True, but that’s not really the relevant question to ask. In fact, aging has a major impact on mortality in the wild, and this poses a dilemma for evolutionary theory. In the earliest stages of senescence, already an individual may be losing its competitive edge. When an epidemic passes through, those with compromised immune function are the first to die. When a predator is chasing the herd, those that cannot run quite as fast as they used to are caught at the back of the crowd. In this way, aging can have a big effect on fitness even if no one is “dying of old age”.
In 1951, Peter Medawar put forward the first modern theory for the evolution of aging. He was a self-made Brazilian giant, 6 foot 5, as charismatic as he was brilliant, and at the age of 36 he had achieved a prestigious appointment at University College, London. For his inaugural address, he chose to tackle an Unsolved Problem of Biology, and asked how aging in nature could be reconciled with Darwinian evolution.
There had been no evolutionary theory of aging in the 50 years since August Weismann had disavowed his own. Medawar was astute enough to realize that Weismann was correct to seek an evolutionary understanding of aging. Aging cannot be understood from thermodynamics or physical processes of attrition. No physical law requires aging. Medawar was also correct in judging that Weismann’s proposed solution was no solution at all. “Weismann caters twice round the perimeter of a vicious circle. By assuming that the elders of his race are decrepit and worn out, he assumes all but a fraction of what he has set himself to prove.”
Medawar proposed the theory that natural selection can only work on living, reproducing individuals. But in the wild, there are so many hazards that can lead to death that, past a certain age, there are very few remaining alive. In nature, everyone dies before they reach old age. This creates a “selection shadow”. Bodies are evolved to be healthy, strong or fertile up to the age where there are still survivors in nature. But at advanced ages, natural selection has never had an opportunity to work her magic, so we should not be surprised that the organism is ill-adapted and falls apart.
We get old and die because of evolutionary neglect. Natural selection needs living, reproducing individuals to select from, or it is ineffectual; hence we expect that aging takes over and the body deteriorates soon after that age at which predators and disease and other hazards of the wild have thinned the population near to zero.
The rest is history
Very quickly, Medawar’s idea was enshrined in the canon of evolutionary theory. Building on Medawar, two more ideas were added. One was the concept of “mutational load”. If there was no natural selection at work for “late-acting genes”, then random mutations would creep in, and this would account for the organism going to pot. This became the Mutation Accumulation theory. The other was the idea that selection at late ages may be weak but not zero, and it could then be overpowered by the drive to maximize fertility early in life, even if it had bad consequences for fitness later on. This became the Antagonistic Pleiotropy theory.
The idea that, in the wild, no one lives long enough to die of old age made a great deal of intuitive sense. George Williams (of the pleiotropy theory) added a refinement: that the early stages of senescence would likely have consequences for individual competitiveness, so he based his theory on the idea that selection against aging was weak but not zero. But everyone was agreed that the fitness consequences of aging were very slight, if not actually negligible.
Evolutionary theory went on to develop on this basis, and continued to be embellished for 40 years.
The inconvenient truth came to light gradually, and several decades on. In physics and chemistry, experimental science is an attractive calling because practitioners get to hang out in a lab and perform magic with nifty apparatus and spiffy electronics. But experimental ecology is a field science requiring travel to remote locations, and many lonely, patient hours of observation, away from the comforts of home. The work is often left to doctoral students who are in no position to protest.
So it was 25 more years before evidence started to accumulate that could bear on the question, how many animals in the wild are dying from the (early) effects of aging?
In principle, it is not hard to determine an answer. Collect carcasses in the woods and use established forensic techniques to estimate the age of the animal when it died. Once you have enough cases, you can plot a curve: how many deaths? (on the y axis) vs what age? (on the x axis). For example:
How to interpret the results? If there were no aging in the wild, then we must expect that the percentage of individuals dying at every age is the same. But the number remaining gets smaller and smaller, so the absolute number of deaths would go down with age. The math tells you that “no aging” corresponds to a falling exponential curve.
If the number that we actually find is flat with age, or even if it declines with age but not as rapidly as an exponential curve, this is evidence that aging is taking a toll on fitness in the wild.
It was 1991 before Daniel Promislow first collected and interpreted the appropriate statistics for 56 different mammals in the wild. He was a doctoral student at Oxford, and this study launched his career. In 46 of the 56 species, he found an increasing risk of death with age. In several species, data were complete enough that he was able to detect a Gompertz curve, meaning that for a given individual, risk of death climbs exponentially with age.
The Gompertz shape of the mortality curve had been known for 150 years—nothing new there. The surprise was that previous to Promislow, scientists had thought that the Gompertz shape only applies in protected environments, like humans in civilization and animals in zoos. In the wild, it was expected that (according to Medawar) everyone dies too early to see the rising shape of the Gompertz curve.
The significance of these results was not lost on Promislow. He boldly asserted that his results conflicted with the accepted evolutionary theories for aging. He was also modest and tactful enough to allow for reasons that his conclusion might be premature, and that adjustments could be made to permit the evolutionary theories to hold their own.
The Evidence Piles on
In 1998, Robert Ricklefs expanded on Promislow’s results by including more mammal surveys and some birds. Ironically, he titled his piece Confirmation of a Fundamental Prediction, but in fact the results made all the extant theories for evolution of aging quite untenable. He fitted mortality curves for each of the species in the study, and reported parameters from these curves. From these data, it is a small further step to answer the question, What proportion of deaths in species can be ascribed to aging? Ricklefs set up the equations and provided all the parameters, but he never completed the calculation. Later, I filled in those numbers, the “percentage of senescent deaths” for each species. You can read them in the column highlighted in orange.
As you can see, there are no animals for which the impact of senescence in the wild is negligible. Many are clusted in the range 15-30%. Some are over 70% — meaning, roughly, aging is reducing fitness in these species by more than 2/3.
Heroic field work
All the above work is based on field studies, data compiled after the fact through searching for remains. But the cleanest kind of study would be an experiment, planned in advance, where individual animals could be tracked in the wild and their fates determined by direct observation. As a Canadian grad student in the early 2000s, Russell Bonduriansky set himself the daunting task of individually labeling, releasing, and recapturing thousands of antler flies to answer directly, how did their risk of death change with age? His doctoral work was stunning enough to be profiled in Nature. The result: 28% of antler fly deaths were due to aging.
Nature doesn’t care if you die once your fertility is gone
The numbers above present a dilemma for evolutionary theory. Scientists dealing loosely with this question sometimes say, animals die once their fertility is ended. It’s no surprise that evolution has permitted these animals to age and die once they have reproduced and replaced themselves. But the theory can’t escape so easily, for two reasons.
First, this doesn’t answer the question, but only kicks the can down the road. Yes, there is no selective advantage to be gained by continuing to live on past the end of fertility. But why should fertility decline in the first place? Why haven’t we all adopted the growth pattern of trees and lobsters, continuing to grow and produce more offspring with each passing year? (Or, if there are size constraints that keep land animals from growing forever, at least we should be maintaining our fertility, not losing it with age.)
Second, responding to the argument about “once they have replaced themselves”… We should note that this is a flat denial of the dominant “selfish gene” view of evolution. In standard evolutionary theory, there is no such thing as “enough”, because individuals are in an arms race to dominate the next generation with their genes. If I have 6 offspring and you have 7, it will not be very many generations before my descendants are completely crowded out by yours (according to the way standard evolutionary calculations are performed). This perspective highlights the evolutionary paradox that natural selection has tolerated declining fertility and increasing mortality in so many different animal species.
The bottom line
Sixty years after Medawar, it is untenable to maintain that aging exists in a “selection shadow”. The negative consequence of aging for individual fitness is a force to be reckoned with. But theorists have yet to face this particular monster. I still hear Medawar’s hypothesis cited as gospel regularly in papers and at conferences. The disconnect between theory and observation is stark.
- The idea of “late-acting genes” made sense in the 1950s when Medawar and Williams were formulating their theories, but we now know that all living things have extensive machinery (epigenetics) for deciding when to turn particular genes on and off. Williams imagined that if a gene is beneficial at one stage of life, we would be stuck with it at another stage, when it is detrimental. We now know that genes are routinely turned on and off as needed.
- The idea that fitness depends on maximizing the number of offspring is enshrined in standard evolutionary theory, which is the “selfish gene” model. But there are many ways we know this cannot be right. Producing too many offspring can be just as disastrous for a species as producing too few. This is the inspiration for my Demographic Theory of Aging.