J. theor. Biol. (1990) 147, 133-142 Evolution of Increased Susceptibility to Infectious Diseases in Age Structured Populations SIGFRID LUNDBERG Department of Ecology, Theoretical Ecology, Ecology Building, Lund University, S-223 62 Lund, Sweden (Received on 6 November 1989, Accepted in revised form on 14 May 1990) Current theory on the epidemiology of infectious diseases in genetically heterogeneous host populations ignores age structure. Thus, the possibility that microparasites might have negative effects on fitness in different ways during different phases of the lives of their hosts is not accounted for. For example, infections causing mortality and morbidity among juveniles might also have an impairing effect on reproduction among adults, as is the case in many so called childhood diseases. I demonstrate that when this is the case there may be a selective pressure for the host to evolve a higher level of susceptibility to an infection, provided it has the following properties: it should (i) provide life-long immunity, (ii) have a negative effect on reproduction and (iii) not cause too many mortalities. Introduction An infectious disease is characterized by, among other things, its age-specific prevalence curve, i.e. a plot of the fraction currently infected within each cohort against age. It is fruitful to regard this curve as a life history trait, which is evolutionarily adjusted in order to minimize the total detrimental effects of the disease at different ages. Adopting this view, we can apply Medawar's (1952) and Hamilton's (1966) propositions, that if there is genetic variation for the age-specific expression of a gene, through, e.g. other genes modifying its age of onset, natural selection should promote an early expression if the gene is beneficial and, conversely, a late expression if it is not. By the same token, a trait which is favourable early in life but disfavourable later is likely to be selected for, since genetic variation for traits expressed late in life tends to be neutral. A gene decreasing the overall susceptibility to an infectious disease is in a sense equivalent with one for a late onset, because it shifts the mode of the prevalence curve towards older ages. Current theory on the epidemiology of infectious diseases in genetically heterogeneous host populations predicts that such genes will increase when rare (Holt & Pickering, 1985; Anderson & May, 1986). Roughgarden (1979) among others has discussed genes improving reproduction at one age at the cost of decreased survival at another. In life history theory it is generally taken for granted that an increased reproductive effort at one age leads to decreased survival at some older age. However, in the context of infectious diseases it can be the other way around. Consider the case of an infection providing lifelong immunity and having an impairing effect on reproduction when contracted by adults. Then the host might be selected for increased susceptibility to the infection, 133 0022-5193/90/021133+ 10 $03.00/0 O 1990 Academic Press Limited