Functional constraints on insect immune system components govern their evolutionary trajectories

The role of constraints in shaping evolutionary outcomes is often investigated in the contexts of developmental biology and population genetics, in terms of the capacity to generate new variants as well as how selection either limits or promotes consequent phenotypic change. Comparative genomics also recognises the role of constraints, in terms of shaping the evolution of gene and genome architectures, sequence evolutionary rates, and gene gains and losses, as well as on molecular phenotypes. Characterising patterns of genomic change where putative functions and interactions of system components are relatively well-described offers opportunities to explore whether genes with similar or analogous roles exhibit similar evolutionary trajectories, possibly governed by common constraints. Using insect innate immunity as our study system, we hypothesise that quantitative characterisation of gene evolutionary histories can define distinct dynamics associated with different functional roles. We develop metrics that quantify gene evolutionary histories, employ these to characterise evolutionary features of immune gene repertoires, and explore relationships between gene family evolutionary profiles and their roles in immunity to understand how different constraints may relate to distinct dynamics. We identified three main axes of evolutionary trajectories characterised by gene duplication and synteny, maintenance/stability and sequence conservation, and loss and sequence divergence, highlighting similar and contrasting patterns across these axes amongst subsets of immune genes. Our results indicate that where and how genes participate in immune responses limit the range of possible evolutionary scenarios they exhibit. Comparative genomics approaches therefore offer opportunities to characterise how functional constraints on different components of biological systems govern their evolutionary trajectories.