I study evolution of aging because I think it is a scientific conundrum. But frequently, people tell me that the evolution of aging is easy to understand. After the individual is done reproducing, its job is finished, and there is no more evolutionary force to keep it alive. It can be pushed over with a feather (if natural selection had feathers to push with).
It’s not just naive people who make this statement. People who should know better sometimes say the same thing. I have heard this explanation from the mouth of a Nobel laureate in medicine.
The reasoning is correct, of course, but the problem is that it begs the question, how did the loss of fertility evolve? Sure, it’s true that once the individual has lost the capacity to reproduce (and is no longer caring for its offspring) there is no evolutionary reason for it to remain alive. But why, in the first place, does evolution put up with the loss of fertility? Why aren’t we all like oak trees that grow larger, stronger and more fertile with every passing year?
The mystery is not that we die after we lose our fertility; the mystery is why natural selection has permitted us to lose our fertility.
Semelparous organisms are those that have evolved to reproduce in one big burst. All of them, to my knowledge, are also evolved to die promptly after reproduction. Familiar examples include Pacific salmon, the octopus, many insects and annual plants. Usually, it is clear that death is internally orchestrated, triggered by hormonal signals, behaviors and anatomical changes. Mayflies, gnats and cicadas have no mouths or digestive capacity as adults. Octopus mothers stop eating and starve to death. Salmon poison themselves with steroid hormones. Pansies shrivel up as soon as they “go to seed”, but you can keep them alive all summer as long as you remember to clip off the flowers when they begin to wilt.
Evolutionary biologists thought they had a good understanding of this dynamic, with the exception of human females. Women lose their fertility in their thirties or forties, but can go on to live into their seventies or eighties. What was evolution thinking, in cutting off female fertility? In classical neo-Darwinian thinking, fitness is maximized by natural selection. There’s no such thing as “enough offspring—ok to stop now,” because if someone else has genes that permit more reproduction, then those genes will be the ones that spread through the next generation and grow to dominate the gene pool. Perhaps there is some physiological limit, and nature has tried and tried to extend female fertility, but it’s just a difficult problem… But that’s just not plausible. Women are born with millions of eggs, but over the course of a lifetime, only a few hundred ripen and descend the fallopian tube where they might be fertilized. The rest die in a process called atresia, akin to programmed cell death. Perhaps the eggs just become damaged over time, and they can no longer develop into a viable foetus. It is true that birth defects increase with a woman’s age, but this hardly seems to be a hard-and-fast physiological limit.
The explanation that was offered until a few years ago was the grandmother hypothesis. Perhaps a woman in her 50s can contribute more to her genetic legacy by helping out rearing her grandchildren. Perhaps infertility frees her from raising new babies of her own, so that she can devote full time to grandmothering, and in this way the number of surviving grandchildren is actually increased over what it would be if she remained fertile for an extra decade or two.
The Grandmother Hypothesis was never so plausible on its face, but it survived by default, having no competition. But a few years ago, some Exeter University researchers did a computation confirming what should have been obvious: If your goal is to have as many children as possible, cutting off your fertility is not a good choice. New children to whom you might be able to give birth if you carry on will all bear your gene, whereas grandchildren have only a 1 in 2 chance of carrying the gene, and you can only indirectly help their survival. Michael Cant and Rufus Johnstone estimated the net cost of menopause with real survival statistics from several primitive human cultures, and it wasn’t even close.
There’s more. Humans are not the only animals to lose their fertility and go on living, as it turns out. Whales and elephants are social mammals, and you might imagine that the grandmother hypothesis applies to them. But birds don’t care for their grandchildren, and several kinds of fowl become infertile long before they die. Fish don’t even care for their children, and post-reproductive life has been discovered in guppies.
Lab worms, C. elegans quite drive the point home as they are hermaphrodites, born with more eggs than sperm. They simply run out of sperm, and stop reproducing after about 4 days, but they can go on to live for 10 days. This is a striking example of “programmed death” because sperm is an itty-bitty, stripped-down cell. Metabolically, the cost of producing sperm is negligible, even for a creature 1/10 mm long. So running out of sperm while there are still plenty of eggs to be fertilized can only be seen as a purposeful curtailment of fertility.
Measuring life span and fertility in the wild is not so easy, and to date there are only a dozen or so examples. But wherever they look, field biologists are finding post-reproductive life span.
This is indeed a mystery. If natural selection is optimizing something called “fitness” which depends most directly on the number of offspring left by an individual, why is fertility being curtailed? If there are resources that could be invested in reproduction or traded in for chips that help to keep the body in good repair, then why are so many chips mis-invested in longevity, when fertility would pay a dividend, and longevity, none?
A couple of years ago, Charles Goodnight and I proposed a solution to this conundrum, but it comes at a steep price. We left behind the neo-Darwinian framework in which maximizing fertility is the essence of fitness. We offered an answer in terms of the Demographic Theory of Senescence. This is a theory that says that nature does not maximize individual fitness only, but also concerns herself with stable and robust communities. The key point is that for animals (but not plants), over-consumption and over-population are ever-present, looming threats to the community. It is all too easy to “win” the game of reproducing, using a strategy of beggar-thy-neighbor. Animals in an area share a communal pool of food, and the easy way to reproduce more is to eat more, to gather more biomass and convert it to babies. This strategy offers a very short-lived victory, because once the food species is depleted, it may take many generations to grow back.
I may have more children than you, and get more of my genes into the gene pool of the next generation. But the result is that my children are greedy, like me, and there are more of them, and it doesn’t take long before they outgrow the food supply that was once sufficient to support our community, and everyone starves.
The classical wisdom is that this is a form of “group selection”, and it’s bound to be slow and inefficient compared to “individual selection”. But as Michael Gilpin first demonstrated 40 years ago, population overshoot can be the basis of a swift and lethal form of group selection. With judicious use of computer modeling and careful mathematical logic, he demonstrated that, in this case, it is easy to understand how group selection tempers individual selection.
The radical conclusion of Gilpin is that, in animals, reproduction can never be maximized without destroying the population. This undermines the assumption at the foundation of classical neo-Darwinism, and introduces a new, more communal picture of how evolution works.
It was in the context of this picture that Charles and I were able to demonstrate the evolutionary benefit of post-reproductive life span. Sustainability is a target of natural selection. The goal is to stabilize populations in good times and bad, to avoid population overshoot that leads to collapse and extinction. The mechanism of natural selection couldn’t be clearer: communities that are not sustainable collapse to extinction.
How does post-reproductive life span help? An infertile, older population acts as a kind of buffer during times when the population might otherwise be expanding too fast. When there is plenty of food, the post-reproductive segment eats some of it, but they do not add to population growth in the next generation. Then, when times become more difficult and food is scarce, the older, weaker segment of the population is the first to die off, and this is no real loss to the population’s reproductive potential.
Remember, all this works in animals but not plants. In fact, post-reproductive lifespan is not found in plants, and indeed most plants appear to follow the expectations of neo-Darwinian theory far more closely than animals; which is to say that plants do appear to be maximizing their reproduction, while animals do not.
This demographic perspective may or may not be the solution to the conundrum of post-reproductive life span. Clearly it doesn’t explain everything–for example, why do pansies die promptly after they go to seed? But at present the Demographic Theory has few competitors, and we think it is a good beginning, and should be a fruitful basis for exploring a new understanding of evolution’s basic machinery.
More details of the Demographic Theory of Aging in my blog post from last year. Here is a link to the journal article by Mitteldorf and Goodnight.