The long lives of primates and the ‘invariant rate of ageing’ hypothesis

Colchero, Fernando; Aburto, José Manuel; Archie, Elizabeth A.; Boesch, Christophe; Breuer, Thomas; Campos, Fernando A.; Collins, Anthony; Conde, Dalia Amor; Cords, Marina; Crockford, Catherine; Thompson, Melissa Emery; Fedigan, Linda M.; Fichtel, Claudia; Groenenberg, Milou; Hobaiter, Catherine; Kappeler, Peter M.; Lawler, Richard R.; Lewis, Rebecca J.; Machanda, Zarin; Manguette, Marie L.; Muller, Martin N.; Packer, Craig; Parnell, Richard J.; Perry, Seymour; Pusey, Anne E.; Robbins, Martha M.; Seyfarth, Robert M.; Silk, Joan B.; Staerk, Johanna; Stoinski, Tara S.; Stokes, Emma J.; Strier, Karen B.; Strum, Shirley C.; Tung, Jenny; Villavicencio, Francisco; Wittig, Roman M.; Wrangham, Richard W.; Zuberbühler, Klaus; Vaupel, James W.; Alberts, Susan C.

doi:10.1038/s41467-021-23894-3

Cited by 61 publications

(54 citation statements)

References 37 publications

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“…On one hand, the explanation of the Gompertz model on the basis of sufficient causes containing LOGE (without EREF) implies that the Gompertz distribution (with a given rate of aging or Gompertz parameter θ) represents a benchmark set by the evolutionary process, in the sense that the schedule of intrinsic mortality is related to the declining force of natural selection and it is somehow "calibrated" to elements of human reproductive biology (e.g., the ages when reproduction starts and ends) as well as intergenerational transfers (5,89,90). This is consistent with recent evidence supporting the invariant rate of aging hypothesis, according to which the rate of aging is relatively constant within humans and other species (91). On the other hand, such an account implies that sufficient causes of death containing EREF underlie departures from the Gompertz distribution (92)(93)(94), or as put by Major Greenwood long ago, "the blurring effect of the 'environmental' factors which it cannot be supposed adequately to express" (95).…”

Section: Explanation Of the Gompertz Mortality Modelsupporting

confidence: 85%

An Evolution-Based Model of Causation for Aging-Related Diseases and Intrinsic Mortality: Explanatory Properties and Implications for Healthy Aging

Levy¹,

Levin

2022

Front. Public Health

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Aging-related diseases are the most prevalent diseases in advanced countries nowadays, accounting for a substantial proportion of mortality. We describe the explanatory properties of an evolution-based model of causation (EBMC) applicable to aging-related diseases and intrinsic mortality. The EBMC takes the sufficient and component causes model of causation as a starting point and develops it using evolutionary and statistical theories. Genetic component causes are classified as “early-onset” or “late-onset” and environmental component causes as “evolutionarily conserved” or “evolutionarily recent.” Genetic and environmental component causes are considered to occur as random events following time-to-event distributions, and sufficient causes are classified according to whether or not their time-to-event distributions are “molded” by the declining force of natural selection with increasing age. We obtain for each of these two groups different time-to-event distributions for disease incidence or intrinsic mortality asymptotically (i.e., for a large number of sufficient causes). The EBMC provides explanations for observations about aging-related diseases concerning the penetrance of genetic risk variants, the age of onset of monogenic vs. sporadic forms, the meaning of “age as a risk factor,” the relation between frequency and age of onset, and the emergence of diseases associated with the modern Western lifestyle. The EBMC also provides an explanation of the Gompertz mortality model at the fundamental level of genetic causes and involving evolutionary biology. Implications for healthy aging are examined under the scenarios of health promotion and postponed aging. Most importantly from a public health standpoint, the EBMC implies that primary prevention through changes in lifestyle and reduction of environmental exposures is paramount in promoting healthy aging.

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Section: Explanation Of the Gompertz Mortality Modelsupporting

confidence: 85%

An Evolution-Based Model of Causation for Aging-Related Diseases and Intrinsic Mortality: Explanatory Properties and Implications for Healthy Aging

Levy¹,

Levin

2022

Front. Public Health

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“…Finally, mother's age also did not predict early survival, although mothers in these two birth cohorts were rather old, with a mean age of 12.6 ± 4.6 years, including an 18-, 19-, and 20-year-old female. Female sifakas have an average life expectancy of 5 years (Colchero et al 2021), and the oldest female in our long-term records was 21 years old. Hence, maternal senescence as described for many other mammals (Ivimey-Cook and Moorad 2020) did not influence infant pre-adult survival.…”

Section: Effects Of Maternal Gc Levels On Maternal Investment and Infant Developmentmentioning

confidence: 76%

Maternal stress effects on infant development in wild Verreaux's sifaka (Propithecus verreauxi)

Malalaharivony

Fichtel

Heistermann

et al. 2021

Behav Ecol Sociobiol

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Maternal effects mediated by nutrients or specific endocrine states of the mother can affect infant development. Specifically, pre- and postnatal maternal stress associated with elevated glucocorticoid (GC) output is known to influence the phenotype of the offspring, including their physical and behavioral development. These developmental processes, however, remain relatively poorly studied in wild vertebrates, including primates with their relatively slow life histories. Here, we investigated the effects of maternal stress, assessed by fecal glucocorticoid output, on infant development in wild Verreaux’s sifakas (Propithecus verreauxi), a group-living Malagasy primate. In a first step, we investigated factors predicting maternal fecal glucocorticoid metabolite (fGCM) concentrations, how they impact infants’ physical and behavioral development during the first 6 months of postnatal life as well as early survival during the first 1.5 years of postnatal life. We collected fecal samples of mothers for hormone assays and behavioral data of 12 infants from two birth cohorts, for which we also assessed growth rates. Maternal fGCM concentrations were higher during the late prenatal but lower during the postnatal period compared to the early/mid prenatal period and were higher during periods of low rainfall. Infants of mothers with higher prenatal fGCM concentrations exhibited faster growth rates and were more explorative in terms of independent foraging and play. Infants of mothers with high pre- and postnatal fGCM concentrations were carried less and spent more time in nipple contact. Time mothers spent carrying infants predicted infant survival: infants that were more carried had lower survival, suggesting that they were likely in poorer condition and had to be cared for longer. Thus, the physical and behavioral development of these young primates were impacted by variation in maternal fGCM concentrations during the first 6 months of their lives, presumably as an adaptive response to living in a highly seasonal, but unpredictable environment. Significance statement The early development of infants can be impacted by variation in maternal condition. These maternal effects can be mediated by maternal stress (glucocorticoid hormones) and are known to have downstream consequences for behavior, physiology, survival, and reproductive success well into adulthood. However, the direction of the effects of maternal physiological GC output on offspring development is highly variable, even within the same species. We contribute comparative data on maternal stress effects on infant development in a Critically Endangered primate from Madagascar. We describe variation in maternal glucocorticoid output as a function of ecological and reproductive factors and show that patterns of infant growth, behavioral development, and early survival are predicted by maternal glucocorticoids. Our study demonstrates how mothers can influence offspring fitness in response to challenging environmental conditions.

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“…Although mean lifespan is influenced by a large number of factors, the respective contribution of social capital versus other biological, ecological and environmental factors in the regulation of senescence and longevity remains an open question. Time is finite for most living animals, but social capital appears to be a promising tool to make senescence an adjustable parameter and to slow down the rate of ageing (Colchero et al 2021).…”

Section: Discussionmentioning

confidence: 99%