Radical lifespan disparities exist in the animal kingdom: Revamping the Evolutionary Theories of Aging

Revamping the Evolutionary Theories of Aging. Adiv A. Johnsona, Maxim N. Shokhirev, Boris Shoshitaishvili. Ageing Research Reviews, August 23 2019, 100947. https://doi.org/10.1016/j.arr.2019.100947

Highlights
• Extrinsic mortality is one of the most important drivers in the evolution of aging.
• Classical predictions expect higher extrinsic mortality to shorten evolved lifespan.
• The bulk of published data conform to the classical evolutionary theories of aging.
• Increased extrinsic mortality can sometimes select for longer evolved lifespans.
• Immortal animals that experience extrinsic mortality challenge classical theories.
• The aging response to extrinsic mortality involves multiple interacting factors.

Abstract: Radical lifespan disparities exist in the animal kingdom. While the ocean quahog can survive for half a millennium, the mayfly survives for less than 48 hours. The evolutionary theories of aging seek to explain why such stark longevity differences exist and why a deleterious process like aging evolved. The classical mutation accumulation, antagonistic pleiotropy, and disposable soma theories predict that increased extrinsic mortality should select for the evolution of shorter lifespans and vice versa. Most experimental and comparative field studies conform to this prediction. Indeed, animals with extreme longevity (e.g., Greenland shark, bowhead whale, giant tortoise, vestimentiferan tubeworms) typically experience minimal predation. However, data from guppies, nematodes, and computational models show that increased extrinsic mortality can sometimes lead to longer evolved lifespans. The existence of theoretically immortal animals that experience extrinsic mortality – like planarian flatworms, panther worms, and hydra – further challenges classical assumptions. Octopuses pose another puzzle by exhibiting short lifespans and an uncanny intelligence, the latter of which is often associated with longevity and reduced extrinsic mortality. The evolutionary response to extrinsic mortality is likely dependent on multiple interacting factors in the organism, population, and ecology, including food availability, population density, reproductive cost, age-mortality interactions, and the mortality source.

Keywords: evolution of agingmutation accumulationantagonistic pleiotropydisposable somalifespanextrinsic mortality