Abstract
BackgroundMenopause is a seemingly maladaptive life-history trait that is found in many long-lived mammals. There are two competing evolutionary hypotheses for this phenomenon; in the adaptive view of menopause, the cessation of reproduction may increase the fitness of older females; in the non-adaptive view, menopause may be explained by physiological deterioration with age. The decline and eventual cessation of reproduction has been documented in a number of mammalian species, however the evolutionary cause of this trait is unknown.ResultsWe examined a unique 30-year time series of killer whales, tracking the reproductive performance of individuals through time. Killer whales are extremely long-lived, and may have the longest documented post-reproductive lifespan of any mammal, including humans. We found no strong support for either of the adaptive hypotheses of menopause; there was little support for the presence of post-reproductive females benefitting their daughter's reproductive performance (interbirth interval and reproductive lifespan of daughters), or the number of mature recruits to the population. Oldest mothers (> 35) did appear to have a small positive impact on calf survival, suggesting that females may gain experience with age. There was mixed support for the grandmother hypothesis – grandoffspring survival probabilities were not influenced by living grandmothers, but grandmothers may positively influence survival of juveniles at a critical life stage.ConclusionAlthough existing data do not allow us to examine evolutionary tradeoffs between survival and reproduction for this species, we were able to examine the effect of maternal age on offspring survival. Our results are consistent with similar studies of other mammals – oldest mothers appear to be better mothers, producing calves with higher survival rates. Studies of juvenile survival in humans have reported positive benefits of grandmothers on newly weaned infants; our results indicate that 3-year old killer whales may experience a positive benefit from helpful grandmothers. While our research provides little support for menopause evolving to provide fitness benefits to mothers or grandmothers, our work supports previous research showing that menopause and long post-reproductive lifespans are not a human phenomenon.
Highlights
Menopause is a seemingly maladaptive life-history trait that is found in many longlived mammals
Anthropologists have suggested that menopause is unique to primates [2] or even just humans [3,4], the phenomenon appears to be widespread in mammals – in a meta-analysis of 42 species, Cohen (2004) found support for post-reproductive lifespans (PRLS) in 83% of taxa
Support for the mutation accumulation hypothesis Evolutionary theory predicts that if menopause is a byproduct of senescence, the difference between female lifespan and menopause would be approximately equal to the time necessary for a female to live long enough to raise her last offspring [12]
Summary
Menopause is a seemingly maladaptive life-history trait that is found in many longlived mammals. Individuals in many mammalian species devote a fraction of their lives to reproduction Females in these species experience a gradual midlife decline in reproductive performance with age, and eventually menopause, the abrupt termination of reproduction [1]. More recent studies have shown that there are a range of species with relatively little or no parental investment that exhibit reproductive senescence and cessation, including species generally considered to be 'r-selected'. These species include guppies [5], parakeets [6], mice [7], and beetles [8]
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