Genome-wide gene birth-death dynamics are associated with diet breadth variation in Lepidoptera

Abstract

Comparative analyses of gene birth-death dynamics (GBDD) have the potential to reveal gene families that played an important role in the evolution of morphological, behavioral, or physiological variation. Here, we used whole genomes of 30 species of butterflies and moths to identify GBDD among the Lepidoptera that are associated with specialist or generalist feeding strategies. Our work advances this field by using a uniform set of annotated proteins for all genomes, investigating associations while correcting for phylogeny, and assessing all gene familes rather than a priori subsets. We discovered that the sizes of several important gene families (e.g., those associated with pesticide resistance, xenobiotic detoxification, and/or protein digestion) are significantly correlated with diet breadth. We also found 12 gene families showing significant shifts in GBDD at the butterfly (Papilionoidea) crown node, the most notable of which was a family of pheromone receptors that underwent a contraction potentially linked with a shift to visual-based mate recognition. Our findings highlight the importance of uniform annotations, phylogenetic corrections and unbiased gene family analyses in generating a list of candidate genes that warrant further exploration. Significance StatementGene duplications and gene deaths are important for the development of novel traits, but their study is often complicated by methodological issues, such as input data coming from different sources with different biases. Here, we address many of these issues in an analysis of gene duplication and death across 30 species of moths by using standardized, genome-wide input data. Importantly, our analysis uses a model that can correlate gene family sizes with any quantitative trait, while also accounting for relatedness between species. Using this model, we provide novel evolutionary insights by showing that the sizes of several important gene families are correlated with increases or decreases in the number of host plant orders that Lepidoptera eat.