Introduction
The evolution of an extended female post-reproductive lifespan is
extremely rare in nature and is at present only known in five species of
wild mammals1–3. Outside of the prolonged
post-reproductive lifespan seen in humans the only other species of
mammals in which females have evolved early cessation of reproduction
are toothed whales: short-finned pilot whales (Globicephala
macrorhynchus ), narwhals (Monodon monoceros ), belugas
(Delphinapterus leucas ) and resident-ecotype killer whales
(Orcinus orca )1,4. Some evidence suggests that
also the false killer whales (Pseudorca crassidens ) have a
substantial post-reproductive period5. In
resident-ecotype killer whales, for example, adult females typically
give birth to their last calf in their mid 30’s to early 40’s followed
by a post-reproductive lifespan that may span many
decades1. In the classical view of evolutionary
theory, early termination of reproduction is not a beneficial
trait6,7 and understanding why and how the
post-reproductive lifespan has evolved remains a considerable challenge
for evolutionary biology.
Adaptive explanations for the evolution of a long post-reproductive
lifespan have tended to focus on the inclusive fitness benefits of
helping kin in late life8–10. Females can gain
inclusive fitness benefits in late life by ceasing reproduction and
instead invest their energy in helping existing offspring survive and
reproduce (‘the mother hypothesis’)6. Further, through
behaviours that help increase the survival of grandchildren, such as
providing ecological knowledge11 or
provisioning12, post-reproductive females can increase
their inclusive fitness (’the grandmother
hypothesis’)13. In humans, grandmother benefits appear
to be key for the evolution of a long post-reproductive lifespan13,14 and recent work in resident killer whales
provides support for both the mother and grandmother hypothesis with the
presence of both mothers and post-reproductive grandmothers having a
positive impact on the survival of their adult offspring and
grandofffspring8,15. However, the inclusive fitness
benefits from helping are likely not on its own sufficient to explain
the timing of menopause in both killer whales and
humans16 leading to the search for additional
mechanisms that can contribute to the early termination of
reproduction17,18. Recent work has shown that
kin-selected costs, as well as benefits, are important for the evolution
of extended post-reproductive lifespans4,19.
Demographic patterns with either female-biased dispersal and local
mating or natal philopatry of both sexes and non-local mating, give rise
to age-specific changes in the relatedness of an individual to its group
(kinship dynamics), in particular an increase in average female
relatedness to other group members with age19. In the
case of resident killer whales, females are born into social unit
(“matriline”) consisting of their mother, siblings and other more
distant relatives20. As they age, their own sons
replace more distantly related males in the matriline, increasing their
average local relatedness to the group over time21.
This ultimately leads to an asymmetry in selection for helping and
harming with age, which means that older females that are more related
on average to the group are under stronger selection to help, while
younger females are under stronger selection to harm4.
Thus, in competition for reproduction older females experience a larger
inclusive fitness cost compared with younger
females21. The combination of such inclusive costs of
inter-generational reproductive conflict and inclusive fitness benefits
of helping kin are hypothesised to be key predictors for the evolution
of a long post-reproductive lifespan in mammals1,4,19.
Investigating kinship dynamics and age-specific life history changes
requires long-term social and demographic data that captures most of the
lifespan of animals. These data are therefore rare in long-lived
mammals. The long term data collected on different populations of killer
whales in the coastal waters of the USA and Canada now extends over more
than four decades, providing an unique opportunity to examine the link
between kinship dynamics and life history evolution in a long-lived
marine mammal. In addition to the support for the mother and grandmother
hypotheses in resident killer whales8,15, there is
strong support for the reproductive conflict hypothesis with offspring
of older females that are born into conflict with offspring of a younger
female having a 1.7 times higher mortality risk21.
However, it is still unknown whether these traits are shared between
different populations of killer whales. Killer whales are among the most
widely dispersed mammals on the planet and are found in all
oceans22,23. Lineages that differ
morphologically24 and
behaviourally25 and are genetically
isolated26, are referred to as ecotypes. Three killer
whale ecotypes are sympatric in the northeast Pacific and among them are
several populations of both resident and Bigg’s killer
whales27,28. In the waters off the west coast of North
America are the Northern and Southern populations of resident killer
whales and the West Coast Transient populations of Bigg’s killer whales
(Table 1; a third offshore ecotype is also encounterd, but only very
rarely is not considered here)26,27,29. Both
populations of residents are specialist fish-eaters with salmon making
up the almost all of their prey20,30, whereas Bigg’s
killer whales are specialised in hunting marine
mammals31. This differentiation in diet is reflected
in the social behaviour of the ecotypes with resident killer whales
typically being observed travelling in larger social groups consisting
of several maternal groups, compared to Bigg’s killer whales. The mean
group size of cohesive maternal groups however are similar for the two
ecotypes (Table 1)32. In resident killer whales there
is almost no dispersal of males and limited dispersal of females from
the maternal group. In contrast, there is dispersal of both sexes from
the maternal group of Bigg’s killer whales31,33, which
may be related to maintaining optimal group foraging size for predating
on marine mammals34,35.