Whole brain gene expression in Lake Malawi cichlid F1 hybrids. Copadichromis virginalis x Mchenga conophoros

Most behaviors are associated with heritable genetic variation. Genetic mapping has revealed genomic regions or, in a few cases, specific genes explaining part of this variation. However, understanding how genetic divergence shapes behavioral evolution remains unclear. Here we analyze the evolution of an innate extended phenotype: bower building among male cichlid fish of Lake Malawi, which build bowers of two types, pits and castles. F1 hybrids of pit-digging and castle-building species perform sequential construction of first pit and then castle bowers. Analysis of brain gene expression in these hybrids showed that genes near behavior-associated variants display behavior-dependent allele-specific expression with preferential expression of the pit-species allele during pit digging, and of the castle-species allele during castle building. These genes are highly enriched for functions and pathways involved in neurodevelopment and neural plasticity. Our results suggest that natural behaviors can be associated with complex genetic architectures that alter behavior via cis-regulatory differences whose effects on gene expression are specific to the behavior itself. Overall design: F1 hybrids of the species Mchenga conophoros (castle builder) and Copadichromis virginalis (pit digger) were produced and run through three independent behavioral paradigms targetting: pit-digging behavior, castle-building behavior, and social isolation. Whole brains were extracted and processed for analyses of allele-specific expression using RNA-seq.