Love Don’t Cost Aging
On why aging is not a penalty for reproduction
“My love don’t cost a thing.”
—Jennifer Lopez
A long-standing hypothesis about aging suggests that it stems from an inherent biophysical limitation that demands the allocation of an organism’s resources between reproduction and longevity, inevitably leading to a trade-off between the two. This notion is based on the belief that some vital resource is never sufficiently abundant to fully support both objectives at once, and so organisms have to balance between extending their lifespan or reproducing more abundantly.
However, advocates of this concept fail to clearly define these essential resources. Are we talking food? Water? Oxygen? No, they concede, external resources like these cannot be the limiting factor; instead, the problem arises when these external resources get converted into internal resources, which then require the aforementioned trade-off that ultimately leads to aging.
I won’t dwell on this for too long; let me state upfront that this hypothesis of limited resources has been debunked numerous times. The most obvious way to test it experimentally was to take animals and selectively breed long-lived ones, expecting their fertility to decrease as they allocate more resources to longevity. Which is exactly what was done in this work. In violation of the trade-off hypothesis, the experiments showed that flies which began to live longer also began to breed more — both their early and overall fertility increased:
Similar results were found in other studies on various types of flies. For example, in this work, researchers analyzed a thousand Mediterranean fruit flies and found no correlation between fertility and longevity:
An unexpected result in the study was the complete absence of any relationship of early reproduction to either subsequent reproduction or to future life expectancy. This was surprising because, according to Roff (19), conventional life history theory holds that because egg laying is stressful and requires a major expenditure of energy, females that are reproductively active at young ages should be more frail and less fecund at older ages than females that were reproductively less active at young ages. Based on this reasoning, this weakening effect should be manifested as either decreased fecundity at later ages or as increased mortality (i.e., demographic cost of reproduction; see refs. 20–22).
The graph below from this work clearly shows how a prolific breeder (65 eggs per day at the peak on day 10 and 2000 eggs in a lifetime) and a mediocre breeder (25 eggs per day at the peak on day 10 and 500 eggs in a lifetime) have pretty much the same lifespan:
The graph above is a 2D slice from an even cooler 3D graph:
The authors did not stop there and next studied reproduction patterns in another 500 flies, confirming the absence of a trade-off between fertility and lifespan:
…our findings do not support the idea that there is a direct cost of reproduction. The link between mortality and reproduction is carried by the dynamics of reproduction and not by the absolute magnitude of reproduction, as measured in the number of eggs produced. For example, a high reproduction rate with slowly declining reproductive potential is associated with a longer life span according to our findings. In contrast, the classical cost-of-reproduction hypothesis would associate high reproduction rates with shortened life spans.
The only correlation between lifespan and reproduction that they observed was the correlation between the rate of decline in reproduction and aging: the faster the relative (not absolute!) fertility falls, the earlier the flies died. It did not matter when a fly began to breed or what its average egg laying rate was. The only thing that correlated with lifespan was the rate of decline in its fertility. The researchers went on to conclude that it looks like the flies had a sort of a reproduction clock that ticked at a certain speed proportional to the rate of aging of the body — i.e. those who aged faster lost fertility faster:
In particular, our analysis provides a detailed description of the nature of the linkage between the dynamics of the reproductive trajectory and subsequent mortality. We have established the primacy of the rate of reproductive decline over absolute levels of reproduction regarding this link. It is quite amazing that, based solely on knowledge of early reproductive patterns, our approach allows a reasonable prediction of the increase in subsequent death rates at the level of the individual. A possible interpretation of this finding is that the rate of reproductive decline is a good indicator of the speed of aging of an organism. In this sense, the reproductive clock is synchronized with an individual’s biological age as contrasted to chronological age.
Next, one of the above coauthors, James Carey, conducted another study on fruit flies where he also showed that there is no negative relationship between fertility and life expectancy:
To find out which parameters are associated with longevity, we take the most long-lived Drosophila, which are in the 10th cluster of flies. It is surprising that these long-lived flies do not differ from the rest of the population in their reproductive capacity, RC (60.3 ± 5.5 vs 60.47 ± 4.3 eggs/day), or in the length of their maturity stage, T (14.3 ± 3.6 vs 13 ± 4.2 days).
…
We can see that, indeed, neither RC nor T is related to prolongation of life span in Drosophila. Only the exponent α-sen is clearly related to prolong senescence. The smaller this exponent is, the slower is the decrease in egg-laying after the onset of senescence, and the longer is life span. The maturity period and the reproductive capacity tend to be constant in all clusters. This means that longevity in Drosophila is associated only with the rate of senescence.
Below is a clear demonstration that the fertility is actually higher in longer-lived flies. The graphs show the dynamics of egg laying in flies with very different lifespans — ranging from 20 to 60 days, and we see that the longer living flies were also the most prolific:
One would think that by now the absence of a trade-off in flies was clear, but, alas, the Lord of the Flies, James Carey, has not yet had enough! He went on to study Mexican flies and yet again showed the absence of a connection between fertility and longevity:
[K]nowledge of early egg laying provides no information for predicting either remaining life span or the number of eggs laid during the subsequent one-month period. Thus, at the level of the individual in non-manipulative studies such as the current one, there appears to be no obvious cost of reproduction.
Ok, enough about flies — let’s look at other insects. Namely, social insects: ants, termites, bees, etc. They don’t just undermine the trade-off hypothesis, they turn it on its head completely! Social insects have queens who live 10–20 times longer than their non-breeding identical twins, while laying thousands of eggs per day. In honeybees, for example, the queens can lay their own weight in eggs per day, and yet they live for up to 8 years, while the workers live for a few weeks in the summer of a few months if they get to stick around the hive for overwintering.
A similar trend holds in ants, including the ant species that holds the lifespan record for insects — the black garden ant — whose queens are known to live for ~30 years, a lifespan unattainable even for most species of mammals:
Another interesting lifespan factoid about these black garden ants is that their worker lifespan seems to get shorter as the colony grows — and we’re talking a sizeable 1.5x decrease in median lifespan — which could be a possible population control mechanism for the colony:
The curious case of Indian jumping ants (Harpegnathos saltator) offers another compelling argument against the trade-off hypothesis. These ants have a special social role called “gamergate” reserved for worker ants that can take on a reproductive role in the absence of a queen. In these species, queens live for about 5 years, whereas workers have a much shorter lifespan of ~7 months. But if a queen dies or is removed, some workers morph into gamergates — pseudo-queens that engage in duels for dominance. The triumphant gamergates collectively assume the queen’s egg-laying duties, and their lifespans skyrockets to 3–4 years:
This further refutes the idea that there’s an inherent “resource” allocated at birth, as some could have argued is done for queens. Because for a worker ant to become a breeder would logically consume more of that inborn “resource,” but in actuality such a transformation results in a marked lifespan extension. So this observation further debunks the notion of an inherent trade-off between reproduction and longevity. Oh, and if a gamergate is moved to a colony with an active queen, it stops breeding and reverts to a worker, with the requisite shrinkage in lifespan. Life’s twists and turns can be so cruel.
Another refutation of the trade-off hypothesis comes from the Monarch butterfly. In the summer, Monarch adults live for only a few weeks, but in the fall they migrate south for wintering, and such migrants can live for up to 9 months. Moreover, not only do these migrants first have to fly for thousands of miles to Mexico, and only then mate in the following spring, but then the females have to make the return journey while pregnant. Talk about the disparity in the “life force resource” between the summer and winter individuals!
Intriguingly, a single JH1 hormone from the family of juvenile hormones seems to play a key role in the disparity in lifespan between migrants and non-migrants in Monarchs. When it is introduced to butterflies under laboratory conditions, they live 2x shorter, but if, on the contrary, its production is blocked, then the butterflies live 1.5x longer. The graphs below show the resulting 3x difference in median life expectancy between those who received additional JH1 (blue curves) and those in whom its production was blocked (red). Top row is females, bottom row — males.
By the way, juvenile hormones are responsible for regulating development in many insect species, including social insects. For example, they were shown to determine social roles in bees during development.
Speaking of social animals, it is not only social insects that display this “anti-trade-off” disparity where reproduction actually prolongs lifespan, but some social mammals as well. In particular, the longest-lived naked mole rat who was 39 years old in 2021 (hopefully, he is still alive!) is a breeding male, and generally breeders have lower mortality risk than non-breeders:
Also, in a close relative of naked mole rats, another social African rodent, Ansell’s mole rat, both male and female breeders have considerably longer lifespans than their non-breeding counterparts:
While we’re on the topic of interesting mammalian species, there is one that has a curious seasonal lifespan disparity highly reminiscent of Monarch butterflies — the Montane vole (Microtus montanus). If it is born in the spring, it quickly matures (within 3–4 weeks), breeds, and dies in the same year. But if it is born in the fall, then just like in Monarch butterflies, its reproductive ability is put on pause until the next spring, which greatly increases its lifespan:
If all of the observations above haven’t yet been convincing, here is a study in which the authors surveyed 12 species of birds and 17 species of mammals living in zoos, and also concluded that there is no reason to believe that early or general fertility negatively affects life expectancy.
Moreover, further counterevidence to the trade-off hypothesis is provided by turtles, in whom fertility only increases with age, as it does in rabbits:
There are yet more species that are characterized by an increase in fertility (the thick line in the graph below) with age:
Finally, human females also do not seem to have any negative effects from childbearing on their lifespan:
So Jennifer Lopez was right — truly, love don’t cost a thing.
