Senescence as a trade-off between successful land colonisation and longevity: critical review and analysis of a hypothesis

Abstract

Background Most common terrestrial animal clades exhibit senescence, suggesting strong adaptive value of this trait. However, there is little support for senescence correlated with specific adaptations. Nevertheless, insects, mammals, and birds, which are the most common terrestrial animal clades that show symptoms of senescence, evolved from clades that predominantly did not show symptoms of senescence. Thus, we aimed to examine senescence in the context of the ecology and life histories of the main clades of animals, including humans, and to formulate hypotheses to explain the causes and origin of senescence in the major clades of terrestrial animals. Methodology We reviewed literature from 1950 to 2020 concerning life expectancy, the existence of senescence, and the adaptive characteristics of the major groups of animals. We then proposed a relationship between senescence and environmental factors, considering the biology of these groups of animals. We constructed a model showing the phylogenetic relationships between animal clades in the context of the major stages of evolution, distinguishing between senescent and biologically ‘immortal’ clades of animals. Finally, we synthesised current data on senescence with the most important concepts and theories explaining the origin and mechanisms of senescence. Although this categorisation into different senescent phenotypes may be simplistic, we used this to propose a framework for understanding senescence. Results We found that terrestrial mammals, insects, and birds show senescence, even though they likely evolved from non-senescent ancestors. Moreover, secondarily aquatic animals show lower rate of senescence than their terrestrial counterparts. Based on the possible life histories of these groups and the analysis of the most important factors affecting the transition from a non-senescent to senescent phenotype, we conclude that aging has evolved, not as a direct effect, but as a correlated response of selection on developmental strategies, and that this occurred separately within each clade. Adoption of specific life history strategies could thus have far-reaching effects in terms of senescence and lifespan. Conclusions Our analysis strongly suggests that senescence may have emerged as a side effect of the evolution of adaptive features that allowed the colonisation of land. Senescence in mammals may be a compromise between land colonisation and longevity. This hypothesis, is supported by palaeobiological and ecological evidence. We hope that the development of new research methodologies and the availability of more data could be used to test this hypothesis and shed greater light on the evolution of senescence.

DNA methylation meta-analysis confirms the division of the genome into two functional groups

“…We regard the ontogenesis program as a strictly defined sequence of IntG gene expression, starting from the zygote stage, for the purpose of organism formation. The main goal of the ontogenesis program is to achieve the maximum competitive advantage by the time the organism reaches the state of fertility, since natural selection is aimed precisely at this stage of metazoan development [26,27,28,29,30]. Genome methylation, as a regulatory tool, is directly involved in the development and implementation of the ontogenesis program, including the processes of cell differentiation in Mammalian [31].…”

The RNA-Seq data analysis shows how the ontogenesis defines aging

“…The biological mechanism of aging remains one of the main mysteries in modern biology. Most scientists dealing with this problem agree in the opinion that aging is either the result of a purposeful evolutionary program inherent in the genome ( Larocca et al, 2021 ; De Magalhães Church., 2005 ; Bilinski et al, 2021 ), or a consequence of spontaneous disturbances in the organism leading to maladaptation ( Soto-Palma et al, 2022 ; Kinzina et al, 2019 ). At the same time both approaches to the causes of aging are not yet presented by the description of a specific mechanism explaining the emergence and acceleration of aging after reaching fertility ( Walker, 2022 ; West et al, 2019 ).…”

“…We understand the ontogenesis program as a strictly defined sequence of IntG gene expression with the assignment of an advantage in the consumption of cellular resources in order to form the organism and achieve its maximum development by the beginning of reproductive age. In our views we proceed from two basic statements: resource capabilities of any cell are always limited; the main goal of the ontogenesis program is to achieve the maximum competitive advantage by the time the organism reaches reproductive age, because natural selection is aimed at this very stage of development ( Gems et al, 2021 ; Bilinski et al, 2021 ; Gems et al, 2021 ; Kirkwood and Holliday, 1979 ). This advantage, gained at a critical moment for the continuation of the species, is paid for by the suppression of autonomous and regenerative potential in the future.…”