length of the
post-reproductive lifespan. Hence our prediction that differences in
dispersal patterns would lead to different selection pressures for a
post-reproductive period in the two different killer whale ecotypes are
currently based on the reasoning that kinship dynamics are an indicator
for the strength of selection for helping vs harming across the
lifespan. It is possible that menopause can not easily be reversed once
evolved which may help explain the universality in the timing of
menopause in humans, and likely also killer whales, despite the evident
differences among societies, such as patterns of
dispersal71.
In conclusion, when taken together with previous work, our findings
support the hypothesis that kinship dynamics play a key role in the
evolution of a prolonged post-reproductive lifespan. However, contrary
to our predictions, the timing and expected duration of the
post-reproductive lifespan did not vary with the dispersal pattern from
the natal group, which likely represents different costs and benefits of
helping and harming in the two ecotypes. These were, however, not taken
into account in our predictions, but would be valuable to disentangle in
future research to better understand the drivers for the timing of long
post-reproductive lifespans in mammals. Nevertheless, the clear
similarity of the post-reproductive period in some of the most
genetically distinct killer whale populations echoes what has been
observed across different human societies. This indicates a long
post-reproductive period being an ancestral trait in killer whales, and
likely present in other killer whale populations and ecotypes.