Aging as Phenoptotic Phenomenon
The concept of phenoptosis, or genome-programmed organism death, was first proposed by one of us (V.P.S.) in 1997 (Skulachev 1997). Phenoptosis is a death program which is encoded in the genome of a dying creature. It is composed as a chain of biochemical events that ultimately cause self-destruction of organism (like apoptosis, programmed death of the cell). Less commonly, such a death results from a behavioral response encoded in the genome of the dying individual, its sexual partner, a close relative of the victim or its partners in the ecosystem. (Libertini 2012a, b; Skulachev 2012). Within this concept, the aging starts as a slow (chronic) phenoptosis, i.e., the process of death of an organism stretched over a considerable period of time (Skulachev 2003).
Overview and Key Findings
Aging starts long before it becomes a direct cause for a death of an individual. At the same time, it can indirectly facilitate its death. For instance, the weakening of the organism that progresses with age undoubtedly increases the probability of death due to attack by predators, pathogens, etc. Loison et al. (1999) and independently R. Bonduryansky and K. Brassil (Bonduriansky and Brassil 2002) directly demonstrated that under natural conditions both long-lived mammals and short-lived insects suffer from aging. Such a result is not surprising if we take into account the fact that, for example, the reduction in the muscle strength with age begins relatively early – when growth of the organism is completed – and the aging of the immune system even earlier (in humans, between 10 and 15 years of age) (Skulachev et al. 2013). According to the data provided by R. Ricklefs (1998), the analysis of the skeletons of mammals and birds of various species, found after their death in the wild, suggests that the percentage of the dead animals with the signs of aging varies from 10% in rabbits and squirrels to 80% in sables and to 90% of female swans.
There are two mandatory features that help easily distinguish the slow programmed aging from other body wear phenomena. First, this program causes a gradual weakening of many key functions of a living being, while a sudden drop of a single vital function is sufficient enough for death. Secondly, it is a coordinated weakening of various functions; otherwise the organism would quickly fall into acute phenoptosis.
The main biological purpose of slow phenoptosis is associated with the acceleration of evolution. The youngest and most numerous and effectively breeding part of the population guarantees the stability of everything that has already been achieved by evolution. At the same time, the aging part of the population can afford to change the genotype somewhat, thereby initiating the selection of some new property. If this property is really useful, it will be fixed in the offspring. If the new trait has adverse side effects that are potentially destructive for the species, the trait will not pass the selection, and the experiment itself is unlikely to have serious consequences for the species, since there are not so many old individuals, they do not breed as actively as the young ones do, and soon they will simply die out. Thus, it turns out that young are mainly responsible for the conservatism of heredity, and the aging ones are responsible for its variability. The latter is facilitated by the fact that mutations (the basis of the variability of living organisms) accumulate with age.
Such an evolutionary strategy resembles one feature of the sexual dimorphism of many bird species, where the female is unimposing, voiceless, and not at all inclined to “stick out” (“a conservator”), while the male is motley, vocal, and active, as if exposing itself in dangerous situations (“a revolutionist”) (Zahavi 1975).
Increase in the diversity of individuals in the population may serve as another function of aging as a mechanism contributing to the evolutionary process. The aging leads to a change in the properties of the organism, which develops at somewhat different speeds in different individuals, thus inevitably resulting in the divergence of the age-dependent signs.
Mitteldorf (Mitteldorf 2016; Mitteldorf and Wilson 2000) points out to another possible function of aging – creation of a cohort of weaker organisms that play the role of a “demographic buffer” in adverse conditions. The older ones (as weaker and inferior to the younger ones in their reproductive abilities) will be the first to take the blow of the worsening conditions (e.g., the appearance of a new enemy), for some time defending the healthy, strong, and faster breeding core of the population.
There are some indications that during aging, chronic phenoptosis can be transformed to acute phenoptosis, a fast biochemical suicide immediately killing an old organism which, due to aging, loses the ability to reproduce progeny, to fight enemies (including pathogens), and to participate in a work helpful for community. However, they still consume a food. At this stage of existence, an individual becomes undesirable for population and should be eliminated as soon as possible. An acute phenoptosis is the simplest way to solve the problem. Sepsis shock seems to be a case of such phenoptosis purifying population from badly infected individuals able to initiate epidemic (Skulachev 2002).
The successful evolution of a species cannot be imagined without the “coevolution” of other species of the same ecosystem. Mitteldorf (Mitteldorf 2016; Mitteldorf and Wilson 2000) provides the example of the locust of the Rocky Mountains (Melanopsis spretus) as an example of a tragic situation when the interests of partners in the ecosystem are being violated. In 1874, the area affected by this insect species was about half a million square kilometers (i.e., of the same order as the area of all of California). After the locust there was nothing green left over the entire giant territory, and the soil was covered with a layer of eggs ready to give a new generation of voracious insects the following year. However, this generation had nothing to eat, and it all died out. Its death occurred, as the author writes, not because the locust individuals were not sufficiently “adapted.” It happened because these individuals were too aggressive and too prolific. Long-lived birds (penguins, alcidae, condors, vultures, eagles, albatrosses) that lay only one egg can serve as examples of moderation and consideration of the interests of other ecosystem members. If this single egg is broken, the bird lays another one, but never two at once (Mitteldorf 2016; Mitteldorf and Wilson 2000). According to anthropologist A.A. Carr-Saunders (Carr-Saunders 1922), populations of primitive hunters that have maintained their numbers for thousands of years used several methods for the limitation of the growth of their population: from abortion to the killing of newborns. As Mitteldorf writes, it is impossible to create a stable ecosystem from the species, where individuals seek to grab as much as they can drag, and reproduce as quickly as they can (Mitteldorf 2016). M.E. Gilpin in his book describes the cases when the evolution of predators in an ecosystem is organized in such a way as to protect the victims from complete extermination by these predators (Gilpin 1975).
Figure 1b illustrates another example of the same natural phenomenon but with the other participants. Antelopes play the role of “patients” with the leopard being the “surgeon.” The photograph shows how the herd of antelopes calmly goes along its way and a leopard making its way to the rear guard of the herd at a walking pace. In both cases shown in the photographs, we are apparently dealing with the most complicated case of senile phenoptosis where the suicide program-encoding genes are distributed between two types of organisms – predators and their victims (Skulachev et al. 2013).
So, the majority of live species (Homo sapiens included) have a suicide program. One of the manifestations of this program is aging which is necessary for acceleration of the evolution by the increase in the pressure of natural selection on the individuals. With regard to human beings, the aging is a harmful atavism, since humans have ceased to rely on the too slow pace of his evolution and, instead of adapting to the environment, chose to adapt this medium to their needs.
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