In 1999, I met Cynthia Kenyon for the first time, and she told me her one-line proof that aging is an evolved trait. Lifespans in nature range from hours to thousands of years. This shows that natural selection is not constrained, but can implement aging on whatever time scale is appropriate.
A few years ago, Annette Baudisch added another dimension to this proof: It’s not only the duration of life, but the shape of the aging curve that takes on so many various forms. Misguided theories of aging are based on the human life cycle (and others like it) with Gompertz mortality. (In the 19th Century, Benjamin Gompertz first noted that risk of death increases exponentially with age.) Several smart theorists have been seduced into attempting proofs—either from thermodynamics or from evolution—that gradual aging is a necessary consequence of the conditions of life.
But Baudisch gathered data on hundreds of animals and plants, demonstrating that the exponential shape of the human mortality curve is just one among many possible. Furthermore, every conceivable shape is paired with every time scale. Any theory of aging must account for all these ways to age. Or not to age: Baudisch got her start in research collecting examples of negative senescence. Given this variety, the only viable theory is, “nature can do whatever she wants”. More formally, natural selection can mold aging as appropriate to fit every possible niche in every ecology.
Aging is ancient, but it is not universal. We are accustomed to think that animals age gradually beginning at maturity, ending with inevitable death, but life is stranger than this. Some animals and many plants have escaped from aging entirely. Many more pass through long periods of their lives without aging. Cicada nymphs mature underground for seventeen years, while not being subject to increasing death rates or aging in any other sense. Then the cicada emerges, mates, ages and dies all in a single day. This is a dramatic example of semelparity, in which aging occurs all in a rush after a single burst of reproduction. In many such cases, the aging can be experimentally decoupled from the reproduction, demonstrating once again that the aging is a separate adaptation. The simplest example of this is the pansies in your garden. As long as you snip off the flowers before they go to seed, you can keep the plant blooming all summer.
Many plants and animals die when they are done reproducing, as evolutionary theory predicts; but among those that long outlive their fertility, there are some (like C. elegans worms) that don’t tend to their children or grandchildren. What evolutionary force has provided for their continued life?
A few animals and many plants don’t age at all, but grow larger and stronger and more fertile through their entire lifespans. Some have been observed to regress from mature states, and start life anew as larvae, with a full life expectancy ahead of them.
What does life without aging look like?
Sanicula is a shrub growing in the meadows of Sweden, and one plot in particular has been studied continuously for seventy years. Sanicula has a life expectancy comparable to a human, but sanicula does not age. For people, the probability of dying gets higher with each passing year, whereas for sanicula, about one shrub in 75 dies each year, irrespective of age. A 75-year-old plant has no more mortality risk than a 10-year-old plant. For a person, the life expectancy at birth might be 75 years; the life expectancy for someone 60 years of age might be 18 more years, and for someone 80 years old, perhaps the life expectancy is 7 more years. For a sanicula, the life expectancy of a seedling is 75 years, and the life expectancy of a 60-year-old shrub is 75 more years. There are, in fact, a few 200-year-old saniculas, and they have a life expectancy of 75 more years. At this rate, about one plant in a million should live a thousand years. A thousand-year-old sanicula is no closer to death than a sapling.
It is unknown today whether lobsters age or not. Lobsters are fished so heavily that they rarely grow larger than a pound, but lobsters weighing more than 5 lbs are still caught occasionally (and usually released). The largest lobster on record was 44 lbs. The reason that the large lobsters are released back into the ocean is not just that they won’t fit on a dinner plate. Lobsters become more fertile as they grow larger, and their young are more viable. A few large lobsters can be the breeding stock for a large area. We don’t have an age record for the oldest lobster ever caught because lobsters don’t have annual rings or layers that broadcast their age. The 44-lb animal was said to be more than one hundred years old, but no one knows for sure.
Clams also can grow larger and more fertile indefinitely. But clams have growth rings that count the years for us. The oldest clam on record (an ocean quahog of the species Arctica islandica) has been tagged at 507 years. Small clams have natural predators, including starfish that latch onto their shells and pull them apart by brute force. But once a clam outgrows the arms of a starfish, it can keep growing indefinitely. Clams have one foot, one mouth, no eyes or ears or stomach, no brain. Giant clams, up to 800 lbs, live the same lifestyle as their smaller relatives, sucking in the seawater, taking in thirty thousand times their weight in water every day, and filtering out plankton and algae, which continue to grow and reproduce inside them. Like giant lobsters, the giant clams provide eggs for a whole community. They have been known to release half a billion eggs in a day.
All of the longest-living species in the world are trees. There are several reasons for this. Trees invest a great deal in growth, always trying to project their leaves upward, out of the shade of other trees, to compete for the best light. The oldest trees tower above the forest, and get first dibs at the sun’s energy. So there is a powerful evolutionary incentive for trees to live a long time so they can grow taller than their competitors, and the sky is the limit.
As opposed to plants, animals’ life spans are limited by a requirement of ecological stability. Most plants produce their own food, but all animals depend on other species (either animals or plants) for their food. Hence it is natural for a plant to live as long as possible and make as many seeds as it can make. Trees are the best examples of Darwin’s dictate that life is about reproduction. (Sequoia trees can produce more than a billion seeds.) But animals can’t get away with reproducing faster than the plants at the base of the food chain. Animals are evolved to guard the species lower down on the food chain, and they must never reproduces faster than the animals they eat—otherwise, in a very few generations, they will wipe out their food source and their children will starve.
Do trees age at all? Some do, and some don’t. Most trees go for long periods of time growing ever larger and less vulnerable to death. That counts as negative senescence. Of course, size itself becomes a hazard as a tree becomes the tallest in its grove—the first to be struck by lightning, the most top-heavy and vulnerable to toppling in the wind when erosion weakens the roots’ hold on terra firma. But in addition to this, it seems that most trees have a characteristic age, after which death finally becomes more likely with each passing year. There is some indication that trees become more vulnerable to fungus and disease with old age, but for the most part, old trees succumb to the mechanical hazards of excess size. The very ability to continue growing that offers them the possibility of “reverse aging” over so many decades proves in the end to be their downfall.
Instant Ageing; Sudden Death
Semelparous animals and plants reproduce just once in a lifetime, usually followed promptly by death. Sudden post-reproductive death is common in nature, affecting organisms as varied as mayflies, octopuses, and salmon, not to mention thousands of annual flowering plants.
The cause of death in semelparous organisms varies widely. Theorists once assumed that the animal just wears itself out in a burst of reproductive effort, but this idea has not held up. The burst of reproduction and the sudden death seem to be separable and independent adaptations. In addition to the example of pansies mentioned above, octopuses can be induced to live beyond their burst of reproduction if their optic gland is surgically removed; and Atlantic salmon, close cousins of the Pacific salmon, also endure treacherous migrations upstream in order to mate, but they don’t necessarily die after laying eggs, and can return to the ocean for another bite at the apple.
Chinook salmon hatch in river pools, often hundreds of miles upstream from the sea. They spend their first year or two in the protected environment of the river, where life is tamer and larger predators rarer. When they have grown large enough to compete, they migrate downriver, out to the ocean to seek their fortunes. They may range up to 2,500 miles from the mouth of the stream where they first entered the sea. They live in the ocean anywhere from two to seven years, growing larger but not weakening or becoming frail with age. When they are ready to reproduce, they find their way back, not to any handy river mouth but to the very same river pool where they were hatched. Their journey is a headlong rush, simultaneously into fertility and death.
By the time the adult salmon reach their spawning ground, their metabolisms are in terminal collapse. Their adrenal glands are pumping out steroids (glucocorticoids) that cause accelerated—almost instant—aging. They’ve stopped eating. Moreover, the steroids have caused their immune systems to collapse, so their bodies are covered with fungal infections. Kidneys atrophy, while the adjacent cells (called interregnal cells, associated with the steroids) become greatly enlarged. The circulatory systems of the rapidly deteriorating fish are also affected. Their arteries develop lesions that, interestingly, appear akin to those responsible for heart disease in ageing humans. The swim upstream is arduous, but it is not the mechanical beating that fatally damages their bodies. It is rather a cascade of nasty biochemical changes, genetically timed to follow on the heels of spawning. The symptoms affect both males and females, despite the uneven share of metabolic work that falls to females, whose eggs may constitute a third of their body mass during the final leg of their trip.
Some organisms are genetically programmed not to eat after reproduction and starve as a result; it’s quicker and surer than traditional ageing. Mayflies entering adulthood have no mouth or digestive system whatever. Elephants chomp and grind so many stalks and leaves during a lifetime that they wear out six full sets of molars. But when the sixth set is gone, they won’t grow another, so old elephants can starve to death.
Praying mantis males take the prize for the most bizarre and macabre mode of programmed death. After an elaborate mating ritual, the male fertilizes his mate’s eggs with his bottom half, while the female chomps off his top half. Sometimes.
Octopuses makes an especially good story. They live a short time, a few months to a few years, depending on the species, and they die after reproducing once. After mating, the female guards and cares for her eggs, but if conditions are not right for her brood, she may eat them, and then she has another chance to try again later. Like praying mantisses, the octopus female sometimes cannibalizes the male. If she decides the time is right to deliver her young, not only does she refrain from eating her eggs, she stops eating altogether. The octopus mom guards her eggs from predators, focused and immobile for months on end. (They are such smart animals, even playful. How is it that they don’t get bored?) During this time, her mouth seals over. She may live for years in this state of suspended animation, just guarding her eggs; but when the eggs hatch, she dies within a few days. Her death isn’t from starvation. We know because there are two endocrine glands, called “optic glands” though they are unrelated to the eyes, whose secretions control mating behaviour, maternal care, and death. The optic glands can be surgically removed, and the octopus mom lives longer. If just one optic gland is removed, the female doesn’t eat but still lives an extra six weeks. If both optic glands are removed, then the octopus doesn’t lose her mouth and resumes eating after the eggs hatch. She then regains strength and size and can live up to forty weeks more.
In 2007, Bruce Robison of the Monterey Bay Aquarium Research Institute discovered a deep-sea octopus mom watching over her clutch of 160 eggs in the deep, cold waters off the California coast. He returned periodically to observe the same octopus on the same rock in the same position. From 2007 to 2011, she didn’t eat, and she didn’t move except to slowly circulate the water over the eggs, assuring a fresh supply of mineral nutrients. After four and a half years, the eggs hatched, and the octopus mom disappeared, presumed dead, all within a few days. The empty eggshells were observed, memorializing her effort. It was the longest gestation ever observed.
Ageing in Reverse
In 1905, the Dutch biologist Friederich Stoppenbrink was studying the life cycles of Planaria, a kind of flatworm, a fraction of an inch long, common in freshwater ponds. He noted that when the animals didn’t have enough to eat, they systematically consumed themselves, beginning with the most expendable organs (sex), proceeding to the digestive system (not much use in a famine), and then muscles. The worms got smaller and smaller until the most precious part—the brain and nerve cells—were all that remained. Stoppenbrink reported that when he started to feed the worms again, they grew back, rapidly regenerating everything they had lost. What’s more, they looked and acted like young worms, and when their cohorts who had not been starved began to die of old age, the starved-and-regrown worms were still alive and kicking. This trick could be performed again and again. As long as Stoppenbrink kept starving and refeeding the worms, they went on living without apparent signs of age.
The medusoid Turritopsis nutricula achieved its fifteen minutes of fame when it was hailed as “the immortal jellyfish” in science news articles of 2010. The adult Turritopsis has inherited a neat trick: after spawning its polyps, it regresses back to a polyp, beginning its life anew. This is accomplished by turning adult cells back into stem cells, going against the usual developmental direction from stem cells to differentiated cells—in essence driving backward down a one-way developmental street. Headlines called Turritopsis the “Benjamin Button of the Sea.” Here again, life seems to imitate art.
Carrion beetles (Trogoderma glabrum) perform a similar trick, but only when starved. As they play life out on a carcass in the woods, the beetles go through six different larval stages in succession, looking like a grub, and then a millipede, and then a water glider before ending up as a six-legged beetle. A pair of entomologists working at the University of Wisconsin in 1972 isolated the sixth-stage larvae (when they were just ready to become adults) in test tubes and discovered that without food, they regressed to stage-five larvae. If they were deprived of food for many days, they would actually shrink and regress backward through the stages until they looked like newly hatched maggots. Then, if feeding was resumed, they would go forward again through the developmental stages and become adults with normal life spans. They found they were able to repeat the cycle over and over again, allowing them to grow to stage six and then starving them back down to stage one, thereby extending their life spans from eight weeks to more than two years.
Hydras are radially symmetrical invertebrates, each with a mouth on a stalk, surrounded by tentacles, which grow back when cut off—like the many-headed monster of Greek mythology for which they are named. With their tentacles, they snare “water fleas” and other tiny crustaceans, on which they feed. Some hydras are green, fed by symbiotic algae living beneath their translucent skin.Hydras have been studied for four years at a time, starting with specimens of various ages collected in the wild, and they don’t seem to die on their own or to become more vulnerable to predators or disease. In the human body, certain cells, such as blood cells, skin, and those of the stomach lining, slough off and regenerate continuously. The hydra’s whole body is like this, regenerating itself from stem cell bedrock every few days. Some cells slough off and die; others, when large enough, grow into hydra clones that bud from the stalk-body to strike out on their own. This is an ancient style of reproduction, making do without sex. For the hydra, sex is optional—an occasional indulgence.
One recent article claims that the hydra does indeed grow older, and it shows it by slowing its rate of cloning. The author suggests that perhaps clones inherit their parents’ age. The hypothesis is that only sexual reproduction resets the ageing clock. If this is true, then the hydra’s style of ageing is a throwback to protists, ancestral microbes more complex than bacteria. Amoebas and microbes of the genus Paramecium are examples of these protists, single cells in a vast lineage that has anciently radiated into over one hundred thousand species and includes all the seaweeds, slime moulds, and ciliates and other organisms that do not belong to the animal, fungal, plant, or bacteria kingdoms.
For paramecium, sex and reproduction are two entirely different functions. Reproduction takes place by simple mitosis—the cell clones itself. Sex takes place by “conjugation”. The paramecium sidles up to another paramecium, their two cells merge and then the two cell nuclei merge, mixing their DNA, reshuffling within each chromosome, as genes cross over from one to the other. Then the two cells separate, but the two cells that come apart are not the two cells that entered. Each one is a different combination of the two original cells—“half me and half you.”
Here is the connection to aging: Cells keep track of how many times they have cloned themselves via telomere length. Each time the cell clones itself, the telomeres becomes a little shorter. When it becomes too short, the cell languishes and dies. The telomere can be re-set to full length with the enzyme telomerase, but this only happens during conjugation, not during mitosis. The result of withholding telomerase is that the individual can clone itself about a hundred times, but at some point, it must share its genes via conjugation, giving up its individual identity. Telomere shortening is an ancient mode of aging that forces the individual to share genes with the community.
This ancient process was a template for the future evolution of aging. Many higher organisms have telomeres that shorten through our lifetimes, until we die. Telomerase is held back in humans, dogs and horses, but not pigs, mice or cows. In the former animals, telomeres are only reset during reproduction, when a new individual is formed from gamete cells of two different parents. Just like paramecia.
Bees That Can Turn Ageing Off
Queen bees and worker bees have the same genes but very different life spans. In the case of the queen bee, royal jelly switches off ageing. When a new hive begins, nurse bees select—arbitrarily so far as we can tell—one larva to be feted with the liquid diet of royalty. Some physiologically active chemical ambrosia in the royal jelly triggers the lucky bee to grow into a queen instead of a worker. The royal jelly confers upon the queen the overdeveloped gonads that give her a distinctive size and shape. The queen makes one flight at the beginning of her career, during which she might mate with a dozen different drones, storing their sperm for years to come.
Weighted down with eggs and too heavy to fly, the full-grown queen becomes a reproducing machine: she lays at a prodigious rate of about two thousand per day, more than her entire body weight. Of course, such reproductive regality requires a suite of specialized workers to feed her, remove her waste, and transmit her pheromones (chemical signals) to the rest of the hive.
Worker bees live but a few weeks and then die of old age. And they don’t just wear out from broken body parts, the rough-and-tumble worlds through which they fly. We know this because their survival follows a familiar mathematical form, called the Gompertz Curve, which is a well-known signature of biological aging. Meanwhile, queen bees, though their genes are identical to those of the workers, show no symptoms of senescence. They can live and lay for years and sometimes, if the hive is healthy and stable, for decades. They are ageless wonders. The queen dies only after running out of the sperm she received during her nuptial flight. At that point, she may continue to lay eggs, but they come out unfertilized and can only grow into stingless drones. Then, the same workers that formerly attended her assassinate the depleted queen. They swarm about her, stinging her to death.
What does it all mean?
Styles and durations of aging in nature are just about as diverse as they can be. Aging doesn’t have to exist at all, and individual fitness would be 20-30% higher in most cases if aging just took a walk. Where mother nature has tempered reproduction and kept aging in the life cycle, it is for the purpose of stabilizing the ecosystem, preventing population overshoot that can lead to extinction. This theory accounts for some broad facts about aging in nature:
- that aging is near universal in animals, but not necessarily in plants,
- that aging slows down when animals are starved (no extra curtailment of life is needed in a famine)
- that animals can substantially outlive their fertility
- that predator lifetimes are generally longer than their prey
- that the genetic basis for aging has been preserved over hundreds of millions of years