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Water-walking insects: marrying evo-devo with ecology for a better understanding of morphological evolution

Final Report Summary - WATERWALKING (Water-walking insects: marrying evo-devo with ecology for a better understanding of morphological evolution)

Understanding the origin of the remarkable biodiversity in nature is an important goal in biological studies. Despite recent advances in evolutionary developmental biology, our understanding of the interaction between developmental genetic processes and the ecological environment in shaping the phenotype remains largely fragmented. The WaterWalking project combines original natural systems, water-walking insects, with state-of-the-art tools of functional and developmental genetics, to study the interplay between developmental genetic pathways and the ecological environment, and how this interaction can shape adaptive phenotypic change. About 200 million years ago, the common ancestor of water-walking insects (Heteroptera, Gerromorpha) invaded water surface and radiated into a diverse array of niches, from shorelines to open oceans. This ecological transition and specialization are associated with an array of adaptive changes that enabled these insects to support their body weight and generate efficient propulsion on the water surface. A characteristic morphology in waters striders is the reversal in relative leg length whereby second legs are longer than the third, a situation that is unusual for an insect. Water striders use their second legs as propellers and third legs as rudders during water surface locomotion. We have shown that this adaptive morphology evolved through changes in the dose of expression and the function of a conserved developmental gene called Ubx. Low dose of Ubx makes the second legs longer and high dose makes the third legs shorter, thus generating the typical morphology of water striders. This dos-dependent role of Ubx does not apply to other insects and demonstrates how diversity can arise through subtle changes in developmental programs. We also have shown the emergence of a new interaction network involving Ubx and immune system genes. This interaction helped shape a morphology that is critical for predator avoidance in water striders. We have also demonstrated that the remarkable diversity in water-walking insects was facilitated by their ability to generate fast movements on water. This increased speed evolved through the combined action of behavioral and morphological phenotypes, and allowed the group to exploit various water surface habitats. Some water habitat, such as fast running streams, impose a challenging environment on locomotion performance. We found that this type of challenging habitat was invaded by a group of species, called Rhagovelia, through the evolution of a novel structure known as the propelling fan. This fan enables the animals to cope with current and its development and evolution has been possible through two taxon-restricted genes we named geisha and mother-of-geisha. This work provides a comprehensive understanding of how the interaction between developmental genetic mechanisms and the selective environment can drive diversification.