The evolution of hyperactivity, impulsivity and cognitive diversity

Abstract

The evolutionary status of attention deficit/hyperactivity disorder (ADHD) is central to assessments of whether modern society has created it, either physically or socially; and is potentially useful in understanding its neurobiological basis and treatment. The high prevalence of ADHD (5-10%) and its association with the seven-repeat allele of DRD4, which is positively selected in evolution, raise the possibility that ADHD increases the reproductive fitness of the individual, and/or the group. However, previous suggestions of evolutionary roles for ADHD have not accounted for its confinement to a substantial minority. Because one of the key features of ADHD is its diversity, and many benefits of population diversity are well recognized (as in immunity), we study the impact of groups' behavioural diversity on their fitness. Diversity occurs along many dimensions, and for simplicity we choose unpredictability (or variability), excess of which is a well-established characteristic of ADHD.Simulations of the Changing Food group task show that unpredictable behaviour by a minority optimizes results for the group. Characteristics of such group exploration tasks are risk-taking, in which costs are borne mainly by the individual; and information-sharing, in which benefits accrue to the entire group. Hence, this work is closely linked to previous studies of evolved altruism.We conclude that even individually impairing combinations of genes, such as ADHD, can carry specific benefits for society, which can be selected for at that level, rather than being merely genetic coincidences with effects confined to the individual. The social benefits conferred by diversity occur both inside and outside the 'normal' range, and these may be distinct. This view has the additional merit of offering explanations for the prevalence, sex and age distribution, severity distribution and heterogeneity of ADHD.

Figure 1

Factors potentially governing prevalence of hyperactive-impulsive traits in the population. Parentheses indicate factors of debatable importance (see text).

Figure 2

Knowledge acquisition in a changing environment (simulation). Four groups of individuals aim to maximize their knowledgeability about locally available food resources, while minimizing the risk of testing unknown foods. (a)–(c) show four independent groups of 40 individuals: a highly predictable group which does very little experimentation; a highly unpredictable group; and two mixed groups. The mixed groups contain mainly predictable individuals, with either 2 or 10 unpredictable individuals. (a) illustrates the paradigm. At any time, four foods (shown as four letters) are available to be freely chosen. This shows the accuracy of the group's knowledge of available foods, which changes as time progresses during a single run (unspecified time units, t.u.). Error increases each 10 t.u. when one food is replaced by another of unknown quality. Error then reduces as each group learns about the new food. (b) illustrates the rate of acquisition of knowledge of food by the four groups. The highly predictable group acquires information slowly, because individuals always choose their favourite three foods, so rarely explore new ones. (c) shows the gradual loss of individuals by each group, over nine food changes with no offspring (mean of 40 runs). In this particular task, groups in which 5% of the individuals are unpredictable survive the best. For discussion see text; for details see appendix A.

Figure 3

Effect of group and environment on survival (simulation). This shows the same overall task as figure 2, but with a much wider variety of groups. In (a) and (b), each datapoint indicates the number of survivors after nine food changes, one each 10 t.u., from an independent group initially of 10 members. (a) shows the effect of the predominant population brittleness on survival. The solid line shows that the survival of a completely uniform group reduces when their brittleness b exceeds 5. The dashed line is produced in exactly the same way, except for the substitution of two unpredictable individuals for two of the others. (b) shows the effect of the rate of environmental change on group survival. When food changes occur more frequently than once every 150 t.u., the presence of unpredictable individuals improves group survival. For discussion see text; for details see appendix A.

Figure 4

Model of ADHD effects on individual and group. Three classes of humans are shown: males with and without ADHD–HI (a continuum in reality), and females. The large grey circuit indicates the reproductive cycle from conception to adulthood and mating. At the right are shown the group benefits that arise from ADHD–HI, which may in turn be caused by the failure of developmental buffering in a minority of males. For more details see text.

Figure 5

Effects of rate of environmental change, and subgroup reproductive fitness, on group predictability and survival (simulation). X-axes are evolutionary time, notionally in units of 2000 months or approximately 200 years. In the first evolutionary period (white, time 0–10), one food changes every 1000 months, in the second (grey, time 10–16) every 20 months, and in the third (white, time 16–22) every 1000 months. Four separate simulations are shown in different colours. Each simulation starts with a population of 50 individuals each with an arbitrary uniform brittleness (9). The blue simulation has all individuals reproducing at the same rate, but in the other simulations subgroups have increased reproduction (see key). Whole-population reproduction rates are normalized for all simulations. Std, standard deviation; SEM, standard error of means on 30 runs. For discussion see text.