Genomic innovations underlying the evolution of termite sociality

• Applicants: Dr. Mark C. Harrison; Professor Dr. Dino McMahon
• Subject Area: Evolution, Anthropology
• Term: from 2020 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 433073542

Increased accuracy and yield of long-read sequencing technologies in combination with emerging molecular methods are now able to deliver highly polished genomes at viable economic cost. This project takes advantage of these very recent developments to build a foundation for insect genomic research, with the primary aim of gaining new insights into a major milestone in evolution: the emergence of sociality. Outside of the well-studied social Hymenoptera (bees, ants and wasps) such advanced levels of eusociality have evolved just once: in the termites. Understanding termite evolution is therefore of exceptional interest: both as an important group in basic and applied research, but also as a comparative system to Hymenoptera. The transition to sociality that exists across the termite phylogeny is a powerful framework for understanding the genomic changes behind this evolutionary milestone. Our recent findings have shed some light by revealing adaptive changes in termite gene families and genomes. But despite these efforts, the molecular basis of this major transition remains largely unresolved. Lack of progress is in large part attributable to the absence of coordinated support for large-scale next generation sequencing. We aim to close this gap by targeting missing data from key cockroach and termite species spanning the transition from a cockroach-like ancestor to higher termites. These groups are critical because they reflect important ecological and evolutionary diversity that has hitherto been overlooked. The first objective of our project is therefore to sequence, assemble and annotate platinum-grade genomes of eight cockroach and termite species. We will then use these data to complete two further objectives: i) investigate the molecular mechanisms underpinning the evolution of termite eusociality, and ii) elucidate the evolutionary origins of termite castes. A major hypothesis we test is that termite sociality occurred via a two-step process involving an initial expansion of genomic elements in cockroaches, followed by extensive genome rearrangements in termites. We then test the exciting hypothesis that transposons facilitated this process through the generation of genomic novelty, by applying a quantitative and systematic analysis of transposon-host gene associations across cockroach and termite genomes. This explicitly requires making use of cutting-edge genomic techniques. Finally, we will combine genomes with high-resolution transcriptomics to explore the mechanistic basis of termite phenotypic plasticity, and thereby understand the evolutionary origins of termite social castes. Our overall goal is to sequence and analyze eight new platinum-grade cockroach and termite genomes, which together with existing data, will allow us to make comparisons of species across the main trajectories of termite social complexity. This will ultimately enable us to answer the overarching question: what are the molecular origins of termite sociality?

• DFG Programme: Research Grants