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Human social communication is impaired in the two primary disorders of the ‘social brain’, autism, and schizophrenia. This chapter describes a new hypothesis for the role of language in the evolution and development of autism and schizophrenia: that the cores of these two conditions are disordered social communication, with dysregulated social-linguistic development mediated in part by extremes of bias in maternal vs paternal imprinted gene expression, resulting in extreme mentalistic vs extreme mechanistic cognition. It evaluates this hypothesis via tests of the molecular evolution of genes underlying schizophrenia and language, analyses of how the human social brain has evolved, and evaluation of the roles of genomic conflicts in human development, enculturation, and communication via study of the genetic and epigenetic underpinnings of social-brain disorders. These convergent lines of evidence from evolutionary theory and neurogenomics support the hypothesis that psychosis represents the ‘illness that made us human’.

Behavioural ecology and cell biology both use the language of communication and signalling. In cell biology, signaller and receiver are cells of a single body or molecules encoded by a single genome and are implicitly assumed to have identical evolutionary interests. The signaller does not have an incentive to deceive. In behavioural ecology, signaller and receiver are different genetic individuals, with possibly conflicting evolutionary interests. Signallers may have an incentive to deceive, so receivers must decide whether signals can be trusted. However, we now know conflicts within genomes are possible. This raises questions about how internal conflicts influence signalling between and within individual organisms. These questions are explored using the example of genomic imprinting.

This chapter examines the ‘genic’ view of evolution associated with Williams, Dawkins, Maynard Smith, and others. A distinction is drawn between the process of genic selection and a gene's eye perspective on selection processes that occur at other levels. Outlaw genes or selfish genetic elements, which spread at the expense of other genes in the same organism, are briefly examined and the use of multi-level selection theory to explore the evolutionary dynamics of outlaws is discussed. A number of objections to gene's eye thinking are examined, including the charge of ‘confusing bookkeeping with causality’ and the charge of ignoring the context-dependence of genes' effects on phenotype.

Mitochondrial genes and nuclear genes are replicated and transmitted across generations as physically separated units. The extent to which these autonomous genomes are co-transmitted depends on the position of nuclear genes on autosomes versus sex chromosomes, and co-transmission has important implications for mitonuclear coevolution and conflict. Mitonuclear co-transmission, coadaptation, and coevolution are potentially very important for understanding fundamental evolutionary phenomena like Haldane’s rule. In addition, because mitochondrial genomes are transmitted strictly through maternal lines in most eukaryotes, selection on mitochondrial genes can favor female fitness over male fitness, leading to mother’s curse. The chapter assesses and draws conclusions about the relative importance of mitonuclear coadaptation and conflict in the evolution of eukaryotic lineages.

In some applications of agential thinking in evolutionary biology, genes and groups, rather than individuals, are the entities that are treated as agents with goals. The genes-as-agents concept is applicable only in cases of intra-genomic conflict, where it helps to make sense of the phenotypic consequences of such conflict. The groups-as-agents concept is applicable only when groups are adapted units, and where within-group conflict is either absent or suppressed; for otherwise the unity-of-purpose constraint on agency will not be satisfied. The idea of group agency has also arisen in social science, where the discussion closely parallels the biological discussion. In both cases, the critical issue is how individuals’ interests can be aligned with that of their group. One such alignment mechanism is the veil-of-ignorance, which deprives individuals of the information needed to pursue their self-interest at the group’s expense.