A central goal of biology is to uncover the genetic basis for the origin of new phenotypes. A particularly effective approach is to examine the genomic architecture of species that have secondarily lost a phenotype with respect to their close relatives. In the eusocial Hymenoptera, queens and workers have divergent phenotypes that may be produced via either expression of alternative sets of caste-specific genes and pathways or differences in expression patterns of a shared set of multifunctional genes. To distinguish between these two hypotheses, we investigated how secondary loss of the worker phenotype in workerless ant social parasites impacted genome evolution across two independent origins of social parasitism in the ant genera Pogonomyrmex and Vollenhovia. We sequenced the genomes of three social parasites and their most-closely related eusocial host species and compared gene losses in social parasites with gene expression differences between host queens and workers. Virtually all annotated genes were expressed to some degree in both castes of the host, with most shifting in queen-worker bias across developmental stages. As a result, despite >1 My of divergence from the last common ancestor that had workers, the social parasites showed strikingly little evidence of gene loss, damaging mutations, or shifts in selection regime resulting from loss of the worker caste. This suggests that regulatory changes within a multifunctional genome, rather than sequence differences, have played a predominant role in the evolution of social parasitism, and perhaps also in the many gains and losses of phenotypes in the social insects.

Sex determination mechanisms play a central role in life-history characteristics, affecting mating systems, sex ratios, inbreeding tolerance, etc. Downstream components of sex determination pathways are highly conserved, but upstream components evolve rapidly. Evolutionary dynamics of sex determination remain poorly understood, particularly because mechanisms appear so diverse. Here we investigate the origins and evolution of complementary sex determination (CSD) in ants and bees. The honey bee has a well-characterized CSD locus, containing tandemly arranged homologs of the transformer gene [complementary sex determiner (csd) and feminizer (fem)]. Such tandem paralogs appear frequently in aculeate hymenopteran genomes. However, only comparative genomic, but not functional, data support a broader role for csd/fem in sex determination, and whether species other than the honey bee use this pathway remains controversial. Here we used a backcross to test whether csd/fem acts as a CSD locus in an ant (Vollenhovia emeryi). After sequencing and assembling the genome, we computed a linkage map, and conducted a quantitative trait locus (QTL) analysis of diploid male production using 68 diploid males and 171 workers. We found two QTLs on separate linkage groups (CsdQTL1 and CsdQTL2) that jointly explained 98.0% of the phenotypic variance. CsdQTL1 included two tandem transformer homologs. These data support the prediction that the same CSD mechanism has indeed been conserved for over 100 million years. CsdQTL2 had no similarity to CsdQTL1 and included a 236-kb region with no obvious CSD gene candidates, making it impossible to conclusively characterize it using our data. The sequence of this locus was conserved in at least one other ant genome that diverged >75 million years ago. By applying QTL analysis to ants for the first time, we support the hypothesis that elements of hymenopteran CSD are ancient, but also show that more remains to be learned about the diversity of CSD mechanisms.

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In the major eusocial species of Hymenoptera, the regulatory mechanisms controlling queen/worker differentiation and exclusive reproduction by queens have been studied extensively. These studies have shown that insulin/insulin‐like growth factors and juvenile hormones (JHs) act as key endocrine factors. However, although considerable knowledge has accumulated in this area, large disparities in the regulatory mechanisms governing caste differentiation have been observed in different hymenopteran taxa to date. We focused on the queenless ant Pristomyrmex punctatus (Hymenoptera: Formicidae), which exhibits the simplest type of sociality and in which reproductive tasks (egg production) are distributed among morphologically and genetically identical workers. To elucidate the molecular mechanisms underlying reproduction in P. punctatus, we analyzed the correlations between the gene expression profiles of a reproductive marker gene, vitellogenin (PripuVTG1), and candidate regulatory genes comprising the major components of the JH and insulin/insulin‐like growth factor signaling pathways that are involved in the regulation of reproduction upstream of JH signaling. Expression of insulin‐like peptide 1 (PripuILP1) and JH signaling‐related genes was negatively correlated with PripuVTG1 expression. On the contrary, insulin‐like peptide 2 (PripuILP2a) was positively correlated with PripuVTG1. These findings suggest that an equilibrium perhaps controlled by switches in JH signaling exists between these two ILP paralogs, and that these interactions are important for regulating reproduction. Our findings are expected to be useful for understanding how various modes of sociality have evolved in insects.