Multi-Omic Analysis Reveals Population Differentiation and Signatures of Social Evolution in Tetragonula Stingless Bees.

Abstract

Stingless bees in the genus Tetragonula are social insects with a fully sterile worker caste, and are therefore well-placed to provide insights into the genomic changes associated with 'superorganismal' life histories. Here we assemble the genome of Tetragonula carbonaria and characterise the population structure and divergence of both T. carbonaria and its cryptic congener T. hockingsi in eastern Australia, revealing three distinct populations for T. carbonaria and two partially differentiated subpopulations for T. hockingsi. We then combine our genomic results with RNA-seq data from different T. carbonaria castes (queens, males, workers) to test two hypotheses about genomic adaptations in social insects: the 'Relaxed Constraint' hypothesis, which predicts indirect, and therefore relaxed, selection on worker-biased genes; and the 'Adapted Worker' hypothesis, which predicts intensified positive selection on worker genes due to their evolutionarily novel functions. Although we do not find a direct signal of either weaker purifying selection or elevated positive selection in worker-biased genes based on deviations from neutral expectations of nucleotide change between the two species, other evidence does support a model of relaxed selection on worker-biased genes: such genes show higher nucleotide diversity and greater interspecies divergence than queen-biased genes. We also find that differentially caste-biased genes exhibit distinct patterns of length, GC content and evolutionary origin. These findings, which converge with patterns found in other social insects, support the hypothesis that social evolution produces distinct signatures in the genome. Overall, Tetragonula bees emerge as a valuable model for studying the genomic basis of social complexity in insects.