Elsevier

Schizophrenia Research

Volume 70, Issue 1, 1 September 2004, Pages 101-109
Schizophrenia Research

Schizophrenia as one extreme of a sexually selected fitness indicator

https://doi.org/10.1016/j.schres.2003.09.014Get rights and content

Abstract

Schizophrenia remains an evolutionary paradox. Its delusions, hallucinations and other symptoms begin in adolescence or early adulthood and so devastate sexual relationships and reproductive success that selection should have eliminated the disorder long ago. Yet it persists as a moderately heritable disorder at a global 1% prevalence—too high for new mutations at a few genetic loci. We suggest that schizophrenia persists and involves many loci because it is the unattractive, low-fitness extreme of a highly variable mental trait that evolved as a fitness (“good genes”) indicator through mutual mate choice. Here we show that this hypothesis explains many key features of schizophrenia and predicts that some families carry modifier alleles that increase the indicator's neurodevelopmental sensitivity to heritable fitness and condition. Such alleles increase the extent to which high-fitness family members develop impressive courtship abilities and achieve high reproductive success, but also increase the extent to which low-fitness family members develop schizophrenia. Here we introduce this fitness indicator model of schizophrenia, discuss its explanatory power, explain how it resolves the evolutionary paradox, discuss its implications for gene hunting, and identify some empirically testable predictions as directions for further research.

Section snippets

Background

Schizophrenia is a devastating mental illness with a well-established Cannon et al., 1998, Cardno et al., 1999, Tsuang et al., 2001 but evolutionarily puzzling (Huxley et al., 1964) genetic basis. Diverse evolutionary theories have attempted to explain why schizophrenia persists at a global 1% lifetime prevalence—far in excess of the rate possible from a single deleterious mutation (Wilson, 1997). One possibility, originally suggested by Julian Huxley (Huxley et al., 1964), is that

Hypothesis

We propose that schizophrenia is the unattractive extreme of a mental and behavioral ability that evolved as a fitness indicator (or set of indicators) through mutual mate choice in humans. If so, then the processes of neural development that go awry in schizophrenia should show high sensitivity to fitness and condition. In an individual with high genetic fitness (e.g., a low deleterious mutation load) and a favorable prenatal and postnatal environment, these neurodevelopmental processes should

Explanatory and predictive power

This hypothesis that schizophrenia represents the unattractive extreme of sexually selected verbal courtship abilities is just one possibility—a special case of our more general claim that schizophrenia is the unattractive extreme of some type of sexually selected fitness indicator (SSFI). This more general claim can be evaluated without specifying the precise nature of the SSFI, because SSFIs have some generic properties that explain many puzzling aspects of schizophrenia and lead to several

Conclusions

In summary, our hypothesis explains many key features of schizophrenia, including onset in adolescence and early adulthood (Hafner et al., 1993), greater severity and earlier age at onset in males (Jablensky, 2000), reduced reproductive rate (Nanko and Moridaira, 1993), substantial heritability (Tsuang et al., 2001), polygenic and multi-factorial basis Jablensky, 2000, Tsuang et al., 2001, frequent developmental abnormalities (Woods, 1998), increased reproductive success of unaffected relatives

Acknowledgements

We thank Paul Andrews, Julia Bailey, Helena Cronin, Joshua Freedman, Steve Gangestad, Alan Garfinkel, Nicholas Humphrey, Suma Jacob, Christina Palmer, Stephanie Shaner and Sydney Shaner for valuable discussions and comments on the manuscript.

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