Life underwater: uncovering the genetic drivers of adaptation to aquatic lifestyles in insects

Insects have evolved from living on land to living in freshwater on more than 50 independent occasions. These habitat transitions facilitated a burst of biodiversity, such that insects now comprise 80% of all freshwater life and are crucial for proper functioning of freshwater ecosystems. Despite their incredible diversity and ecological importance, we know little about the genetic, developmental, and physiological innovations required for the terrestrial-aquatic transition, a fundamental repeated lifestyle change across insects. This knowledge gap exists because, until recently, genomic resources for aquatic insects were restricted to vector species (e.g. mosquitoes). The huge expansion of genomic data – associated principally with the Darwin Tree of Life project – now enables us to approach this question for the first time. Within the project, each UK and Irish eukaryote species is being sequenced to deliver high quality genomes. This project is developing a huge, but still largely untapped, resource for comparative genomics analysis and forms the basis of greater exploration of the link between molecular evolution and organism adaptation. With these new data, I can now examine how genomes of aquatic and closely related terrestrial lineages differ. Further, because each habitat transition event will have required adaptations to overcome common environmental pressures (e.g. respiration, osmoregulation), the genetic signatures of convergent evolution – independent adaptive solutions to the same environmental problem – will reveal the basis of adaptation in freshwater lineages. Investigations into how aquatic insects have evolved are timely given that freshwater habitats, and the species that occupy them, are increasingly recognized as the most threatened on Earth. The aim of this study is to determine and functionally examine the genetic elements which permitted terrestrial to aquatic habitat transitions across insect evolution. To achieve this, I will combine field sampling with comparative genomics, transcriptomics, and functional genomics to delineate the genes involved in insect adaptation to a new environment. The three objectives are as follows: (1) Determine shared signatures of adaptation associated with transition to aquatic environments across all insects. I will use large scale comparative genomics and bioinformatic methods to interrogate genomic data of terrestrial/freshwater pairs of genomes for patterns of genome change common to freshwater lineages, relative to their terrestrial counterparts. (2) Evaluate the contribution of gene expression changes associated with the transition to aquatic life. Here, I will construct a multi-species transcriptome dataset of larval and adult life stages of wild specimens from closely related terrestrial and aquatic species belonging to three insect orders (Diptera, Trichoptera, and Lepidoptera). (3) Enable functional analysis through establishing a new, genetically tractable lab model. I will develop the common dronefly, Eristalis tenax (family Syrphidae), which has aquatic larvae and terrestrial adults. A new model system of an aquatic insect will permit functional genetic testing of loci found in the previous objectives to be associated with adaptation to life in freshwater key for onward advances in this field. This project will, for the first time, pinpoint the genes and patterns of molecular evolution underpinning adaptation to the freshwater environment. In addition to addressing a general and common change in life mode, this baseline understanding of the genetics underpinning adaptation of terrestrial taxa to life in freshwater will help us to determine how they may, or may not, adapt to future changing environmental conditions.