Lifespan Extension in Long-Lived Vertebrates Rooted in Ecological Adaptation

Abstract

Contemporary studies on aging and longevity have largely overlooked the role that adaptation plays in lifespan variation across species. Emerging evidence indicates that the genetic signals of extended lifespan may be maintained by natural selection, suggesting that longevity could be a product of organismal adaptation. The mechanisms of adaptation in long-lived animals are believed to account for the modification of physiological function. Here, we first review recent progress in comparative biology of long-lived animals, together with the emergence of adaptive genetic factors that control longevity and disease resistance. We then propose that hitchhiking of adaptive genetic changes is the basis for lifespan changes and suggest ways to test this evolutionary model. As individual adaptive or adaptation-linked mutations/substitutions generate specific forms of longevity effects, the cumulative beneficial effect is largely nonrandom and is indirectly favored by natural selection. We consider this concept in light of other proposed theories of aging and integrate these disparate ideas into an adaptive evolutionary model, highlighting strategies in decoding genetic factors of lifespan control.

The Danaid Theory of Aging

“…The lack of complete coverage acknowledges the potential for non-genetic mechanisms, or for mechanisms that are related to genetics in substantially more complex ways than typically considered under antagonistic pleiotropy (effects that are high-dimensionally epistatic as well as contingent on environment). The adaptive hitchhike hypothesis posits that slow aging is a byproduct of other adaptations ( Omotoso et al, 2021 ), and thus is also consistent with optimality approaches. All of these theories, as well as our Danaid theory and adaptive theories, can then be related to purely mechanistic theories of aging, such as those contained in the Hallmarks framework ( López-Otín et al, 2013 ).…”

“…If the Hallmarks of aging are shown to be not just present in most/all species, but sufficient explanations, and modulable, our theory would be disproven. Conversely, our theory will be supported if increasing data show variation in aging mechanisms/constraints in different taxa (Omotoso et al, 2021), often at variance with the forces of selection, and if we continue to uncover a larger and larger role for the breakdown in homeostatic mechanisms or other basic constraints in shaping the aging process. It is time for theory on the evolution of aging to incorporate what is known about development, physiology, genetics, and comparative biology, and to acknowledge explicitly that constraints could result in aging even in the absence of the selection shadow, and thus even in the absence of the classical theories.…”

“…First, why could aging evolve, given that, all else being equal, an individual’s fitness should be maximized by living as long as possible? Second, why do patterns of aging vary across the tree of life the way they do ( Omotoso et al, 2021 )? The classical evolutionary theories of aging have long provided a convincing answer to the first question ( Medawar, 1952 ; Williams, 1957 ; Hamilton, 1966 ; Kirkwood, 1977 ).…”

Editorial: Mechanisms and Pathways Contributing to the Diversity of Aging Across the Tree of Life

“…Two, in fact, present novel evolutionary theories of aging. The adaptive hitchhike model by Omotoso and others ( Omotoso et al, 2021 ) suggests that pro-longevity mutations may arise for reasons unrelated to longevity and then hitchhike around the tree of life. In a complementary perspective, Wensink and Cohen ( Wensink and Cohen 2021 ) propose the Danaid theory of aging: that complex organisms are often unmaintainable, i.e.…”

Bioethical and social constructions of life extension and longevity

“…In this regard, the question arises not only of the survival of bioethics (defined by Potter (1971) "as a bridge to the future"), but also of the diversity of the human species and the entire biosphere. With the positive results of current technological achievements and scientific knowledge in prolonging the life of some animal species (Tian, Seluanov and Gorbunova 2017;Omotoso, Gladyshev and Zhou 2001), it is to be expected that research efforts, under the justification of disease control in old age, will continue, resulting in this knowledge being applied to humans. There are two fundamental approaches that can predict in which direction this research will go.…”