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Genetic architecture of an evolutionary novelty: the development of the male-specific turban-shaped eyes of Cloeon dipterum

Periodic Reporting for period 1 - EvoNovo (Genetic architecture of an evolutionary novelty: the development of the male-specific turban-shaped eyes of Cloeon dipterum)

Reporting period: 2016-01-01 to 2017-12-31

Morphological novelties are associated with innovative functions that have been conductive to major revolutions in the history of life: the development of limbs from fins to colonize the land, the invention of wings in insects that allowed the occupation of the air or the emergence of the placenta in mammals are amongst them. Nevertheless, it is still an open debate what genetic changes underlie these novelties, and whether these are generated through accumulation of progressive small changes or rather by major leaps. Despite their importance in the history of life, how morphological novelty arises and evolves is a long-standing question in Evolutionary Biology. One of the most striking examples of a sexually dimorphic novel structure is the extra pair of eyes present in the males of the mayfly species Cloeon dipterum. The males of this species develop, in addition to the compound eyes (shared by males and females), an extra pair of extremely large dorsal, turban-shaped eyes. EvoNovo wanted to take advantage of this novel visual system to make ground-breaking advances in the way we understand the genetic forces that control the origin of new organs and structures during evolution.
To investigate the appearance of the turbanate eye in C. dipterum, we combined a number of experimental approaches, including non-invasive imaging, gene expression analyses, genomics, transcriptomics, and epigenomics to knit the gene regulatory network responsible for the development of the turbanate eye. EvoNovo described the formation of this new organ in males and the regulatory networks that have evolved to originate this structure in the males of this species.
In addition, the establishment of C. dipterum as a model serves to other researchers as a foundation for further investigations in an organism placed in a key position in the phylogeny of insects.
We have successfully established C. dipterum as a model species with a continuous culture in the lab. We described the development of the eye and its integration with the optic lobes of male and female Cloeon nymphs using confocal and electron microscopy. Moreover, we have sequenced and assembled a high quality reference genome and generated a wide characterisation of the genes that are expressed in Cloeon tissues and developmental stages. Using these datasets, we compared sex-specific gene expression in nymphal heads, with a special focus on genes of the highly conserved network that controls the formation of the eye in multiple groups of animals, to show how the elements of this network have evolved to play a role in the origin of this dimorphic organ. Finally, we tested functionally the role of some of these components in the development of the turbanate eye during nymphal stages, demonstrating their role in the development of the turbanate eye in males.
These findings have been presented in several national and international scientific meetings, and talks to the general public and they will be publicly available after the publication of the results in high impact factor journals as open access manuscripts
Despite their fundamental role in the diversification of animals, the genetic basis of the origin of new morphological structures during evolution is still poorly understood. EvoNovo has greatly contributed to the understanding of this evolutionary processes by characterising the regulatory networks that have changed in order to generate a complete new visual system in the males of the C. dipterum mayfly. These findings have greatly improved our understanding of the genetic events leading to the appearance of evolutionary novelties.
To gain these new insights we have generated during this project multiple resources, tools and datasets that will be of great help to the scientific community. This includes the establishment of this mayfly as a model system, functional tools and the generation of gene expression and genomic datasets that will have a broad impact to other researchers in future comparative studies.
Furthermore, the dissemination efforts carried out during the project have increased the current awareness of the importance of evolutionary studies and basic research among the general public.
In conclusion, EvoNovo will boost the formulation of new hypotheses, ideas and new research lines in the evodevo, genomics and developmental biology fields.
Graphical abstract