Abstract
How the sophisticated vertebrate behavioural repertoire evolved remains a major question in biology. The behavioural repertoire encompasses the set of individual behavioural components that an organism uses when adapting and responding to changes in its external world. Although unicellular organisms, invertebrates and vertebrates share simple reflex responses, the fundamental mechanisms that resulted in the complexity and sophistication that is characteristic of vertebrate behaviours have only recently been examined. A series of behavioural genetic experiments in mice and humans support a theory that posited the importance of synapse proteome expansion in generating complexity in the behavioural repertoire. Genome duplication events, approximately 550 Ma, produced expansion in the synapse proteome that resulted in increased complexity in synapse signalling mechanisms that regulate components of the behavioural repertoire. The experiments demonstrate the importance to behaviour of the gene duplication events, the diversification of paralogues and sequence constraint. They also confirm the significance of comparative proteomic and genomic studies that identified the molecular origins of synapses in unicellular eukaryotes and the vertebrate expansion in proteome complexity. These molecular mechanisms have general importance for understanding the repertoire of behaviours in different species and for human behavioural disorders arising from synapse gene mutations.
Highlights
Approximately 550 Ma, produced expansion in the synapse proteome that resulted in increased complexity in synapse signalling mechanisms that regulate components of the behavioural repertoire
As synapse proteins play a role in all aspects of the behavioural repertoire of metazoans, it might seem unlikely that synapse signalling mechanisms could be relevant to the behaviour of unicellular organisms
My colleagues and I have hypothesized that the greater complexity in the vertebrate behavioural repertoire and synaptic plasticity arose from the expansion and diversification in synapse proteins [11,12]
Summary
The notion that humans and other animals use a behavioural repertoire of individual behavioural responses was articulated in the nineteenth century by Herbert Spencer, Charles Darwin, George Romanes and William James. Romanes, a protegeof Darwin and considered as the father of evolutionary psychology, suggested that there was a hierarchical continuum between these three broad classifications of behaviour These pioneers noted that invertebrates and even unicellular organisms displayed reflexes, instincts and a capacity to learn. Charles Sherrington, who is principally known for his electrophysiological studies of the reflex, recognized that the protozoa Vorticella exhibited all three major components of the reflex (reception, conduction, end-effect) [2] He noted that metazoans had specialized these three components of the reflex into individual cell types and specific structures. A major question in biology that remains is: how did the mammalian vertebrate behavioural repertoire evolve and what were the underlying mechanisms?
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