Diptera is one of the biggest insect orders and displays a large diversity of visual adaptations. Similarly to other animals, the dipteran visual process is mediated by opsin genes. While the diversity and function of these genes is well studied in key model species, a comprehensive comparative genomic study across the dipteran phylogeny is missing. Here we mined the genomes of 61 dipteran species, reconstructed the evolutionary affinities of 528 opsin genes and determined the selective pressure acting in different species. We found that opsins underwent several lineage-specific events, including an independent expansion of Long Wave Sensitive opsins in flies and mosquitoes, and numerous family-specific duplications and losses. Both the Drosophila and the Anopheles complement is derived in comparison with the ancestral dipteran state. Molecular evolutionary studies suggest that gene turnover rate, overall mutation rate, and site-specific selective pressure are higher in Anopheles than in Drosophila. Overall, our findings indicate an extremely variable pattern of opsin evolution in dipterans, showcasing how two similarly aged radiations, Anopheles and Drosophila, are characterized by contrasting dynamics in the evolution of this gene family. These results provide a foundation for future studies on the dipteran visual system.

AbstractOpsin receptors mediate the visual process in animals and their evolutionary history can provide precious hints on the ecological factors that underpin their diversification. Here we mined the genomes of more than 60 Dipteran species and reconstructed the evolution of their opsin genes in a phylogenetic framework. Our phylogenies indicate that dipterans possess an ancestral set of five core opsins which have undergone several lineage-specific events including an independent expansion of low wavelength opsins in flies and mosquitoes and numerous family specific duplications and losses. Molecular evolutionary studies indicate that gene turnover rate, overall mutation rate, and site-specific selective pressure are higher in Anopheles than in Drosophila; we found signs of positive selection in both lineages, including events possibly associated with their peculiar behaviour. Our findings indicate an extremely variable pattern of opsin evolution in dipterans, showcasing how two similarly aged radiations - Anopheles and Drosophila - can be characterized by contrasting dynamics in the evolution of this gene family.

Monoamines like serotonin, dopamine, and adrenaline/noradrenaline (epinephrine/norepinephrine) act as neuromodulators in the nervous system. They play a role in complex behaviours, cognitive functions such as learning and memory formation, as well as fundamental homeostatic processes such as sleep and feeding. However, the evolutionary origin of the genes required for monoaminergic modulation is uncertain. Using a phylogenomic approach, in this study, we show that most of the genes involved in monoamine production, modulation, and reception originated in the bilaterian stem group. This suggests that the monoaminergic system is a bilaterian novelty and that its evolution may have contributed to the Cambrian diversification.

Monoamines like serotonin, dopamine, and adrenaline/noradrenaline (epinephrine/ norepinephrine) act as neuromodulators that tune the response of the nervous system to the environment with predictable advantages for fitness. For instance, monoamines influence action selection depending on the internal state of the organism, contribute to higher cognitive functions like learning and memory formation and modulate fundamental homeostatic needs such as sleep or feeding. Despite their significance and the extensive research in model organisms, the evolutionary origin of the monoaminergic system is uncertain. Here using a phylogenomic approach we study the evolution of the majority of genes involved in the production, modulation, and detection of monoamines. Our analyses suggest that most of the genes of the monoaminergic system originated in the common ancestor of bilaterians. These findings suggest that the monoaminergic synaptic pathway is a bilaterian innovation. We hypothesise that monoaminergic neuromodulation contributed to the diversification and complexification of behaviour and forms found in Bilateria.

Chemokine signalling performs key functions in cell migration via chemoattraction, such as attracting leukocytes to the site of infection during host defence. The system consists of a ligand, the chemokine, usually secreted outside the cell, and a chemokine receptor on the surface of a target cell that recognises the ligand. A number of non-canonical components interact with the system. While canonical components have been described in vertebrate lineages, the distribution of the non-canonical components is less clear. Uncertainty over the relationships between canonical and non-canonical components hampers our understanding of the evolution of the system. We used phylogenetic methods, including gene-tree to species-tree reconciliation to untangle the relationships between canonical and non-canonical components, identify gene duplication events and clarify the origin of the system. We found that unrelated ligand groups independently evolved chemokine-like functions. We found non-canonical ligands outside vertebrates, such as TAFA “chemokines” found in urochordates. In contrast, all receptor groups are vertebrate-specific and all - except ACKR1 - originated from a common ancestor in early vertebrates. Both ligand and receptor copy numbers expanded through gene duplication events at the base of jawed vertebrates, with subsequent waves of innovation occurring in bony fish and mammals.