Ashdin Publishing Journal of Evolutionary Medicine Vol. 5 (2017), Article ID 235975, 11 pages doi:10.4303/jem/235975 ASHDIN publishing Research Article THEORY The Evolving Opportunistic Pathogen Communities on Host Individuals and the Evolution of Host Aging Ulfat Baig, Akanksha Ojha, and Milind Watve Indian Institute of Science Education and Research, Dr. Homi Bhabha Road, Pune, Maharashtra 411008, India Address correspondence to Milind Watve, milind@iiserpune.ac.in Received 24 February 2016; Revised 4 April 2017; Accepted 6 April 2017 Copyright © 2017 Ulfat Baig et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract In the coevolution of host and the associated oppor- tunistically pathogenic microbiota, the microbiota has an advantage of a smaller generation time and thereby faster evolution. Sexual reproduction by the host is hypothesized to be the hosts’ evolutionary counter-strategy. We propose further that the ticking clock of the evolving microbiota influences the evolution of host aging. Modeling these dynamics shows that if transmission of microbes has a small to moderate vertical or kin-biased component, early aging can evolve in the host. Host genotypes with shorter longevity are more likely to escape pathogen evolution thereby getting a selective advantage for their progeny when risk of infection is high. As parasite communities are ecologically and evolutionarily dynamic, hosts can in response evolve plasticity in aging. The model shows that a genotype which activates aging or death pathways in response to threshold parasite colonization gets a selective advantage whenever there is a nonzero kin transmission bias. The hypothesis is compatible with classical hypotheses for aging. We make many predictions testable by epidemiological, comparative or experimental methods. Keywords parasites transmission; evolution of lifespan; kin selection; lifespan; life history 1. Introduction Whether aging is inevitable or is a trait specifically evolved under some kind of selection is an old debate. One school of thought assumes aging to be inevitable and beyond the reach of natural selection [1]. Many of the processes implicated in aging such as accumulation of somatic mutations, protein aggregation, oxidative damages or telomere shortening might be biochemically and thermodynamically inevitable [2]. However, since mechanisms of repair, replacement, throwing away or asymmetric segregation of damage exist, inevitability of mechanisms does not necessarily mean inevitability of the process. Germ line cells in higher organisms appear to perpetuate without any signs of aging [3,4,5,6,7]. Since every new generation begins with a single celled zygote, mutations in germ line cells are directly subject to natural selection, which prevents accumulation of deleterious mutations; therefore germ line cells do not seem to age. Organisms such as hydra and many plants that reproduce vegetatively do not show any obvious aging [4,5,8,9,10,11]. In some species, viability or reproductive capacity actually increases monotonically with age [11, 12]. If decline in viability is not universal with aging, it is worth asking why and how it declines in some organisms including humans. For a long time, bacteria that divide by binary fission were believed to be immune to aging. The demonstration of signs of aging in bacteria even during exponential growth [13] changed the perspective. However, asymmetric damage segregation, which is responsible for bacterial aging, has been shown to be both plastic and evolvable [14]. Bacterial aging provides many other grounds to doubt the inevitability of aging. Although some cells in a growing clone of bacteria undergo senescence, the clone as a whole grows with continued rejuvenation. A process that works for clones of bacteria should be possible, in principle, for multicellular organisms which are essentially clones of the zygote. Is aging inevitable after a germ-soma division of cell lines? Even if one assumes that aging is inevitable for a somatic cell, it does not necessarily imply that it is inevitable for an organism. A multicellular organism may program the cell turnover so as to replace the old cells in a balanced manner and thus escape organismal senescence indefinitely if resource provisioning is adequate. On the other hand, senescence of a system is theoretically possible even if its components are individually nonaging but irreplaceable [15]. Therefore, cellular senescence is neither necessary nor sufficient to explain organismal senescence. Since inevitability of aging is theoretically inadequate and empirically not universal, it can be said to have evolved to take different shapes in different species. The central logic of theories of evolution of aging is that the force of natural selection decreases with age of an individual [16, 17,