Hallucinatory experiences are as old as humankind and until the nineteenth century these experiences were generally attributed to mystical or divine sources such as gods or demons, whereas in modern times, hallucinations have generally been regarded as pathological and as signs of illness. ^{Reference Jenner2} Recently, however, our ideas about hallucinations and delusions are being challenged by findings from epidemiology. A new viewpoint is emerging. Simply put, hallucinations and delusions are more common than we think. Population-based studies using both self-report and interview surveys show that the prevalence of psychotic symptoms is far greater than had been previously considered, with a recent meta-analysis suggesting a prevalence rate of 5–8% in the general population, which is about ten times higher than the prevalence of diagnosed psychotic disorders. ^{Reference van Os, Linscott, Myin-Germeys, Delespaul and Krabbendam3} Prevalence rates of such symptoms may be even higher among young people. Ten years ago, Poulton et al ^{Reference Poulton, Caspi, Moffitt, Cannon, Murray and Harrington4} reported that 14% of 11-year-old children in the Dunedin birth cohort reported psychotic symptoms on interview and showed that these symptoms were associated with a 5- to 16-fold increased rate of psychotic illness in early adulthood, depending on the strength of the initial symptoms. Since then, large, population-based studies surveying psychotic symptoms among adolescents have found rates of 9–14% in interview-based studies, ^{Reference Bartels-Velthuis, Jenner, van de Willige, van Os and Wiersma5,Reference Horwood, Salvi, Thomas, Duffy, Gunnell and Hollis6} and greater than 25% in some studies using self-report questionnaires. ^{Reference Laurens, Hodgins, Maughan, Murray, Rutter and Taylor7–Reference Kelleher, Harley, Murtagh and Cannon9} Positive answers on self-report questionnaires have been validated on clinical interview. ^{Reference Kelleher, Harley, Murtagh and Cannon9} Therefore it is becoming increasingly clear that a sizable minority of young people experience psychotic symptoms.

This high prevalence of non-clinical psychotic symptoms in the population prompts us to re-evaluate these symptoms in the light of evolutionary theory. ^{Reference Nesse10} In this editorial we discuss how this non-clinical phenotype (i.e. psychotic symptoms) may hold the key to understanding the persistence of psychosis in the population and provide a new perspective on aetiology and treatment.

Evolutionary theories of psychosis

Psychosis is highly heritable and exerts strong negative fitness effects. Despite this apparent disadvantage, schizophrenia maintains a relatively stable prevalence worldwide. Several theories drawing on the Darwinian paradigm of selective advantage have been formulated to explain the persistence of psychosis in the human population. Crow's ‘speciation’ hypothesis argues that psychosis is the ‘price that Homo sapiens pays’ for development of language. ^{Reference Crow11} Burns proposed that schizophrenia is a ‘costly by-product’ in the evolution of complex social cognition ^{Reference Burns12} and Nesse developed this idea further in terms of ‘cliff-edge’ fitness, ^{Reference Nesse13} whereby certain traits may increase fitness up to a critical threshold, but beyond this point, fitness falls precipitously. For instance, strong tendencies to use metarepresentation and theory of mind can increase the ability to predict other people's behaviours and discern their intentions, but, as Nesse explains, ‘it is only one step further, over the cliff's edge of psychotic cognition… to finding secret meanings and evidence for conspiracies in other people's most casual gesture’. ^{Reference Nesse13} Recently, Dodgson & Gordon have proposed that certain types of hallucinations could be viewed as evolutionary by-products of a cognitive system designed to detect threat since, from a survival perspective, it is much worse to fail to recognise a threat such as the sound of an approaching predator than to mistakenly believe that a predator is approaching when it is not. ^{Reference Dodgson and Gordon14} Evolution may therefore favour a selective skew towards propagation of genes that promote false positives over false negatives, thus resulting in ‘hypervigilance hallucinations’ in the population. ^{Reference Dodgson and Gordon14} In social or pack animals, such as humans, hypervigilance is not necessary for every member, but the presence of this trait in at least some members stands to benefit the entire group. Such a trade-off allows the persistence of advantageous traits even in the presence of increased risk of disorder.

Implications for genetic studies

The possibility that vulnerability to psychosis may be a by-product of ‘normal’ human brain evolution, may offer an explanation for the difficulty in locating a genetic ‘point of rarity’ between individuals with schizophrenia and controls. ^{Reference van Os15,Reference Craddock and Owen16} We would also suggest that the limited success in findings in schizophrenia to date may be a result of shared genetic variation between the clinical (disease) phenotype and the non-clinical (symptom) phenotype. Genetic research thus far has used the simple dichotomy of people with psychotic disorder compared with the general population. However, the relatively high prevalence of the non-clinical psychosis phenotype in the general population may have masked genes of importance. Rather than searching for genetic variation only between individuals with psychotic disorders and the rest of the population (which contains, as we have discussed, significant numbers of individuals with the non-clinical phenotype), it may prove more fruitful to investigate genetic variation among individuals with the non-clinical phenotype in the general population (plus or minus individuals with the disease phenotype) compared with the individuals without such symptoms. Furthermore, an understanding of these genes and their functions may hold the key to explaining the persistence of psychosis in the population. It is possible that there are evolutionary advantages associated with genes that contribute to the non-clinical phenotype but which, in a fitness trade-off, also increase the risk for psychotic disorder. If, for example, as suggested by cliff-edge fitness theory, ^{Reference Nesse10} psychosis results from the development of certain useful traits beyond an optimal peak, we might find that people with the non-clinical psychosis phenotype demonstrate advantageous traits compared with the rest of the population in, for example, certain language, cognitive or metacognitive skills. Detailed investigation of the non-clinical psychosis phenotype might, therefore, allow us to uncover a Darwinian explanation for the persistence of psychosis genes in the general population that has not been possible by looking only at psychotic disorder.

Implications for diagnosis and treatment

The current diagnostic nosological systems are undergoing revision. Evolutionary theories lend support for the idea of a continuum approach to the diagnosis of psychosis ^{Reference van Os15} and provide some clues as to why the traditional Kraepelinian or categorical approaches to psychosis are beginning to prove problematic. ^{Reference Craddock and Owen16} Breaking down the categorical barriers may also help reduce the stigma associated with psychosis, which remains one of the greatest obstacles standing in the way of recovery and rehabilitation. Taking an evolutionary perspective may also lead to changes in how we think about treatment – for instance the idea of schizophrenia as a disorder of social brain development points to the importance of family therapy and social skills training. Some therapies such as hallucination-focused integrative therapy already incorporate such elements alongside more traditional cognitive–behavioural therapy approaches. ^{Reference Jenner, Laroi and Aleman17} The idea of hallucinations as a ‘hypervigilance’ reaction also suggests the value of engaging directly with the content of the symptoms in psychosis and acknowledging the fact that some individuals may wish to preserve positive or ‘useful’ voices that they feel support or help them. ^{Reference Jenner, Laroi and Aleman17}

Broadening the evolutionary perspective

An evolutionary approach may also prove fruitful in other areas of psychiatry. Higher than expected prevalences have been reported for depression and anxiety. Prospective studies are showing that up to half (and perhaps even a majority) of the population can expect one or more episodes of depression over their lifetime. ^{Reference Andrews, Poulton and Skoog18,Reference Moffitt, Caspi, Taylor, Kokaua, Milne and Polanczyk19} Taking an evolutionary perspective, one could speculate that the tendency for unhappiness and dissatisfaction is intrinsic to the human species (man as the ‘unhappy ape’) and this is one of the features that has been a contributory factor in the success of our species, driving Homo sapiens onwards, even to the surface of the moon, in search of new terrain and challenges. Applying evolutionary theories to depression may also lead to new approaches to treatment and novel aetiological theories. ^{Reference Nesse10}

Conclusion

Charles Darwin's anniversary year has ended but that does not mean we should put the theory of evolution back on the shelf and dust it off only when the next anniversary comes round. As Theodosius Dobzhansky famously stated, ‘Nothing in biology makes sense except in the light of evolution’. ^{Reference Dobzhansky20} From a neuroscientific point of view, detailed investigation of the non-clinical psychosis phenotype should provide novel leads for research into the aetiology, nosology and treatment of psychosis and other mental disorders.

Funding

M.C. is supported by a Health Research Board (Ireland) Clinician Scientist Award and a NARSAD Independent Investigator Award and is a member of the European Network of National Schizophrenia Networks Studying Gene–Environment Interactions (EU-GEI) funded by EU–FP7.