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.

Keywords: Aging; Energy; Growth; Life program; Longevity; Regeneration; Senescence.

Figure 1. Percentage share of species with long maximal lifespan (≥ 35 years) among all analysed species.

Figure 2. Differences among animal groups in terms of maximal lifespans.

Non-parametric ANOVA (Kruskal–Wallis test; H_8,36 = 1963.25; P < 0.00001) indicates significant differences among animal groups in terms of maximal lifespans. Groups 1–5 were identified based on Dunn’s post-hoc test. Boxes show interquartile range. Median value is indicated by horizontal line and mean value is indicated by cross. Whiskers indicate non-outlier range. Circles indicate longevity records.

Figure 3. Results of maximal lifespan (MLS) categories comparisons, performed separately for each pair of animal groups in thirty-six 2 ×3 contingency tables from which the chi-squared values (χ2) were calculated.

MLSs classes: SHORT, MLS <5 years; INTERM –INTERMEDIATE, 5 ≤ MLS <35 years; LONG, MLS ≥ 35 years.

Figure 4. Generalised model showing the phylogenetic relationships between animal clades, in the context of the major stages of evolution; red –senescent animals, blue –biologically ‘immortal’ animals.

Topology is based on the Tree of Life Web Project (http://www.tolweb.org) in addition to many studies from the literature that were used to resolve uncertainty in the ToL project phylogeny.

Figure 5. Simplified model of the senescence hypothesis.

Model depicting the hypothesis that senescence did not evolve independently but evolved as a side effect of previously chosen developmental strategies.