Senescence as a trade-off between successful land colonisation and longevity: critical review and analysis of a hypothesis
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 th...
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| Format: | Article |
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PeerJ Inc.
2021-11-01
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| Series: | PeerJ |
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| Online Access: | https://peerj.com/articles/12286.pdf |
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| author | Tomasz Bilinski Aneta Bylak Krzysztof Kukuła Renata Zadrag-Tecza |
| author_facet | Tomasz Bilinski Aneta Bylak Krzysztof Kukuła Renata Zadrag-Tecza |
| author_sort | Tomasz Bilinski |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-09T06:31:30Z |
| format | Article |
| id | doaj.art-d88a721cf5f54b32a053778775661470 |
| institution | Directory Open Access Journal |
| issn | 2167-8359 |
| language | English |
| last_indexed | 2024-03-09T06:31:30Z |
| publishDate | 2021-11-01 |
| publisher | PeerJ Inc. |
| record_format | Article |
| series | PeerJ |
| spelling | doaj.art-d88a721cf5f54b32a0537787756614702023-12-03T11:05:34ZengPeerJ Inc.PeerJ2167-83592021-11-019e1228610.7717/peerj.12286Senescence as a trade-off between successful land colonisation and longevity: critical review and analysis of a hypothesisTomasz Bilinski0Aneta Bylak1Krzysztof Kukuła2Renata Zadrag-Tecza3Department of Biochemistry and Cell Biology, Faculty of Biology and Agriculture, University of Rzeszów, Rzeszów, PolandDepartment of Ecology and Environmental Protection; Institute of Agricultural Sciences, Land Management and Environmental Protection, University of Rzeszów, Rzeszów, PolandDepartment of Ecology and Environmental Protection; Institute of Agricultural Sciences, Land Management and Environmental Protection, University of Rzeszów, Rzeszów, PolandDepartment of Biochemistry and Cell Biology, Institute of Biology and Biotechnology, University of Rzeszów, Rzeszów, PolandBackground 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.https://peerj.com/articles/12286.pdfSenescenceAgingLongevityEnergyLife programGrowth |
| spellingShingle | Tomasz Bilinski Aneta Bylak Krzysztof Kukuła Renata Zadrag-Tecza Senescence as a trade-off between successful land colonisation and longevity: critical review and analysis of a hypothesis PeerJ Senescence Aging Longevity Energy Life program Growth |
| title | Senescence as a trade-off between successful land colonisation and longevity: critical review and analysis of a hypothesis |
| title_full | Senescence as a trade-off between successful land colonisation and longevity: critical review and analysis of a hypothesis |
| title_fullStr | Senescence as a trade-off between successful land colonisation and longevity: critical review and analysis of a hypothesis |
| title_full_unstemmed | Senescence as a trade-off between successful land colonisation and longevity: critical review and analysis of a hypothesis |
| title_short | Senescence as a trade-off between successful land colonisation and longevity: critical review and analysis of a hypothesis |
| title_sort | senescence as a trade off between successful land colonisation and longevity critical review and analysis of a hypothesis |
| topic | Senescence Aging Longevity Energy Life program Growth |
| url | https://peerj.com/articles/12286.pdf |
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