Abstract
The detection of external and internal cues alters gene expression in the brain which in turn may affect neural networks that underly behavioral responses. Previous studies have shown that gene expression profiles differ between major brain regions within individuals and between species with different morphologies, cognitive abilities and/or behaviors. A detailed description of gene expression in all macroanatomical brain regions and in species with similar morphologies and behaviors is however lacking. Here, we dissected the brain of two cichlid species into six macroanatomical regions. Ophthalmotilapia nasuta and O. ventralis have similar morphology and behavior and occasionally hybridize in the wild. We use 3′ mRNA sequencing and a stage-wise statistical testing procedure to identify differential gene expression between females that were kept in a social setting with other females. Our results show that gene expression differs substantially between all six brain parts within species: out of 11,577 assessed genes, 8,748 are differentially expressed (DE) in at least one brain part compared to the average expression of the other brain parts. At most 16% of these DE genes have |log2FC| significantly higher than two. Functional differences between brain parts were consistent between species. The majority (61–79%) of genes that are DE in a particular brain part were shared between both species. Only 32 genes show significant differences in fold change across brain parts between species. These genes are mainly linked to transport, transmembrane transport, transcription (and its regulation) and signal transduction. Moreover, statistical equivalence testing reveals that within each comparison, on average 89% of the genes show an equivalent fold change between both species. The pronounced differences in gene expression between brain parts and the conserved patterns between closely related species with similar morphologies and behavior suggest that unraveling the interactions between genes and behavior will benefit from neurogenomic profiling of distinct brain regions.
Highlights
Behavioral responses to external and internal cues are essential for organismal survival and reproductive success, because they allow organisms to find food, flee from predators and find mating partners, amongst others
The diencephalon was separated from all other brain parts, while the telencephalon and olfactory bulbs on the one hand, and the optic tectum and brain stem on the other hand, were more similar in gene expression to each other than to the other brain parts
The enriched Gene ontology (GO) terms for each brain part did not point to mRNA decay (Table S2); (4) we did not observe a decrease of gene expression levels of the 200 most differential expression (DE) genes from the cerebellum, optic tectum, telencephalon, olfactory bulbs, brain stem to the diencephalon (Figure S2)
Summary
Behavioral responses to external and internal cues are essential for organismal survival and reproductive success, because they allow organisms to find food, flee from predators and find mating partners, amongst others. The vertebrate brain is divided in morphologically distinct but interconnected structures that are well conserved across different taxa (Northcutt, 2002) These brain parts are functionally distinct: the nuclei of two behavioral neural networks (the social behavior network and mesolimbic reward system) are mainly located in the diencephalon and in the telencephalon, respectively (O’Connell and Hofmann, 2011; Bshary et al, 2014). The cerebellum has an important role in implementing motory programs (Roberts et al, 1992) and spatial and emotional learning (Yoshida et al, 2004) These functional differences are reflected in brain region specific gene expression profiles in different model organisms (Khaitovich et al, 2004; Lein et al, 2007; Myers et al, 2015)
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