Tracing Slow Phenoptosis to the Prenatal Stage in Social Vertebrates

Vladimir Skulachev's coining of the term "phenoptosis" 25 years ago (Skulachev, V. P., Biochemistry (Moscow), 62, 1997) highlighted the theoretical possibility that aging is a programmed process to speed the exit of individuals posing some danger to their social group. While rapid "acute phenoptosis" might occur at any age (e.g., to prevent spread of deadly infections), "slow phenoptosis" is generally considered to occur later in life in the form of chronic age-related disorders. However, recent research indicates that risks for such chronic disorders can be greatly raised by early life adversity, especially during the prenatal stage. Much of this research uses indicators of biological aging, the speeding or slowing of natural physiological deterioration in response to environmental inputs, leading to divergence from chronological age. Studies using biological aging indicators commonly find it is accelerated not only in older individuals with chronic disorders, but also in very young individuals with health problems. This review will explain how accelerated biological aging equates to slow phenoptosis. Its occurrence even in the prenatal stage is theoretically supported by W. D. Hamilton's proposal that offsprings detecting they have dangerous mutations should then automatically speed their demise, in order to improve their inclusive fitness by giving their parents the chance to produce other fitter siblings.