Abstract
The evolutionary explanation for lifespan variation is still based on the antagonistic pleiotropy hypothesis, which has been challenged by several studies. Alternative models assume the existence of genes that favor aging and group benefits at the expense of reductions in individual lifespans. Here we propose a new model without making such assumptions. It considers that limited dispersal can generate, through reduced gene flow, spatial segregation of individual organisms according to lifespan. Individuals from subpopulations with shorter lifespan could thus resist collapse in a growing population better than individuals from subpopulations with longer lifespan, hence reducing lifespan variability within species. As species that disperse less may form more homogeneous subpopulations regarding lifespan, this may lead to a greater capacity to maximize lifespan that generates viable subpopulations, therefore creating negative associations between dispersal capacity and lifespan across species. We tested our model with individual‐based simulations and a comparative study using empirical data of maximum lifespan and natal dispersal distance in 26 species of birds, controlling for the effects of genetic variability, body size, and phylogeny. Simulations resulted in maximum lifespans arising from lowest dispersal probabilities, and comparative analyses resulted in a negative association between lifespan and natal dispersal distance, thus consistent with our model. Our findings therefore suggest that the evolution of lifespan variability is the result of the ecological process of dispersal.
Highlights
With only a few exceptions, organisms deteriorate as they age and die, but large variation in longevity still exists among species (Finch, 1990)
Maybe as a response to this incapacity of the antagonistic pleiotropy hypothesis to provide a general explanation for the evolution of lifespan variability, some theoretical models have appeared in the last years based on the idea of programmed aging, stating that organisms have a genetically fixed senescence rate that is favored by natural selection because senescence may be adaptive in certain circumstances (Longo, Mitteldorf, & Skulachev, 2005; Mitteldorf, 2016; Mitteldorf & Martins, 2014; Mitteldorf & Pepper, 2009; Werfel, Ingber, & Bar-Yam, 2015)
A large body of empirical research demonstrates that senescence is not the result of natural selection favoring short lifespans log10 Natal dispersal distance
Summary
With only a few exceptions, organisms deteriorate as they age and die, but large variation in longevity still exists among species (Finch, 1990). Maybe as a response to this incapacity of the antagonistic pleiotropy hypothesis to provide a general explanation for the evolution of lifespan variability, some theoretical models have appeared in the last years based on the idea of programmed aging, stating that organisms have a genetically fixed senescence rate that is favored by natural selection because senescence may be adaptive in certain circumstances (Longo, Mitteldorf, & Skulachev, 2005; Mitteldorf, 2016; Mitteldorf & Martins, 2014; Mitteldorf & Pepper, 2009; Werfel, Ingber, & Bar-Yam, 2015) These models have the important limitation of dealing with group selection, as they assume that senescence benefits lineages by avoiding overpopulation and associated problems such as resource depletion and epidemics, and lack an evolutionary logic (Kowald & Kirkwood, 2016). We test this model with individual-based simulations and with empirical data from wild populations of 26 species of birds
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