THE EVOLUTION OF HUMAN LONGEVITY ROBIN HOLLIDAY* Most animals live in a hazardous natural environment. The major problems confronted are scarcity of food or water, predators, and disease. A high mortality means that few, if any, individuals reach an age where senescence becomes apparent. This was first made clear by Medawar in outlining a new theory for the evolution of ageing, and Williams independently developed a similar theory [1, 2]. Medawar proposed that deleterious mutations acting late in life would not be selected against, so could accumulate, and eventually bring about senescence. Williams emphasized the importance ofpleiotropic genes which had beneficial effects early in life but deleterious effects in late maturity. The Medawar-Williams theory has subsequently been the cornerstone ofextensive and comprehensive discussions by others [3-10]. It is universally agreed that populations are age-structured, and that there are many more young breeding adults than old ones. The life history of any given species is based on several parameters, including the time taken to reach reproductive maturity, the rate of reproduction, the mortality from birth onwards, and the lifespan. It is evident that if mortality is very high, then rapid growth to reproductive maturity and a high rate of reproduction is necessary to allow the population to survive. In these species maximum lifespan is short. In contrast, animals with low annual mortality can evolve slow rates of growth and reproduction, and a long lifespan. As well as the extensive theoretical studies, there is also experimental work with Drosophila which confirms some of the basic conclusions. Starting with a heterozygous population, offspring were selected from the oldest parents over successive generations. After many generations of selection , the time of onset of reproduction was significantly greater and there was an increase in longevity [4, 10-12]. In mammals, there are examples of the evolution of progressively shorter The author acknowledges with gratitude the helpful comments of Leslie Orgel and Linda Partridge. *CSIRO Division of Biomedical Engineering, Sydney Laboratory, North Ryde, NSW 2113 Australia.© 1996 by The University of Chicago. All rights reserved. 0031-5982/96/3903-0942$01.00 100 Robin Holliday ¦ Evolution ofHuman Longevity 15 C O fi 10 3 "D O ?a a> (L d 5 •14 •11 •12 ·13 •10 •7 •9 •8 •1 2· ·3 •4 10 20 30 40 50 Longevity (years) 60 70 80 Fig. 1.—The relationship between the age of onset of reproduction of primate genera, including the gestation period, and their maximum life span. 1, Slow loris (Nyctocebus) ; 2, Slender loris (Loris); 3, Mouse lemur (Microcebus) ; 4, Brown lemur (Lemur); 5, Squirrel monkey (Saimirí); 6, Marmoset (Calithrix); 7, Spider monkey (Atetes); 8, Macaque (Macaca); 9, Baboon (Papio); 10, Gibbon (Hylobales); 11, Chimpanzee (Pan); 12, Gorilla (Gorilla); 13, Orangutan (Pongo); 14, Human (Homo). The sources of information are [13-17] and M. L. Jones, personal communication. The estimation of maximum longevity is from small numbers of animals held in captivity. Although the maximum recorded human lifespan is 120 years, this is based on the records of a very large number of individuals. A small cohort, comparable to that of captive animals, is likely to have a life span of about 80 years. lifespan and progressively longer ones. Amongst carnivores, the stoats and weasels have evolved a life history in which survival depends on continuous availability of food, and mortality from starvation is high. Growth to reproductive maturity is rapid, and litter size is large. Lifespan even in a protected zoo environment is only a few years [13] . In contrast, the primates provide one of the best examples of the evolution of a longer lifespan. It is evident that there is a clear relationship between the age of reproductive maturity and the maximum lifespan, which is illustrated in Figure 1. Man is not only Perspectives in Biology and Medicine, 40, 1 ¦ Autumn 1996 101 the longest living primate, but the longest living mammalian species. The reasons for the evolution of increased longevity in man have not been satisfactorily explained. In this article, I discuss the life history parameters of the earliest humans and suggest how a longer lifespan evolved by natural selection. In natural environments it is common, but of course not invariable...